\r\n\tThis book aims to explore the issues around the rheology of polymers, with an emphasis on biopolymers as well as the modification of polymers using reactive extrusion.
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1. Introduction
Alzheimer\'s disease (AD) is the most common cause of dementia in the elderly and is characterized by progressive memory loss leading to a gradual and irreversible deterioration of cognitive function. The neuropathology of AD is characterized by the accumulation of fibrillary lesions in the form of neuritic plaques (NPs, Fig. 1A), neurofibrillary tangles (NFTs, Fig. 1C,D; small arrow) and dystrophic neurites (DNs, Fig. 1; arrows) in neocortex, amygdala and hippocampus [1]. The density of the NPs and NFTs correlate with the degree of dementia in AD [2]. The accumulation of these lesions does not occur at random; the presence of NFTs is associated with vulnerability of the perforant pathway [3]. NPs are comprised of extracellular deposits of amyloid-β peptide fibrils that are associated with DNs of dendritic and axonal origin (Fig. 1A; arrows). Intracellular NFTs selectively kill neurons in specific brain areas. In AD, the distribution of NFTs follows a stereotypical profile arising first in layer II of the entorhinal cortex, hippocampal region and CA1/subicular layer IV of the entorhinal cortex and then neocortex (mainly in fronto-temporal and parietal areas). This pattern of distribution was first described by Braak and Braak in 1991 [4], and provides the most important neuropathological criteria for a definite diagnosis of AD (Fig. 2) [5]. Ultrastructurally, NFTs are composed of dense accumulations of structures known as paired helical filaments (PHFs) [6, 7], which are mainly distributed in the perinuclear area of the neuron and in proximal processes (Fig. 1C). Tau protein is the major structural constituent of the PHF subunits [7-9]. Normally, tau protein exists as a family of microtubule-associated protein (MAPs) that are found predominantly in axons. Through repeated domains located toward the carboxy-terminus of the protein, tau provides stability to the microtubule and this process can be regulated through a balance in the phosphorylation/dephosphorylation process of tau protein [10]. In AD, tau protein accumulates as PHFs in the somatodendritic compartment, with consequent destabilization of axonal microtubules. Tau is further post-translationally in AD, with modifications of ubiquitination [11, 12], glycation [13, 14], glycosylation [15], nitration [16], polyamination [17], hyperphosphorylation [18, 19] and proteolysis [7, 20-24]. The latter two changes occur throughout the tau molecule [25-27].
Figure 1.
Neuropathological hallmarks of Alzheimer´s disease. Double labelling with tau antibody (green channel) counterstained with thiazine red (red channel). A) A classical neuritic plaquein which an amyloid fibrillar plaque (Aβ), recognized by thiazine red, is associated with dystrophic neurites (arrows). B). Pre-tangle cells are characterized by diffuse granular deposits throughout the perinuclear area (small arrow) and proximal processes. C) A neurofibrillary tangle that is strongly labeled by tau antibody and colocalized with tiazine red. (A,B) projection of 20 and 9 confocal microscopy sections, respectively, each of 1.0 μm thickness.
Figure 2.
Braak stages of AD neuropathology base on the pattern of neurofibrillary change (NFT, Neuropil threads and plaques dystrofic neurites) [4], Although clinic-pathological correlations were not made, Braak and Braak did speculate that the entorhinal stage (I-II) represents clinically silent periods of the disease with NFT involvement confined to trans-entorhinal layer pre-alpha. Limbic stages (III/IV) correspond with clinically incipient AD, and NFT involvement of CA1, and neocortical stages (V/VI) represent fully developed AD, with NFT involvement of all areas of association cortex.
Tau protein can be phosphorylated at multiple sites. While there is evidence that phosphorylation of tau protein promotes its assembly into PHFs [18, 19, 28, 29], the role of phosphorylation in the genesis of PHFs has been limited to the analysis of "mature", intracellular NFTs (NFT-I). By this stage in the disease, tau protein will have been affected by many different pathological processes, several of which may be associated with the hyperphosphorylation process [25, 26, 30].
Another post-translational modification found in AD is the proteolytic truncation of the C-terminal portion of tau protein [7, 20, 21, 23, 31, 32]. It has been proposed that such truncation unlike hyperphosphorylation, favours polymerisation of tau [33, 34][35].
In recent years, evidence from both in vitro and in vivo studies[36, 37], suggests that hyperphosphorylation of tau protein has a protective role. In this review, we analyze the protective effects of hyperphosphorylated species of tau protein and their relationship to toxicity, and the participation of truncated species of tau in the formation of PHFs.
2. Tau protein
The cytoskeleton is formed by three types of filaments: microfilaments, intermediate filaments and microtubules [38]. The cytoskeleton provides a dynamic scaffold to proteins, vesicles and organelles, essential for proper cell function and changes in the state of its polymerization, play an important role in neuronal process such as polarization, axonal transport, maintenance of neuronal extensions, synaptic plasticity and protein sorting [39]. Tau protein functions as a regulator of microtubule assembly [40]. Tau protein participates in microtubule polymerization [41], regulation of axonal diameter [42], regulation of axonal transport [43], neurogenesis and the establishment of neuronal polarity in development [44]. Furthermore, tau participates in the regulation of signaling pathways by acting as a protein scaffold.
The gene that encodes for tau consists of 16 exons and is located at the chromosomal locus 17q21 [45]. Through alternative splicing, six tau isoforms are generated in the CNS, varying from 352-441 amino acids in length (Fig. 3). Tau protein can be divided into three domains: an acidic region in the N-terminal projection, a proline-rich domain and a microtubule-binding domain (Fig. 4) [46]. The alternative transcription of exons 2, 3 and 10 modifies the presence of repeats in the N-terminus of tau (0-2N) and the number of microtubule-binding repeat domains (3R or 4R), respectively.
3. Tau protein metabolism
The MAPT (tau) gene is transcribed mainly in neurons and a promoter that confers neuronal specificity has been described [47]. It has been reported that the presence of a tau promoter lacking neuronal specificity might account for the expression of tau in peripheral tissue [48]. In both cases, sequences containing binding sites for transcription factors AP2 and Sp1 were described. Whereas tau protein synthesis is unaffected by microtubule polymerization or depolymerization, degradation of tau is stimulated by microtubule depolymerization [49].
Figure 3.
Schematic representation of the human MAPT (tau) gene, the primary tau transcript and the six CNS tau protein isoforms. The MAPT gene is located over 100kb of the long arm of chromosome 17 at position 17q21. It contains 16 exons, with exon −1 is a part of the promoter (upper panel). The tau primary transcript contains 13 exons. Exons −1 and 14 are transcribed but not translated. Exons 1, 4, 5, 7, 9, 11, 12, 13 are constitutive, and exons 2, 3, and 10 are alternatively spliced, giving rise to six different mRNAs, translated in six different CNS tau isoforms (lower panel). These isoforms differ by the absence or presence of one or two N-terminal inserts of 29 amino acids encoded by exon 2 (yellow box) and 3 (green box), in combination with either three (R1, R3 and R4) or four (R1–R4) C-terminal repeat-regions (black boxes). The additional microtubule-binding domain is encoded by exon 10 (pink box) (lower panel). Adult tau includes all six tau isoforms, including the largest isoform of 441-amino acids containing all inserts and other isoforms as indicated. The shortest 352-amino acids isoform is the only one found only in fetal brain.
Figure 4.
Schematic representation of the functional domains of the largest tau isoform (441 amino acids). The projection domain, including an acidic and a proline-rich region, interacts with cytoskeletal elements to determine the spacing between microtubules in axons. The N-terminal part is also involved in signal transduction pathways by interacting with proteins such as PLC-γ and Src-kinases. The C-terminal part, referred to as the microtubule-binding domain, regulates the rate of microtubules polymerization and is involved in binding with functional proteins such as protein phosphatase 2A (PP2A) or presenilin 1(PS1).
It is technically difficult to determine the half life of the different tau isoforms and several factors may regulate tau degradation such as, for example, the extent of phosphorylation and acetylation of tau (see below). The half life of tau decreases in rats by neonatal period P20 and there is less demand for tau in non-dividing, mature neurons [50].
Two main mechanisms for tau protein degradation have been documented: 1) the proteasomal ubiquitin pathway and 2) the lysosomal autophagic pathway. Proteasomal degradation of tau protein has been described by 20S proteasomal processing [51], although there have also been reports suggesting that tau is not normally degraded by the proteasome [52]. Tau, modified by phosphorylation, can be ubiquitinated by the CHIP-hsc70 complex and degraded by the proteasome [53]. Furthermore, acetylation of tau can regulate its proteasomal degradation by modifying those lysine residues needed for ubiquitination. In this way, acetylation of tau inhibits its degradation through a competition between ubiquitination and acetylation [54].
On the other hand, tau may get processed through a lysosomal autophagic mechanism. It has been reported that tau can be degraded by lysosomal proteases [55] and, more recently, it was shown that tau fragmentation and clearance can occur by lysosomal processing [56].
Tau protein is a microtubule-associated protein. It’s mostly abundant in neurons in the Central Nervous System (CNS). The main function of Tau protein is to interact with tubulin to stabilize microtubules and promote tubulin assembly into microtubules. Tau protein controls microtubule stability in two different ways : isoforms and phosphorylation.
Normally, the tau protein is very important, as it manages the transport of materials within soma and other cellular regions through the myelin sheaths. Once it spotted something suspicious or irrelevant, it stops the information sending process automatically. However, in Alzheimer’s disease, the tau proteins started to perform uncommon reaction, where it transmitting the information to the brain simultaneously, regardless of its validity.
Once the above problem happening, it causes the brain overloading with information and might lead to inflammation, clumps or tangles, which kill most of the brain cells (Fig. 5).
4. Phosphporylation of tau protein
Protein phosphorylation is the addition of a phosphate group, by esterification, to one of three different amino acids: serine, threonine and tyrosine. Phosphorylation is the most common post-translational modification of tau described and increased tau phosphorylation reduces its affinity for microtubules leading to cytoskeletal destabilization. Eighty-five putative phosphorylation sites on tau protein have been described in AD brain tissue (Fig. 6). The formation of fibrillar aggregates of post-translationally modified tau protein in the brain are characteristic of AD and other tauopathies. The phosphorylation of tau protein affects its solubility, localization, function, interaction with partners and susceptibility to other post-translational modifications. However, the role of specific sites of tau phosphorylation in early neurodegenerative mechanisms is unknown. The molecular mechanisms of aggregation of tau into insoluble forms may help to account for the different dementias in which both clinical symptoms and age of onset differ.
Figure 5.
tau protein, which forms part of a microtubule. The microtubule helps transpot nutrients and other important substances from one part of the nerve cells to another. Axon are long threadlike extensions that conduct nerve impulses away from the nerve cells; dendrites are short branched threadlike extensions that conduct nerve impulses toward the verve cell body. In Alzheimer´s disease the tau protein is abnormal and the microtubule structures collapse.
5. C-terminal truncation of tau protein in AD
5.1. PHF-core concept
In 1988, Wischik et al, [7, 22] identified tau protein as the major constituent of Pronase-resistant PHFs and tau was characterized by a specific C-terminal truncation of the protein at Glu-391. This truncation is identified by the monoclonal antibody (mAb) 423 [23, 31], and the acid-reversible occlusion of the intact core tau domain. PHFs are labeled by the fluorescent dye, thiazin-red, a dye which can be used to differentiate between amorphous and fibrillar states of tau and amyloid proteins in AD. The minimum tau fragment in the PHF [20, 24] corresponds to the tandem repeat region in the C-terminal domain of tau protein, a species having a molecular weight of 12.5 kDa. Characteristically, this fragment is highly stable to proteolysis, insoluble and toxic and is referred to as PHF-core tau [22, 57, 58]. PHF-core tau and mAb 423 immunoreactivity of NFTs, have a close clinical-pathological relationship; the density of NFTs immunolabelled with mAb 423 is correlated with the progression of neurofibrilary pathology, as determined by Braak staging criteria (Fig. 2). Most significantly, there is a correlation between mAb 423 immunoreactivity and both clinical severity and progression to dementia [3]. On the other hand, over-expression of PHF-core tau, in cell culture, favors a programmed cell death or apoptosis, which shows that it is highly toxic[59]. Recombinant tau protein truncated at Glu-391 also shows increased rates of polymerization compared with recombinant full-length tau. From confocal microscopy studies, it has been shown that this fragment of tau is hidden within the PHF-core and exposed by formic acid treatment [57]. In the cytoplasm of susceptible neurons, this truncated tau triggers an autocatalytic process in which the fragment has a high affinity for full length tau and, once bound, leads to cycles of proteolysis and further tau binding to form a proto-filament [60]. In this scenario, the initiating tau species that gave rise to the filament is hidden within a large number of covering tau molecules, some of which become hyperphosphorylated. This would correspond to the early aggregation of tau protein associated with PHF in small NFT. Tau molecules of the NFT would become exposed on death of the neuron to reveal the extracellular NFT, or "ghost tangle" (Fig. 1D, small arrow) which shares the properties of being stable, insoluble and immunoreactive with mAb 423 [57, 61]. The proteases responsible for truncation at Glu-391 are not known.
Figure 6.
Location of tau phosphorylation sites and epitopes for tau antibodies. Multiple amino acids are phosphorylated with some those observed in AD brain [5], normal brain (green) and both normal and AD brains (blue). Putative phosphorylation sites that have not yet been demonstrated in vitro or in vivo (black). Localization of antibody epitopes are indicated arrows. Residues are numbered according to the longest tau isoform.
6. Truncation of tau protein at Asp-421
In 2003, a second truncation of tau protein was found to be associated with PHFs [62-65]. This truncation is found at position Asp-421 in the C-terminus of the tau molecule and its presence can be detected specifically by using mAb TauC-3[25, 63]. Unlike truncation at Glu-391, for which the protease responsible is unknown, caspase-3 (an enzyme involved in the apoptotic pathway) is responsible for the truncation at Asp-421 in vitro [59, 62, 63]. This suggests that cleavage of the carboxyl terminus of tau protein, could result as a neuronal response to prevent or control the polymerization of tau in PHF [58]. In 2005, Binder and colleagues discovered a truncation at the amino terminus of the tau protein associated with PHFs. This cut corresponds to Asp-13, which is produced by caspase-6, another enzyme involved in the apoptotic pathway [66]. An antibody to detect this cleavage site of the amino terminus of tau protein has not yet been generated.
Tau-C3 has an affinity for NFTs, NDs and neuropil threads in AD brains. Immunohistochemical studies indicated that truncation at Asp-421 occurs after conformational change; the antibody binds with greatest affinity when the amino terminus of tau molecule contacts the third microtubule binding repeat (MTBR), as recognized by mAb Alz-50 [26]. However, other studies have shown Tau-C3 immunoreactivity in pre-tangle cells before they become Alz-50 immunoreactive and in the absence of PHFs [64, 67].
7. Impact of phosphorylation and truncation on the abnormal processing of tau protein in AD
7.1. A neuroprotective mechanism for the phosphorylation of tau protein in the AD brain
During neurodegeneration in AD, tau protein is abnormally phosphorylated in the proline-rich region at Ser and Thr residues [68], and such phosphorylation sites can be identified using highly specific antibodies such as: AT8 (Ser-202/Thr-205) AT100 (Ser-212 and Ser-214), TG3 (Thr-231/Ser-235) and PHF-1 (Ser-396/Ser-404), among others (Fig. 6). However, NFTs are found in viable neurons at late stages of the disease, and they persist in neuronal cells for decades with a significant number of NFTs being found in the cognitively intact elderly [69, 70]. Such NFT-bearing neurons contain normal content and structure of microtubules [68]. The findings from studies in transgenic mice and human data, suggest that tau accumulation in the somatodendritic compartment may represent the manifestation of a protective mechanism or a cellular adaptation that arises with advancing age. An increase in tau phosphorylation in AD brain has been associated with a protective mechanism against oxidative stress [71]. In another study, intact microtubules were found in NFT-bearing neurons [8], calling into question whether accumulation of phosphorylated tau and destabilization of microtubules are necessarily linked. Although microtubules are depolymerized in neurons with fibrillary degeneration, one study found evidence that the reduction of microtubules in AD is marked and specifically limited to vulnerable pyramidal neurons, and that even these alterations were observed in the absence of PHF [72]. This finding is also consistent with previous work by one of the authors noting a microtubule decrease of nearly 50% in dendrites that did not correlate with either PHFs or age [73], suggesting that a proportion of phosphorylated tau protein is associated with microtubules [71]. In animal models, it has been confirmed that axonal transport is not affected by either over-expression or reduction of tau protein in vivo [42, 74]. Another study found evidence that axonopathy precedes the formation of NFTs in a transgenic mouse [75]. A transgenic mouse expressing a human tau isoform developed NFTs, neuronal loss and behavioral impairments [58]. After suppression of tau expression, the behavioral deficits stabilized yet NFTs continued to accumulate, suggesting that NFTs are not sufficient to cause cognitive decline or neuronal death.
Within NFTs, different species of tau protein associated with phosphorylation are observed, but the neurodegenerating neurons still appear to be functional [75]. These observations suggest that the cytoplasmic accumulation of hyperphosphorylated tau protein is non-toxic, similar to the accumulation of lipofuscin that does not alter cellular metabolism[68]. It is generally assumed that disintegration of microtubules is associated with an imbalance between kinase and phosphatase activities, which lead to an alteration in the stability of microtubules, disruption of cell function and culminate in neuronal death. The data, however, suggest that, at least, a subpopulation of hyperphosphorylated NFTs may be not toxic. This is controversial, given the fact that the hyperphosphorylation of tau and NFTs are considered to be toxic. However, the ability of tau protein fractions, purified from AD brains, to alter microtubule assembly, in vitro, has been attributed to sequestration of normal tau molecules [18]. Alonso and colleagues [28] demonstrated that recombinant hyperphosphorylated tau, in vitro, decreases the breakdown of the recombinant microtubule when assembled into small aggregates [19, 28]. On this basis, the authors suggested that hyperphosphorylated tau protein plays a protective role against the disintegration of the microtubule.
Tau that has been hyperphosphorylated with GSK3-β kinase becomes immunoreactive with mAbs AT8, PHF1 and TG-3, antibodies whose epitopes are very closely related to AD [29, 76]. The fact that GSK3-β is capable of creating epitopes considered pathological in AD suggests that there are other participants that require to be considered. These data suggest the possible existence of a toxic species of non-phosphorylated tau protein, which would be responsible for capturing further molecules of tau in PHFs, yet would not be exposed on the filament [7, 57, 61]. It is possible that, by hiding the toxic form in PHFs could protect the neuron [77]. It is important to note that the presumed "intermediaries" are present in the cytoplasm of the neuron when it is still viable. Another study showed that NFTs (and presumably tau oligomers) could remain in the cytoplasm of the neuron for decades [78], an observation that would further argue against a primary toxicity of phosphorylated tau protein in AD.
7.2. Hyperphosphorylation of tau protein protecting neurons from apoptosis
It is also proposed that apoptosis plays an important role in neuronal damage in AD. This proposal is based on the detection of fragmented DNA and expression of apoptosis signaling proteins such as caspases 3, 6, 8 and 9, Bax, Fas and Fas-L, in the cortex and hippocampus, in postmortem brain tissue [79, 80] and observations that amyloid-β can induce neuronal apoptosis [81]. Apoptosis is a process that usually occurs over a period of hours, whereas the accumulation of tangles found in AD brains occurs over a period of years or decades [78]. It has been suggested that hyperphosphorylation of tau protein is a mechanism used to evade cell death by apoptosis. Cells over-expressing hyperphosphorylated tau appear to avoid the apoptotic process [82].
8. Participation of hyperphosphorylated and truncated tau species in the early formation of PHFs
8.1. Model for the mechanism of assembly
Despite suggestions of a neuroprotective role for tau protein in AD, links between phosphorylated species (that are presumed to be protective) and the complex assembly of toxic, truncated tau into insoluble PHFs is not clear. In recent years, we have characterized the early stages of tau protein processing in neurons (pre-tangle state) (Fig. 1B, small arrows) and have described accumulations of tau that possess pathological species present in NFT, yet which do not show the presence of assembled structures in PHFs [67, 83]. The pre-tangle (Fig. 1B) is the first step in non-fibrillar aggregation of tau protein in AD and one in which at least 5 different changes take place (Fig 1 C,D). These events include: a) the presence of a C-terminally truncated and toxic tau species (Glu-391); b) a cascade of specific phosphorylation of tau protein in the N-terminus; c) C-terminal truncation via the action of caspase-3; d) oligomerization and aggregation of tau species and e) assembly of tau into PHFs.
A model to accommodate the observations are represented schematically in Fig. 7. In this model, the first event to occur would be the emergence of tau oligomers or a PHF subunit (Fig. 7 A,B). The mechanism whereby this is initiated is unknown, but its toxicity and high affinity for binding to intact tau molecules would trigger an immediate need for the cell to protect itself. That would be reflected by hyperphosphorylation of the molecule in a failed attempt to hide the PHF and prevent the capture of further intact tau molecules (Fig. 7 B,C). In AD, this protective function of the phosphorylated species favors more molecules becoming available for sequestration and formation into PHFs (Fig. 7D). Gradually, phosphorylated tau will be affected by exogenous proteolysis to re-expose the PHF-core (Fig. 7E). These steps follow as a molecular consequence of the catastrophic fragmentation of the microtubule, synaptic dysfunction, oxidative stress and post-translational modifications of tau. This model emphasizes that polymerization and neuroprotective mechanisms are both involved in the development of PHFs. The phosphorylated species of tau protein play a role in the initial protective response of the neuron to prevent the assembly of these filaments [35]. Thus NFTs, in which externally available tau is hyperphosphorylated, represents a mechanism whereby the neuron may try to protect itself from neurofibrillary degeneration and further studies to confirm this hypothesis are warranted.
Figure 7.
Scheme illustrating the early steps of aggregation and polymerization of tau protein in Alzheimer´s disease. (A) The model starts with the appearance of PHF-core tau in cytoplasm of susceptible neurons. (B) The high binding capacity of PHF-tau results in the assembly of dimers of PHF-core and intact tau molecules in the cytoplasm. (C) The phosphorylation of intact tau would be an early event to hide the toxic soluble aggregates of molecules. (D). The high affinity and stability of the proto-filaments that make up the mature intracellular NFT allows tau molecules to form PHFs. (E) With the death of the neuron, the PHF-core subunit becomes exposed again in the extracellular space following proteolysis. Further details are described in the text.
Acknowledgments
Authors express their gratitude to the Mexican families for the donation of brain tissue from their beloved and without which these studies would not be possible. Amparo Viramontes Pintos for the handling of brain tissue.This work was financially supported by CONACyT grants, No. 142293 (to B.F.).
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Meraz-Ríos and Benjamin Floran-Garduño",authors:[{id:"26577",title:"Dr.",name:"Jesús",middleName:null,surname:"Avila",fullName:"Jesús Avila",slug:"jesus-avila",email:"javila@cbm.uam.es",position:null,institution:null},{id:"42225",title:"Dr.",name:"Jose",middleName:null,surname:"Luna-Muñoz",fullName:"Jose Luna-Muñoz",slug:"jose-luna-munoz",email:"jluna@fisio.cinvestav.mx",position:"Reseach",institution:null},{id:"42226",title:"Dr.",name:"Raul",middleName:null,surname:"Mena-López",fullName:"Raul Mena-López",slug:"raul-mena-lopez",email:"rmena@fisio.cinvestav.mx",position:null,institution:null},{id:"158873",title:"Prof.",name:"Charles",middleName:null,surname:"R. Harrington",fullName:"Charles R. Harrington",slug:"charles-r.-harrington",email:"c.harrington@abdn.ac.uk",position:null,institution:null},{id:"158874",title:"Prof.",name:"Claude",middleName:null,surname:"M. Wischik",fullName:"Claude M. Wischik",slug:"claude-m.-wischik",email:"c.m.wischik@abdn.ac.uk",position:null,institution:null},{id:"158877",title:"Dr.",name:"Paola",middleName:null,surname:"Flores-Rodríguez",fullName:"Paola Flores-Rodríguez",slug:"paola-flores-rodriguez",email:"drapaoflogon@hotmail.com",position:null,institution:null},{id:"158879",title:"Dr.",name:"Sergio",middleName:null,surname:"Zamudio R.",fullName:"Sergio Zamudio R.",slug:"sergio-zamudio-r.",email:"zrzamudio@hotmail.com",position:null,institution:null},{id:"158880",title:"Dr.",name:"Fidel",middleName:null,surname:"De La Cruz",fullName:"Fidel De La Cruz",slug:"fidel-de-la-cruz",email:"flacruz90@hotmail.com",position:null,institution:null},{id:"158882",title:"Dr.",name:"Benjamín",middleName:null,surname:"Florán-Garduño",fullName:"Benjamín Florán-Garduño",slug:"benjamin-floran-garduno",email:"bfloran@fisio.cinvestav.mx",position:null,institution:null}],sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Tau protein",level:"1"},{id:"sec_3",title:"3. Tau protein metabolism",level:"1"},{id:"sec_4",title:"4. Phosphporylation of tau protein",level:"1"},{id:"sec_5",title:"5. C-terminal truncation of tau protein in AD",level:"1"},{id:"sec_5_2",title:"5.1. PHF-core concept",level:"2"},{id:"sec_7",title:"6. Truncation of tau protein at Asp-421",level:"1"},{id:"sec_8",title:"7. Impact of phosphorylation and truncation on the abnormal processing of tau protein in AD",level:"1"},{id:"sec_8_2",title:"7.1. A neuroprotective mechanism for the phosphorylation of tau protein in the AD brain",level:"2"},{id:"sec_9_2",title:"7.2. Hyperphosphorylation of tau protein protecting neurons from apoptosis",level:"2"},{id:"sec_11",title:"8. Participation of hyperphosphorylated and truncated tau species in the early formation of PHFs",level:"1"},{id:"sec_11_2",title:"8.1. Model for the mechanism of assembly",level:"2"},{id:"sec_13",title:"Acknowledgments",level:"1"},{id:"sec_13",title:"Acknowledgments",level:"2"}],chapterReferences:[{id:"B1",body:'Arnold, S.E., et al., The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer\'s disease. Cerebral cortex, 1991. 1(1): p. 103-16.'},{id:"B2",body:'Arriagada, P.V., et al., Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer\'s disease. Neurology, 1992. 42(3 Pt 1): p. 631-9.'},{id:"B3",body:'Garcia-Sierra, F., et al., The extent of neurofibrillary pathology in perforant pathway neurons is the key determinant of dementia in the very old. Acta Neuropathol, 2000. 100(1): p. 29-35.'},{id:"B4",body:'Braak, H. and E. Braak, Neuropathological stageing of Alzheimer-related changes. 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J Neuropathol Exp Neurol, 1999. 58(2): p. 188-97.'},{id:"B79",body:'Guo, H., et al., Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer\'s disease. Am J Pathol, 2004. 165(2): p. 523-31.'},{id:"B80",body:'Lassmann, H., et al., Cell death in Alzheimer\'s disease evaluated by DNA fragmentation in situ. Acta Neuropathol, 1995. 89(1): p. 35-41.'},{id:"B81",body:'Kudo, W., et al., Inhibition of Bax protects neuronal cells from oligomeric Abeta neurotoxicity. Cell death & disease, 2012. 3: p. e309.'},{id:"B82",body:'Li, H.L., et al., Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer\'s neurodegeneration. Proc Natl Acad Sci U S A, 2007. 104(9): p. 3591-6.'},{id:"B83",body:'Luna-Munoz, J., et al., Regional conformational change involving phosphorylation of tau protein at the Thr231, precedes the structural change detected by Alz-50 antibody in Alzheimer\'s disease. J Alzheimers Dis, 2005. 8(1): p. 29-41.'}],footnotes:[],contributors:[{corresp:null,contributorFullName:"José Luna-Muñoz",address:null,affiliation:'
Departments of Physiology, Biophysics and Neurosciences, National Laboratory of experimental services (LaNSE), CINVESTAV-IPN, Mexico
'},{corresp:null,contributorFullName:"Charles R. Harrington",address:null,affiliation:'
Division of Applied Health Sciences, School of Medicine and Dentistry, University of Aberdeen, USA
'},{corresp:null,contributorFullName:"Claude M. Wischik",address:null,affiliation:'
Division of Applied Health Sciences, School of Medicine and Dentistry, University of Aberdeen, USA
Departments of Physiology, Biophysics and Neurosciences, National Laboratory of experimental services (LaNSE), CINVESTAV-IPN, Mexico
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Sánchez López.",slug:"angelica-l.-sanchez-lopez."},{id:"173293",title:"MSc.",name:"Dhea",middleName:null,surname:"Nuño-Penilla",fullName:"Dhea Nuño-Penilla",slug:"dhea-nuno-penilla"},{id:"173294",title:"MSc.",name:"Lorenzo",middleName:null,surname:"Sánchez-Romero",fullName:"Lorenzo Sánchez-Romero",slug:"lorenzo-sanchez-romero"},{id:"173295",title:"Dr.",name:"Mario",middleName:null,surname:"Mireles-Ramírez",fullName:"Mario Mireles-Ramírez",slug:"mario-mireles-ramirez"},{id:"173377",title:"Dr.",name:"J Luis",middleName:null,surname:"Flores-Alvarado",fullName:"J Luis Flores-Alvarado",slug:"j-luis-flores-alvarado"}]},{id:"48055",title:"Gait Pathway in Subcortical Vascular Dementia and in Alzheimer’s Disease",slug:"gait-pathway-in-subcortical-vascular-dementia-and-in-alzheimer-s-disease",signatures:"Rita Moretti, Arianna Sartori, Beatrice Baso and Silvia Gazzin",authors:[{id:"31246",title:"Dr.",name:"Rita",middleName:null,surname:"Moretti",fullName:"Rita Moretti",slug:"rita-moretti"}]},{id:"47690",title:"The Alzheimer’s Patient in the Emergency Department — Specificities of Care",slug:"the-alzheimer-s-patient-in-the-emergency-department-specificities-of-care",signatures:"De Breucker Sandra, Pepersack Thierry and Bier Jean-Christophe",authors:[{id:"25946",title:"Dr.",name:"Jean-Christophe",middleName:null,surname:"Bier",fullName:"Jean-Christophe Bier",slug:"jean-christophe-bier"},{id:"172269",title:"Dr.",name:"Sandra",middleName:null,surname:"De Breucker",fullName:"Sandra De Breucker",slug:"sandra-de-breucker"}]},{id:"48138",title:"Uncontrolled Sexual Behaviour in Dementia",slug:"uncontrolled-sexual-behaviour-in-dementia",signatures:"Susan van Hooren and Wim Waterink",authors:[{id:"33952",title:"Dr.",name:"Susan",middleName:null,surname:"van Hooren",fullName:"Susan van Hooren",slug:"susan-van-hooren"},{id:"36164",title:"Mr.",name:"Wim",middleName:null,surname:"Waterink",fullName:"Wim Waterink",slug:"wim-waterink"}]}]}]},onlineFirst:{chapter:{type:"chapter",id:"62303",title:"Modified Titanium Dioxide for Photocatalytic Applications",doi:"10.5772/intechopen.79374",slug:"modified-titanium-dioxide-for-photocatalytic-applications",body:'\n
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1. Introduction
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The rapid growth of global population as well as industrialization has led to a concomitant increase in environmental pollution. This has very negative effects on natural elements that are vital for life on earth such as air and water. It becomes very crucial therefore to find sustainable ways to mitigate pollution in order to provide a clean and safe environment for humans. Photocatalysis has attracted worldwide interest due to its potential to use solar energy not only to solve environmental problems but also provide a renewable and sustainable energy source. An efficient photocatalyst converts solar energy into chemical energy which can be used for environmental and energy applications such as water treatment, air purification, self-cleaning surfaces, hydrogen production by water cleavage and CO2 conversion to hydrocarbon fuels.
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Research in the development of efficient photocatalytic materials has seen significant progress in the last 2 decades with a large number of research papers published every year. Improvements in the performance of photocatalytic materials have been largely correlated with advances in nanotechnology. Of many materials that have been studied for photocatalysis, titanium dioxide (TiO2; titania) has been extensively researched because it possesses may merits such as high photocatalytic activity, excellent physical and chemical stability, low cost, non-corrosive, nontoxicity and high availability [1, 2, 3, 4]. The photocatalytic activity of titania depends on its phase. It exists in three crystalline phases; the anatase, rutile and brookite. The anatase phase is metastable and has a higher photocatalytic activity, while the rutile phase is more chemically stable but less active. Some titania with a mixture of both anatase and rutile phases exhibit higher activities compared to pure anatase and rutile phases [5, 6, 7]. When titania is irradiated with light of sufficient energy, electrons from the valence band are promoted to the conduction band, leaving an electron deficiency or hole, h+, in the valence band and an excess of negative charge in the conduction band. The free electrons in the conduction band are good reducing agents while the resultant holes in the valence band are strong oxidizing agents and can both participate in redox reactions.
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Titania however suffers from a number of drawbacks that limit its practical applications in photocatalysis. Firstly, the photogenerated electrons and holes coexist in the titania particle and the probability of their recombination is high. This leads to low rates of the desired chemical transformations with respect to the absorbed light energy [8, 9]. The relatively large band gap energy (~ 3.2 eV) requires ultraviolet light for photoactivation, resulting in a very low efficiency in utilizing solar light. UV light accounts for only about 5% of the solar spectrum compared to visible light (45%) [1, 10]. In addition to these, because titania is non-porous and has a polar surface, it exhibits low absorption ability for non-polar organic pollutants [10, 11, 12, 13]. There is also the challenge to recover nano-sized titania particles from treated water in regards to both economic and safety concern [14]. The TiO2 nanoparticles also suffer from aggregation and agglomeration which affect the photoactivity as well as light absorption [15, 16, 17, 18]. Several strategies have been employed in the open literature to overcome these drawbacks. These strategies aim at extending the wavelength of photoactivation of TiO2 into the visible region of the spectrum thereby increasing the utilization of solar energy; preventing the electron/hole pair recombination and thus allowing more charge carriers to successfully diffuse to the surface; increasing the absorption affinity of TiO2 towards organic pollutants as well as preventing the aggregation and agglomeration of the nano-titania particles while easing their recovery from treated water. Several reviews have been published in recent years on the development of strategies to eliminate the limitations of titania photocatalysis [1, 19, 20, 21, 22, 23, 24, 25]. Most of these however focus on pollutant removal from wastewater, water splitting for hydrogen production, CO2 conversion and reaction mechanisms [1, 21, 25, 26, 27, 28, 29, 30, 31]. In this chapter, we review some of the latest publications mainly covering the last 5 years, on strategies that have been researched to overcome the limitations of TiO2 for general photocatalytic applications and the level of success that these strategies have been able to achieve. Based on the current level of research in this field, we also present some perspectives on the future of modified TiO2 photocatalysis.
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2. Modification of TiO2 photocatalysts
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A large number of research works have been published on TiO2 modification to enhance its photocatalytic properties. These modifications have been done in many different ways which include metal and non-metal doping, dye sensitization, surface modification, fabrication of composites with other materials and immobilization and stabilization on support structures. The properties of modified TiO2 are always intrinsically different from the pure TiO2 with regards to light absorption, charge separation, adsorption of organic pollutants, stabilization of the TiO2 particles and ease of separation of TiO2 particles.
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2.1. Metal doping
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Metal doping has been extensively used to advance efforts at developing modified TiO2 photocatalysts to operate efficiently under visible light. The photoactivity of metal-doped TiO2 photocatalysts depends to a large extent on the nature of the dopant ion and its nature, its level, the method used in the doping, the type of TiO2 used as well as the reaction for which the catalyst is used and the reaction conditions [32]. The mechanism of the lowering of the band gap energy of TiO2 with metal doping is shown in Figure 1. It is believed that doping TiO2 with metals results in an overlap of the Ti 3d orbitals with the d levels of the metals causing a shift in the absorption spectrum to longer wavelengths which in turn favours the use of visible light to photoactivate the TiO2.
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Figure 1.
Band-gap lowering mechanism of metal-doped TiO2.
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Doping of TiO2 nanoparticles with Li, Na, Mg, Fe and Co by high energy ball milling with the metal nitrates was found to widen the TiO2 visible light response range. In the Na-doped sample, Ti existed as both Ti4+ and Ti3+ and the conversion between Ti4+ and Ti3+ was found to prevent the recombination of electrons and (e−) and holes (h+). The metal ion doping promoted crystal phase transformations that generated electrons (e−) and holes (h+) [33]. Mesoporous TiO2 prepared by sol gel technique and doped with different levels of Pt (1–5 wt% nominal loading) resulted in a high surface area TiO2 with an enhanced catalytic performance in photocatalytic water splitting for the Pt-doped samples. The 2.5 wt%Pt-TiO2 had showed the optimum catalytic performance and a reduction in the TiO2 band gap energy from 3.00 to 2.34 eV with an enhanced electron storage capacity, leading to a minimization of the electron-hole recombination rate [34]. Noble metal nanoparticles such as Ag [35], Pt [34], Pd [36], Rh [37] and Au [38] have also been used to modify TiO2 for photocatalysis and have been reported to efficiently hinder electron-hole recombination due to the resulting Schottky barrier at the metal-TiO2 interface. The noble metal nanoparticles act as a mediator in storing and transporting photogenerated electrons from the surface of TiO2 to an acceptor. The photocatalytic activity increases as the charge carriers recombination rate is decreased.
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In a recent review by Low et al. [21] the deposition of Au onto TiO2 surface is reported to result in electron transfer from photo-excited Au particles (> 420 nm) to the conduction band of TiO2, which showed a decrease in their absorption band (∼550 nm) and the band was recovered by the addition of electron donors such as Fe2+ and alcohols. Zhang et al. [39] reported that the visible light activity of coupled Au/TiO2 can be ascribed to the electric field enhancement near the metal nanoparticles. Moreover, numerous researchers coupled Au and Ag nanoparticles onto TiO2 surface to use their properties of localized surface plasmonic resonance (LSPR) in photocatalysis [40]. Wang et al. [41] and Hu et al. [42] reported an improved photocatalytic performance due to the Pt nanoparticle which increased the electron transfer rate to the oxidant. It was observed that photocatalytic sacrificial hydrogen generation was influenced by several parameters such as platinum loading (wt%) on TiO2, solution pH, and light (UV, visible and solar) intensities [43]. Moreover, complete discoloration and dye mineralization were achieved using Pt/TiO2 as catalyst; the results were attributed to the higher Pt content of the photocatalyst prepared with the highest deposition time. For Pt-TiO2 catalysts the best discoloration and dye mineralization were obtained over the catalyst prepared by photochemical deposition method and using 120 min of deposition time in the synthesis. These results may be due to the higher Pt content of the photocatalyst prepared with the highest deposition time.
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Haung et al. [44] prepared Pt/TiO2 nanoparticles from TiO2 prepared at various hydrolysis pH values and found that the phase of TiO2 obtained depended largely on the hydrolysis pH. The anatase/rutile intersection of a Pt/TiO2 sample had a lower recombination rate compared to the anatase phase of Pt/TiO2 due to the longer recombination pathway. Though, the Pt/TiO2 anatase phase showed better degradation efficiency than the Pt/TiO2 anatase/rutile intersection. The decrease in the anatase composition of TiO2, and the decrease in the composition of TiO2 resulted in the degradation rate decrease, suggesting that anatase composition in the Pt/TiO2 system played a crucial role of increasing the photocatalytic degradation of Acid Red 1 dye.
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Liu et al. [45] prepared the palladium doped TiO2 (Pd-TiO2) photocatalyst using chemical reduction method and tested it the photocatalytic degradation of organic pollutant. It was found that the TiO2 grain size was reduced while the specific surface area increased and the absorption of ultraviolet light also enhanced after using chemical reduction method, however, all these changes had no effect on degradation of organic pollutant. But the degradation was significantly improved due to the deposition of Pd nanoparticles; the Pd/TiO2 organic pollutant degradation was 7.3 times higher compared to TiO2 (P25).
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Repouse et al. [46] prepared a series of noble metal promoted TiO2 (P25) by wet impregnation and found that the dispersion of the small metal crystallites on TiO2 did not affect the optical band gap of TiO2. The Pt-promoted catalyst exhibited the highest photocatalytic efficiency in the degradation of bisphenol A under solar irradiation. They also found the presence of humic acid to considerably improve the reaction rate of Rh/TiO2 but had a clearly adverse effect with P25 TiO2 photocatalyst. Fluorescence data revealed that humic acid is capable of photosensitizing the Rh/TiO2 catalyst.
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Indium-doped TiO2 have recently been used for photocatalytic reduction of CO2 [47]. Indium doping resulted in an increase in surface area because of suppression of TiO2 particle growth during the TiO2 synthesis. The light absorption ability of the In-TiO2 was enhanced due to the introduction of the impurity level below the conduction band level of the TiO2. The photocatalytic CO2 reduction activity of the In-TiO2 was about 8 time that of pure TiO2 as a consequence of the high surface area and extended light absorption range.
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The doping of TiO2 with transition metals such as Cr [48], Co [48], Fe [48, 49, 50], Ni [48, 51], Mn [48, 52], V [53], Cu [54], Ni [51] and Zn [55], has been studied by different research groups. Numerous studies reported that doping of TiO2 with transition metals improve the photocatalytic activity, attributable to a change in the electronic structure resulting in the absorption region being shifted from UV to visible light. The shift results from charge-transfer transition between the d electrons of the transition metals and the conduct or valence band of TiO2 nanoparticles. Inturi et al. [48] compared the doping of TiO2 nanoparticles with Cr, Fe, V, Mn, Mo, Ce, Co, Cu, Ni, Y and Zr and it was found that Cr, Fe and V showed improved conversions in the visible region while, the incorporation of the other transition metals (Mn, Mo, Ce, Co, Cu, Ni, Y and Zr) exhibited an inhibition effect on the photocatalytic activity. The Cr-doped TiO2 demonstrated a superior catalytic performance and the rate constant was found to be approximately 8–19 times higher than the rest of the metal doped catalysts. It was reported that the reduction peaks in Cr-doped TiO2 shifted to much lower temperatures, due to the increase in the reduction potential of titania and chromium. Therefore, the higher photocatalytic efficiency of Cr/TiO2 in the visible light can be attributed to strong interaction (formation of Cr-O-Ti bonds). Fe-doped TiO2 nanoparticles were used in the visible light degradation of para-nitrophenol and it was found that the Fe-dopant concentration was crucially important in determining the activity of the catalyst. The maximum degradation rate of para-nitrophenol observed was 92% in 5 h when the Fe(3+) molar concentration was 0.05 mol%, without addition of any oxidizing reagents. The excellent photocatalytic activity was as a result of an increase in the threshold wavelength response as well as maximum separation of photogenerated charge carriers [49]. On the other hand, Fe-doped TiO2 evaluated for solar photocatalytic activity for the degradation of humic acid showed a retardation effect for the doped catalysts compared to the bare TiO2 specimens, which could be attributed to surface complexation reactions rather than the reactions taking place in aqueous medium. The faster removal rates attained by using bare TiO2 could be regarded as substrate specific rather than being related to the inefficient visible light activated catalytic performance [50]. Ola et al. [56] reported that the properties of V doped TiO2 were tuned towards visible light because of the substitution of the Ti4+ by V4+ or V5+ ions since the V4+ is centred at 770 nm while the absorption band of V5+ is lower than 570 nm. Moradi et al. [57] obtained high photocatalytic activity of Fe doped TiO2 and studied the effects of Fe3+ doping content on the band gap and size of the nanoparticles. It was found that the increase in the doping content decreased the band gap energy and particle size from 3.3 eV and 13 nm for bare TiO2 to 2.9 eV and 5 nm for Fe10-TiO2, respectively.
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The rare earth metals doped TiO2 catalyst also have good electron trapping properties which can result in a stronger absorption edge shift towards longer wavelength, obtaining narrow band gap. Bethanabotla et al. [58] carried out a comprehensive study on the rare earth doping into a TiO2 and found that the rare earth dopants improved the aqueous-phase photodegradation of phenol at low loadings under simulated solar irradiation, with improvements varying by catalyst composition. Differences in defect chemistry on key kinetic steps were given as the explanation for the enhanced performance of the rare earth doped samples compared to pure titania. Reszczyńska et al. [59] prepared a series of Y3+, Pr3+, Er3+ and Eu3+ modified TiO2 nanoparticles photocatalysts and results demonstrate that the incorporation of RE3+ ions into TiO2 nanoparticles resulted in blue shift of absorption edges of TiO2 nanoparticles and could be ascribed to movement of conduction band edge above the first excited state of RE3+. Moreover, incorporated RE3+ ions at the first excited state interact with the electrons of the conduction band of TiO2, resulting in a higher energy transfer from the TiO2 to RE3+ ions. But observed blue shift could be also attributed to decrease in crystallite size of RE3+–TiO2 in comparison to TiO2. The Y3+, Pr3+, Er3+ and Eu3+ modified TiO2 nanoparticles exhibited higher activity under visible light irradiation compared to pure P25 TiO2 and can be excited under visible light in the range from 420 to 450 nm. In a similar work on rare earths (Er, Yb, Ho, Tb, Gd and Pr) titania nanotubes (RE-NTs), [60] the RE3+ species were found to be located at the crystal boundaries rather than inside the TiO2 unit cell and an observed excitation into the TiO2 absorption band with resulting RE3+ emission confirmed energy migration between the TiO2 matrix and RE3+. The presence of the rare earth component was found to reduce recombination of the electrons and holes successfully by catching them and also by promoting their rapid development along the surface of TiO2 nanoparticles. Lanthanide ions doping did not impact the energy gap of TiO2 nanoparticles, however this enhanced the light absorption of catalyst. The surface range of TiO2 nanoparticles generally increases by La3+ particle doping by diminishing the crystallite size and accordingly, the doped TiO2 nanoparticle displayed higher adsorption capacity. Based on theoretical calculations, it was proposed that during the electrochemical process, new Ho-f states and surface vacancies were formed and may reduce the photon excitation energy from the valence to the conduction band under visible light irradiation. The photocatalytic activity under visible light irradiation was attributed not to ·OH but to other forms of reactive oxygen species (O2·−, HO2, H2O2).
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2.2. Non-metal doping
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TiO2 nanoparticles have been comprehensively doped at the O sites with non-metals such as C [61], B [62], I [63], F [64], S [65], and N [66]. Non-metal dopants are reported to be more appropriate for the extension of the photocatalytic activity of TiO2 into visible region compared to metal dopant [67, 68]. This can be ascribed to the impurity states which are near the valence band edge, however, they do not act as charge carriers, and their role as recombination centres might be minimized [53]. As shown in Figure 2, the mixing of the p states of the doped non-metal with the O2p states shifts the valence band edge upward and narrows the band-gap energy of the doped TiO2 photocatalyst. The nitrogen and carbon doped TiO2 nanoparticles has been reported to exhibit greater photocatalytic activity under visible light irradiation compared to other non-metal dopants.
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Figure 2.
Band-gap energy narrowing mechanism for non-metal-doped TiO2.
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N-doped TiO2 (N-TiO2) appears to be the most efficient and extensively investigated photocatalyst for non-metal doping. Zeng et al. [69] reported the preparation of a highly active modified N-TiO2 nanoparticle via a novel modular calcination method. The excellent photocatalytic performance of the photocatalyst was ascribed to excellent crystallinity, strong light harvesting and fast separation of photogenerated carriers. Moreover, the enhancement of charge separation was attributed to the formation of paramagnetic [O-Ti4+-N2−-Ti4+-VO] cluster. The surface oxygen vacancy induced by vacuum treatment trapped electron and promoted to generate super oxygen anion radical which was a necessary active species in photocatalytic process. Phongamwong et al. [70] investigated the photocatalytic activity of CO2 reduction under visible light over modified N-TiO2 photocatalyst and they have found that the band gap of N-TiO2 photocatalyst slightly decreases with increasing N content. In addition, the sub-band energies related to the impurity energy level were observed in the N-TiO2 photocatalyst because of the interstitial N species and the sub-band gap energies were found to have decreased from 2.18 eV with 10 wt% N-TiO2 photocatalyst. In contrast, the replacement of O by N is difficult because of the radius of N (17.1 nm) being higher compared to O (14 nm) and the electroneutrality can be maintained by oxygen vacancies, that are provided by replacement of three oxygen vacancies by two nitrogen atom [71]. N-TiO2 photocatalyst reduces the oxygen energy vacancies from 4.2 to 0.6 eV, suggesting that N favors the formation of oxygen vacancies [72].
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In contrast, O atoms (14 nm) could be substituted easily by F atoms (13.3 nm) because of their similar ionic radius [73]. Yu et al. [64] reported that the F-doped TiO2 (F-TiO2) is able to absorb visible light due to the high-density states that were evaluated to be below the maxima valence band, although there was no shift in the band edge of TiO2. Samsudin et al. found a synergistic effect between fluorine and hydrogen in hydrogenated F-doped TiO2 which enabled light absorption in UV, visible and infrared light illumination with enhanced electrons and holes separation. Surface vacancies and Ti3+ centres of the hydrogenated F-doped catalyst coupled with enhanced surface hydrophilicity facilitated the production of surface-bound and free hydroxyl radicals. Species present on the surface of the catalyst triggered the formation of new Ti3+ occupied states under the conduction band of the hydrogenated F-doped TiO2, thus narrowing the band gap energy [73]. Enhanced photocatalytic performance of N-doped TiO2 over pure TiO2 has also been ascribed to efficient separation of electron-hole pairs as well as an increased creation of surface radicals such as hydroxyl The band gap can also be narrowed by doping TiO2 with S, since replacement of S into TiO2 can be performed easily due to larger radius of S atoms (18 nm) compared to O atoms (14 nm). S incorporation in TiO2 has been reported to change the lattice spacing of the TiO2 with a reduction in the band gap width from 3.2 to 1.7 eV allowing for higher photocatalytic activity [74]. N, S and C co-doped TiO2 samples photocatalytic reduction of Cr(IV) showed that the co-doping and calcination played an important role in the microstructure and photocatalytic activity of the catalysts. The co-doped samples calcined at 500°C showed the highest activities ascribed to the synergistic effect in enhancing crystallization of anatase and (N, S and C) co-doping. The carbon doped TiO2 (C-TiO2) is reported to be more active than N-TiO2, therefore, C-TiO2 has received special attention [75]. Noorimotlagh et al. [76] investigated the photocatalytic removal of nonylphenol (NP) compound using visible light active C-TiO2 with anatase/rutile. It was found that the doping of C into TiO2 lattice may enhance the visible light utilization and affect the structural properties of the as-synthesized photocatalysts. Moreover, it was reported that after C doping and changing the calcination temperature, the band gap was narrowed from 3.17 to 2.72 eV and from 2.72 to 2.66 eV, respectively. Ji et al. [61] reported the preparation of C-TiO2 with a diameter of around 200 nm and the tube wall was composed of anatase TiO2, amorphous carbon, crystalline carbon and carbon element doping into the lattice of TiO2. The C-TiO2 nanotubes exhibited much better performance in photocatalytic activity than bare TiO2 under UV and visible light. The obtained results were ascribed to the C doping, which narrowed the band gap energy of TiO2, extended the visible light adsorption toward longer wavelength and hindered charge recombination.
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2.3. Co-doping and tri-doping
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Although single metal doped and non-metal doped TiO2 have exhibited excellent performance in decreasing the electrons and holes recombination, but they suffer from thermal stability and losing a number of dopants during catalyst preparation process [77]. Therefore, co-doping of two kinds of atoms into TiO2 has recently attracted much interest [78]. The electronic structure of TiO2 can be altered by co-doping on TiO2 by formation of new doping levels inside its band gap. Abdullah et al. [77] reported that the doping levels situated within the band gap of TiO2 can either accept photogenerated electrons from TiO2 valence band or absorb photons with longer wavelengths. Therefore, suggesting that the TiO2 absorption range can be expanded.
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Zang et al. [79] evaluated the photocatalytic degradation of atrazine under UV and visible light irradiation by N,F-codoped TiO2 nanowires and nanoparticles in aqueous phase. It was found that photocatalytic degradation of atrazine was higher in the presence of N,F-codoped TiO2 nanowires than that of N,F-codoped TiO2 nanoparticles. The higher photocatalytic performance in the presence of N,F-codoped TiO2 nanowires was attributed to the higher charge carrier mobility and lower carrier recombination rate. Moreover, the speed of electron diffusion across nanoparticle intersections is several orders of magnitude smaller compared to that of nanowire because of frequent electron trapping at the intersections of nanoparticles and increasing the recombination of separated charges before they reach the TiO2 nanoparticles surface. Park et al. [80] showed the best performance for novel Cu/N-doped TiO2 photoelectrodes for dye-sensitized solar cells. It was found that the Cu/N-doped TiO2 nanoparticles provided higher surface area, active charge transfer and decreased charge recombination. Moreover, the addition of suitable content of Cu- to N-doped TiO2 electrode effectively inhibited the growth of TiO2 nanoparticles and improved the optical response of the photoelectrode under visible light irradiation. Chatzitakis et al. [81] studied the photoelectrochemical properties of C, N, F codoped TiO2 nanotubes. It was found that increasing surface area is not followed by increase in the photoconversion efficiency, but rather that an optimal balance between electroactive surface area and charge carrier concentration occurs.
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Zhao et al. [82] investigated the photocatalytic H2 evolution performance of Ir-C-N tridoped TiO2 under UV-visible light irradiation. The photocatalytic activity of TiO2 nanoparticles was reported to be improved by Ir-C-N tridoped TiO2 under UV-visible light, due the synergistic effect between Ir, C and N on the electron structure of TiO2. It was found that Ir existed as Ir4+ by substituting Ti in the lattice of TiO2 nanoparticles, whereas the C and N were also incorporated into the surface of TiO2 nanoparticles in interstitial mode. The absorption of TiO2 nanoparticles was expanded into the visible light region and the band gap was narrowed to ~3.0 eV, resulting in improved photocatalytic H2 evolution under UV-visible light irradiation. Tan et al. [83] investigated the photocatalytic degradation of methylene blue by W–Bi–S-tridoped TiO2 nanoparticles. It was found that the absorption edge of TiO2 was expanded into visible-light region after doping with W, Bi and S and the catalytst showed the best photocatalytic activity, than that of TiO2, S-TiO2, W–S–TiO2 and Bi–S–TiO2. This might be attributed to the synergistic effect of W, Bi and S.
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2.4. Nano-structured TiO2
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Amongst the various strategies that have been used to enhance TiO2 photocatalytic activity, improvement of morphology, crystal structure and surface area have also been considered important and widely investigated approach to achieve better photocatalytic performance. The nanotitania crystallinity can simply be enhanced by optimizing the annealing temperature. However, the stability of the structure and geometries have to be considered when annealing [84]. For the nanotitania morphology and surface area, various ordered structures have been studied. TiO2 nanotubes [85, 86], nanowires [79], nanospheres [87], etc. Tang et al. fabricated monodisperse mesoporous anatase TiO2 nanospheres using a template material and found the resulting catalysts to show high photocatalytic degradation efficiency and selectivity towards different target dye molecules and could be readily separated from a slurry system after photocatalytic reaction [87]. Anodic TiO2 nanotubes have been reported to allow a high control over the separation of photogenerated charge carriers in photocatalytic reactions. The nanotube array has as key advantage the fact that nanotube modifications can be embedded site specifically into the tube wall or at defined locations along the tube wall. This allows for engineering of reaction sites giving rise to enhanced photocatalytic efficiencies and selectivities [88].
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2.5. Nanocarbon modified TiO2
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The design and preparation of graphene-based composites containing metal oxides and metal nanoparticles have attracted attention for photocatalytic performances. For example, Tan et al. [89] prepared a novel graphene oxide-doped-oxygen-rich TiO2 (GO–OTiO2) hybrid heterostructure and evaluated its activity for photoreduction of CO2 under the irradiation of low-power energy-saving daylight bulbs. It was found that the photostability of O2–TiO2 was significantly improved by the addition of GO, at which the resulting hybrid composite retained a high reactivity. The photoactivity attained was about 1.6 and 14.0 folds higher than that of bare O2–TiO2 and the commercial Degussa P25, respectively. This high photocatalytic performance of GO–OTiO2 was attributed to the synergistic effect of the visible-light-responsiveness of O2–TiO2 and an enhanced separation and transfer of photogenerated charge carriers at the intimate interface of GO–OTiO2 heterojunctions. This study is reported to have opened up new possibilities in the development of novel, next generation heterojunction photocatalysts for energy and environmental related applications. Lin et al. [90] also investigated photoreduction of CO2 with H2O vapor in the gas-phase under the irradiation of a Xe lamp using TiO2/nitrogen (N) doped reduced graphene oxide (TiO2/NrGO) nanocomposites. They found that the quantity and configuration of N dopant in the TiO2/NrGO nanocomposites strongly influenced the photocatalytic efficiency, and the highest catalytic activity was observed for TiO2/NrGO nanocomposites with the highest N doping content. Moreover, modified TiO2/rGO demonstrated a synergistic effect, enhancing CO2 adsorption on the catalyst surface and promoting photogenerated electron transfer that resulted in a higher CO2 photoreduction rate of TiO2/NrGO. Qu et al. [91] prepared the graphene quantum dots (GQDs) with high quantum yield (about 23.6% at an excitation wavelength of 320 nm) and GQDs/TiO2 nanotubes (GQDs/TiO2 nanoparticles) nanocomposites and the photocatalytic activity was tested towards the degradation of methyl orange. It was found that the GQDs deposited on TiO2 nanoparticles can expand the visible light absorption of TiO2 nanoparticles and enhance the activity on photocatalytic degradation of methyl orange under UV-vis light irradiation (ʎ = 380–780 nm). Furthermore, the photocatalytic activity of GQDs/TiO2 nanoparticles was approximately 2.7 times as higher than that of bare TiO2 nanoparticles. Tian et al. [92] reported the preparation of N, S co-doped graphene quantum dots (N, S-GQDs)-reduced graphene oxide- (rGO)-TiO2 nanotubes (TiO2NT) nanocomposites for photodegradation of methyl orange under visible light irradiation. It was found that the S-GQDs+rGO + TiO2 nanocomposites simultaneously showed an extended photoresponse range, improved charge separation and transportation properties. Moreover, the apparent rate constant of N, S-GQDs+rGO + TiO2NT is 1.8 and 16.3 times higher compared to rGO + TiO2NT and pure TiO2NT, respectively. Suggesting that GQDs can improve the utilization of solar light for energy conversion and environmental therapy.
\n
\n
\n
2.6. Immobilized TiO2
\n
Another drawback of TiO2 nanoparticles mentioned above is the formation of uniform suspension in water which makes its recovery difficult, therefore hindering the application of photocatalytic in an industrial scale. As a result, many studies have attempted the modification of TiO2 nanoparticles on support materials such as clays [93, 94] quartz [95], stainless steel [96], etc. Clays have been reported to be a significant support material for TiO2 nanoparticles because of their layered morphology, chemical as well as mechanical stability, cation exchange capacity, non-toxic nature, low cost and availability. Therefore, TiO2/clay nanocomposites have attracted much attention for application in both water and air purification and have been prepared by numerous researchers. Belver et al. [97] investigated the removal of atrazine under solar light using a novel W-TiO2/clay photocatalysts. It was found that the photocatalytic activity of W-TiO2/clay catalyst exhibited higher photocatalytic performance than that of an un-doped TiO2/clay, which was explained by the presence of W ions in the TiO2 nanostructure. The substitution of Ti ions with W resulted in the increase of its crystal size and the distortion of its lattice and moderately narrower band gap of photocatalysts. Mishra et al. [98] reported the preparation of TiO2/clay nanocomposites for photocatalytic degradation of VOC and dye. They found that the photocatalytic performance of TiO2/clay nanocomposites is highly dependent on the clay texture (as 2:1 clays show highest activity than 1:1) apart from their surface area and porosity. Moreover, the reactions involving TiO2/Clay photocatalyst were fast with rate constant of 0.02886 and 0.04600 min−1 for dye and VOC respectively than the other nanocomposites.
\n
\n
\n
\n
3. Conclusions
\n
In this chapter, we have given an overview of the development of modified TiO2 catalysts and its future prospects from a scientific point of view. We note that the field has experienced major advances in the last 5 years especially in the area of modifying TiO2 with carbon nanomaterials. Based on the literature we have covered here, we believe that there is still quite a lot that can be achieved in improving the performance of TiO2 catalysts for photocatalytic applications.
\n
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Conflict of interest
There are no conflicts of interest to declare.
\n',keywords:"titanium dioxide, photocatalysis, environmental pollution, modification",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/62303.pdf",chapterXML:"https://mts.intechopen.com/source/xml/62303.xml",downloadPdfUrl:"/chapter/pdf-download/62303",previewPdfUrl:"/chapter/pdf-preview/62303",totalDownloads:2524,totalViews:918,totalCrossrefCites:9,dateSubmitted:"March 12th 2018",dateReviewed:"June 7th 2018",datePrePublished:"November 5th 2018",datePublished:"March 6th 2019",dateFinished:null,readingETA:"0",abstract:"Titanium dioxide (TiO2) has been widely used as a photocatalyst in many environmental and energy applications due to its efficient photoactivity, high stability, low cost, and safety to the environment and humans. However, its large band gap energy, ca. 3.2 eV limits its absorption of solar radiation to the UV light range which accounts for only about 5% of the solar spectrum. Furthermore, the photocatalytic activity of TiO2 is also limited by the rapid recombination of the photogenerated electron-hole pairs. When used in water treatment applications, TiO2 has a poor affinity toward organic pollutants, especially hydrophobic organic pollutants. Several strategies have been employed to reduce its band gap energy, its electron-hole recombination rates as well as enhance its absorption of organic pollutants. In this chapter, we review some of the most recent works that have employed the doping, decoration, and structural modification of TiO2 particles for applications in photocatalysis. Additionally, we discuss the effectiveness of these dopants and/or modifiers in enhancing TiO2 photoactivity as well as some perspective on the future of TiO2 photocatalysis.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/62303",risUrl:"/chapter/ris/62303",signatures:"John Moma and Jeffrey Baloyi",book:{id:"7478",title:"Photocatalysts",subtitle:"Applications and Attributes",fullTitle:"Photocatalysts - Applications and Attributes",slug:"photocatalysts-applications-and-attributes",publishedDate:"March 6th 2019",bookSignature:"Sher Bahadar Khan and Kalsoom Akhtar",coverURL:"https://cdn.intechopen.com/books/images_new/7478.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"245468",title:"Dr.",name:"Sher Bahadar",middleName:null,surname:"Khan",slug:"sher-bahadar-khan",fullName:"Sher Bahadar Khan"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:[{id:"250026",title:"Dr.",name:"John",middleName:null,surname:"Moma",fullName:"John Moma",slug:"john-moma",email:"john.moma@wits.ac.za",position:null,institution:null},{id:"250963",title:"Mr.",name:"Jeffrey",middleName:null,surname:"Baloyi",fullName:"Jeffrey Baloyi",slug:"jeffrey-baloyi",email:"jeffreyb@mintek.co.za",position:null,institution:null}],sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Modification of TiO2 photocatalysts",level:"1"},{id:"sec_2_2",title:"2.1. Metal doping",level:"2"},{id:"sec_3_2",title:"2.2. Non-metal doping",level:"2"},{id:"sec_4_2",title:"2.3. Co-doping and tri-doping",level:"2"},{id:"sec_5_2",title:"2.4. Nano-structured TiO2",level:"2"},{id:"sec_6_2",title:"2.5. Nanocarbon modified TiO2",level:"2"},{id:"sec_7_2",title:"2.6. Immobilized TiO2",level:"2"},{id:"sec_9",title:"3. Conclusions",level:"1"},{id:"sec_13",title:"Conflict of interest",level:"1"}],chapterReferences:[{id:"B1",body:'Dong H, Zeng G, Tang L, Fan C, Zhang C, He X. An overview on limitations of TiO2-based particles for photocatalytic degradation of organic pollutants and the corresponding countermeasures. Water Research. 2015;79:128-146\n'},{id:"B2",body:'Jiang L, Wang Y, Feng C. Application of photocatalytic technology in environmental safety. 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Journal of Molecular Catalysis A: Chemical. 2015;406:51-57\n'},{id:"B75",body:'Lei XF, Xue XX, Yang H, Chen C, Li X, Niu MC, et al. Effect of calcination temperature on the structure and visible-light photocatalytic activities of (N, S and C) co-doped TiO2 nano-materials. Applied Surface Science. 2015;332:172-180\n'},{id:"B76",body:'Noorimotlagh Z, Kazeminezhad I, Jaafarzadeh N, Ahmadi M, Ramezani Z, Silva Martinez S. The visible-light photodegradation of nonylphenol in the presence of carbon-doped TiO2 with rutile/anatase ratio coated on GAC: Effect of parameters and degradation mechanism. Journal of Hazardous Materials. 2018;350:108-120\n'},{id:"B77",body:'Abdullah H, Khan MMR, Ong HR, Yaakob Z. Modified TiO 2 photocatalyst for CO 2 photocatalytic reduction: An overview. Journal of CO2 Utilization. 2017;22:15-32\n'},{id:"B78",body:'Jin Q, Nie C, Shen Q, Xu Y, Nie Y. Cobalt and sulfur co-doped TiO2 nanostructures with enhanced photo-response properties for photocatalyst. Functional Materials Letters. 2017;10(05):1750061\n'},{id:"B79",body:'Zhang Y, Han C, Zhang G, Dionysiou DD, Nadagouda MN. PEG-assisted synthesis of crystal TiO2 nanowires with high specific surface area for enhanced photocatalytic degradation of atrazine. Chemical Engineering Journal. 2015;268:170-179\n'},{id:"B80",body:'Park J-Y, Kim C-S, Okuyama K, Lee H-M, Jang H-D, Lee S-E, et al. Copper and nitrogen doping on TiO2 photoelectrodes and their functions in dye-sensitized solar cells. Journal of Power Sources. 2016;306:764-771\n'},{id:"B81",body:'Chatzitakis A, Grandcolas M, Xu K, Mei S, Yang J, Jensen IJT, et al. Assessing the photoelectrochemical properties of C, N, F codoped TiO2 nanotubes of different lengths. Catalysis Today. 2017;287:161-168\n'},{id:"B82",body:'Zhao XG, Huang LQ. Iridium, carbon and nitrogen multiple-doped TiO2 nanoparticles with enhanced photocatalytic activity. Ceramics International. 2017;43(5):3975-3980\n'},{id:"B83",body:'Tan D, Liu Y, Guo W, Wang J, Chang Z, Li D. Synthesis and characterisation of W–Bi–S-tridoped TiO2 nanoparticles with enhanced photocatalytic activity. Materials Science and Technology. 2016;32(16):1673-1677\n'},{id:"B84",body:'Lin J, Liu X, Zhu S, Liu Y, Chen X. Anatase TiO(2) nanotube powder film with high crystallinity for enhanced photocatalytic performance. Nanoscale Research Letters. 2015;10:110\n'},{id:"B85",body:'Podporska-Carroll J, Panaitescu E, Quilty B, Wang L, Menon L, Pillai SC. Antimicrobial properties of highly efficient photocatalytic TiO2 nanotubes. Applied Catalysis B: Environmental. 2015;176-177:70-75\n'},{id:"B86",body:'Weon S, Choi W. TiO2 nanotubes with open channels as deactivation-resistant photocatalyst for the degradation of volatile organic compounds. Environmental Science & Technology. 2016;50(5):2556-2563\n'},{id:"B87",body:'Tang H, Zhang D, Tang G, Ji X, Li C, Yan X, et al. Low temperature synthesis and photocatalytic properties of mesoporous TiO2 nanospheres. Journal of Alloys and Compounds. 2014;591:52-57\n'},{id:"B88",body:'Zhou X, Liu N, Schmuki P. Photocatalysis with TiO2 nanotubes: “Colorful” reactivity and designing site-specific Photocatalytic centers into TiO2 nanotubes. ACS Catalysis. 2017;7(5):3210-3235\n'},{id:"B89",body:'Tan L-L, Ong W-J, Chai S-P, Goh BT, Mohamed AR. Visible-light-active oxygen-rich TiO2 decorated 2D graphene oxide with enhanced photocatalytic activity toward carbon dioxide reduction. Applied Catalysis B: Environmental. 2015;179:160-170\n'},{id:"B90",body:'Lin L-Y, Nie Y, Kavadiya S, Soundappan T, Biswas P. N-doped reduced graphene oxide promoted nano TiO2 as a bifunctional adsorbent/photocatalyst for CO2 photoreduction: Effect of N species. Chemical Engineering Journal. 2017;316:449-460\n'},{id:"B91",body:'Qu A, Xie H, Xu X, Zhang Y, Wen S, Cui Y. High quantum yield graphene quantum dots decorated TiO2 nanotubes for enhancing photocatalytic activity. Applied Surface Science. 2016;375:230-241\n'},{id:"B92",body:'Tian H, Shen K, Hu X, Qiao L, Zheng WN. S co-doped graphene quantum dots-graphene-TiO2 nanotubes composite with enhanced photocatalytic activity. Journal of Alloys and Compounds. 2017;691:369-377\n'},{id:"B93",body:'Mishra A, Mehta A, Sharma M, Basu S. Impact of ag nanoparticles on photomineralization of chlorobenzene by TiO2/bentonite nanocomposite. Journal of Environmental Chemical Engineering. 2017;5(1):644-651\n'},{id:"B94",body:'Seftel EM, Niarchos M, Mitropoulos C, Mertens M, Vansant EF, Cool P. Photocatalytic removal of phenol and methylene-blue in aqueous media using TiO2@ LDH clay nanocomposites. Catalysis Today. 2015;252:120-127\n'},{id:"B95",body:'He Y, Sutton NB, Rijnaarts HHH, Langenhoff AAM. Degradation of pharmaceuticals in wastewater using immobilized TiO2 photocatalysis under simulated solar irradiation. Applied Catalysis B: Environmental. 2016;182:132-141\n'},{id:"B96",body:'Feng D, Xu S, Liu G. Application of immobilized TiO2 photocatalysis to improve the inactivation of Heterosigma akashiwo in ballast water by intense pulsed light. Chemosphere. 2015;125:102-107\n'},{id:"B97",body:'Belver C, Han C, Rodriguez JJ, Dionysiou DD. Innovative W-doped titanium dioxide anchored on clay for photocatalytic removal of atrazine. Catalysis Today. 2017;280:21-28\n'},{id:"B98",body:'Mishra A, Mehta A, Sharma M, Basu S. Enhanced heterogeneous photodegradation of VOC and dye using microwave synthesized TiO2/clay nanocomposites: A comparison study of different type of clays. Journal of Alloys and Compounds. 2017;694:574-580\n'}],footnotes:[],contributors:[{corresp:"yes",contributorFullName:"John Moma",address:"john.moma@wits.ac.za",affiliation:'
School of Chemistry, University of the Witwatersrand, South Africa
School of Chemistry, University of the Witwatersrand, South Africa
Advanced Materials Division, Mintek, South Africa
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It is an intricate malignancy caused by the reciprocity of intrinsically genetic, environmental, and host-related elements. The silent property, advanced clinical characterization, and potential heterogeneity have made GC a thorny disease with a high death rate. The increasing knowledge of the abundant genetic abnormalities regarding GC will definitely elongate the patients’ survival. Scientists have been working hard to discover the myths beneath gastric tumorigenesis: novel biomarkers have been established, and cell transduction cascades have been well described. The study grouping GC into four molecular subtypes by The Cancer Genome Atlas (TCGA) broadens our horizon of GC etiologies. Knowledge regarding to the sophisticated networks in tumor microenvironment also bring new insights into the mechanisms assist GC development. In the future, people will strive for translating more research achievements into clinical utility. 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She is Professor of Internal Medicine & Head of Department Internal Medicine Faculty of Medicine, Helwan University, Egypt.\r\nDr. Gamie has been an author and reviewer in international publications. She is also\r\nMember of Egyptian board of Internal medicine, Examiner In Egyptian fellowship of Internal Medicine, Consultant of Internal Medicine, gastroentrology and hepatology unit, and was in Ministry of Health, United Arab Of Emirate from 2002 till 2012.\r\nDr. Gamie was Member of hypertension and Diabetes Guideline in UAE 2010 and organizer of ultrasound training course (lectures and practical) in Ain Shams University.\r\nHer areas of interest include: ultrasonogrophy, needle guided liver biopsy, color Doppler (for 15 years), musculoskeletal ultrasound. 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OASPA
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OASPA
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STM
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COPE
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Creative Commons
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Crossref
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Crossref is the official Digital Object Identifier (DOI) Registration Agency for scholarly and professional publications with a goal of making scholarly communications more effective. IntechOpen deposits metadata and registers DOIs for all content using the Crossref System. IntechOpen also deposits its references and uses the Crossref Cited-by service that enables researchers to track citation statistics.
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Altmetric and Dimensions from Digital Science
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Digital Science is a technology company serving the needs of scientific and research communities at key points along the full cycle of research. They support innovative businesses and technologies that make all parts of the research process more open, efficient and effective. IntechOpen integrates tools such as Altmetric to enable our researchers to track and measure the activity around their academic research and Dimensions, to ease access to the most relevant information and better understand and analyze the global research landscape.
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CLOCKSS
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CLOCKSS preserves scholarly publications in original formats, ensuring that they always remain available and openly accessible to everyone.
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iThenticate
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Enago
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SPi Global
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Amazon
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DHL
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