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1. Introduction
RNA interference (RNAi) is a conserved gene-regulation mechanism in all eukaryotic cells, where small RNAs including small interfering RNA (siRNA), small hairpin RNA (shRNA), and micro-RNA (miRNA, miR) interact with message RNAs (mRNAs) in a sequence-specific manner and cause the cleavage or translational blockage of a gene [1, 2]. Because of its specificity and efficiency, it has been widely utilized as a routine tool for gene functional studies in biology laboratories worldwide. In addition, since RNAi blockage is very specific and at the transcriptional level, RNAi-based gene therapy (RNAi therapy) is thought to hold a great potential for treating many diseases, especially viral infections and genetic disorders. Synthesized siRNA is thus regarded as a specialized drug for gene therapies. So far, promising results have been obtained with RNAi therapy in various diseases and many are being tested in clinical trials, including viral infections, cancers, and genetic or inflammatory disorders [3-7]. As cancers and other emerging diseases such as dementia and super-bug infections become major public health issues, RNAi therapy can offer a new solution and has the additional ability to overcome drug resistances.
Beside the fundamental gene-silencing and gene-regulating roles of RNAi, which will also regulate the gene functions of immune cells and thus the immune responses, RNAi pathway itself has an additional function and involvement in inducing adaptive immunity. This function has not been well-studied, and the mechanism is not clear. Its relationship with the immune system in terms of antigen reactivation and antigen presentation is still a new area to be investigated. Indeed, in plants and primitive species, RNAi is a part of the defense system against viral infections. However, in mammals, RNAi seems not directly involved in the immune system, probably due to the development of an advanced and sophisticated immune system. This chapter summarizes the evidence of RNAi-induced immunity against tumors and provides some updated possible explanations for the findings. The possible link between miRNA and its degraded products with the immune system has been also discussed. Exploring the relationship between RNAi and the immune system may lead to new discoveries in RNAi biology and approaches for more effective cancer immunotherapy or treatment for viral and intracellular pathogen infections.
2. The discovery of RNAi-induced adaptive immunity against tumors
In 2009, we reported a discovery about RNAi-induced immunity [7]. We investigated two shRNAs encoded by lentiviral vectors on their ability to suppress tumor cell growth and stimulate antitumor immunity in vivo. One shRNA targeted the downstream site of a dominant cytotoxic T lymphocyte (CTL) epitope of the oncogene E7 of human papillomavirus (HPV) type 16 (termed downstream shRNA), while another shRNA targeted the upstream site of this epitope (termed upstream shRNA). Both shRNAs were equally effective at silencing E7 gene expression (in mRNA and protein levels) and led to the inhibition of tumor cells growth in vitro and in vivo [7]. In spite of this, TC1 tumor cells (expressing HPV E6 and E7) treated with downstream shRNA stimulated an immune response against E7 in C57BL6 mice and resulted in elimination of tumor growth in vivo, whereas cells treated with the upstream shRNA did not. When untreated TC1 tumor cells were injected to the same mice (challenging tumors), the group of downstream shRNA exhibited a total inhibition of challenging tumor growth, whereas no inhibition was observed in the upstream shRNA group. This ability of downstream shRNA was absent in Rag-/- mice (lack of T- and B-cells), suggesting adaptive immune response or T-cell response was required. To prove that the immune response was antigen-specific, we carried out a same animal experiment by immunizing C57BL/6 mice with TC-1 cells treated with these shRNAs but challenged with another tumor cell line C2, which has the E7 expression and H-2b genetic background as C57BL/6 mice. Again, we observed that only mice immunized with downstream shRNA treated cells had a loss of tumor formation, indicating tumor clearance was specific to E7. Our data indicate that a more effective treatment can be developed for cervical cancer by combining RNAi treatment with immunotherapy. Our results also reveal that RNAi may be widely used as an antitumor immunity stimulator or enhancer (Fig 1).
Figure 1.
Schematic diagram shows RNAi targeting site and 5\' mRNA fragment. It is known that in cervical cancer HPV E7 and mouse lymphoma EG7/OVA (ovalbumin) models, the shRNA targets the downstream site of the CTL epitope that produce the 5\' fragment of mRNA. This makes immature proteins and further induces an immune response.
To prove the applicability of immune response to general tumor antigens, we tested a model antigen ovalbumin (OVA) expressed in EG7 cells that are a mouse thymoma cell line with C57BL6 genetic background. We chose the major CTL epitope of OVA, SIINFEKL, as the target site and designed two upstream shRNAs OVA-1 and -2 and a downstream shRNA OVA-3. The shRNA-treated EG7 cells were used to immunize the mice, which were subsequently challenged with untreated EG7 cells. We observed that only mice inoculated with OVA-3-shRNA treated cells had significantly reduced tumor formation but not with OVA-1 and -2 shRNAs.
3. Confirmation of mRNA fragments and truncated proteins in treated cells
To determine if the RNAi-induced immune response was actually from degraded products of RNAi, we designed a series of primers that would amplify RNA fragments inside and outside the targeting sites of upstream shRNA (E6-1) and downstream shRNA (E7-1, Fig 2A). If an inside fragment was present while the outside fragment was absent, it would indicate that the mRNA had been cleaved by shRNA at the target site. The cells were treated with E6-1 and E7-1 shRNAs and incubated for 2–4 days before real-time RT-PCR was carried out. As expected, the shortest PCR fragment, R3, was observed in all samples (Fig 2B). The full-length R1 PCR fragment was only observed in untreated TC1 cells or cells infected with the lentiviral vector control (PLL, Fig 2B). In cells treated with both E7-1 and E6-1, R1 was not found, indicating that shRNA-mediated cleavage was occurring. Of most interest was the R2 fragment which was found in all samples except cells treated with E6-1. These results suggest that R2 or R3 short fragments of E6-1 and E7-1 existed in the cells, at least temporarily at the time we isolated RNA. These short-form mRNAs may act as templates for short-form proteins (truncated proteins) and trigger antigen presentation to CD8+ T-cells and a CTL immune response to E7.
Apart from our data, a previous study reported that degradation of the 3\' mRNA fragment resulting from siRNA-mediated cleavage was blocked for some mRNAs, leaving an mRNA fragment that could act as a template for cDNA synthesis. They suggested that this could give rise to false negative results and that this phenomenon may be avoided by the careful design of RT-qPCR primers for each individual siRNA experiment [8]. This report further confirms that mRNA fragments from RNAi do sometimes exist in the cells. In addition, it was noticed by researchers that un-degraded fragments of an siRNA-targeted mRNA may cause false positive effects of microarray analysis [9]. To avoid this, they developed a qRT-PCR protocol, which allowed for the determination of the optimal time point for mRNA analyses, indicating mRNA fragments after RNAi can be present in cell for a certain time.
What is the functional role of these mRNA fragments after RNAi? Our data demonstrated that they can be involved in translational machinery and produce truncated proteins. To experimentally prove this, we utilized the OVA-expressing EG7 cell model again. The cells were treated with downstream and upstream shRNAs and further treated with the protease inhibitor MG132 to reduce protein degradation before immunoblotting was performed. The blots were probed with an antibody against the N terminus of OVA protein. The predicted size of a truncated protein produced by the cleavage of OVA-2 shRNA was 14.7 kDa. We observed a protein band about 15-kDa in cells treated with the OVA-2 shRNA but not in untreated and OVA-1 or OVA-3 shRNA treated cells. It proves that truncated proteins can be produced in cells by the translation of mRNA fragment cleaved by shRNA. The predicted truncated product by shRNA-OVA3 was not observed due to cross-reacting proteins on the blot [7].
Our recent data (unpublished) showed that the cleaved 5’ and 3’ fragments of human papillomavirus type 16 (HPV-16) E6/7 mRNA after shRNA treatment were unevenly degraded. The 5’ mRNA fragment was more abundant and displayed a greater stability than the corresponding 3’ fragment in the treated cells. Further analysis revealed that the 5’ fragment was polysome-associated, indicating its active translation, and this was further confirmed by using tagged E7 protein to show that C-terminally truncated proteins were produced in treated cells (Singhania et al. submitted).
Figure 2.
The shRNA targeting sites and primer design for HPV E6/E7 mRNA (Adapted from Gu et al 2009). (A) The shRNA and primer sites on E6/E7 mRNA. (B) The PCR products on an agarose gel. Notes: TC1, the untreated cell control. PLL, lentiviral vector control. *: indicates the site of CTL epitope. F: forward primer, R: reverse primer.
4. Possible models for explaining RNAi-induced immunity
It is well established that miRNAs play an important role in regulating innate and adaptive immune responses as a part of their gene-regulating roles. Evidence has accumulated that miRNAs are involved in the adaptive immune responses by regulating T-cells, B-cells, and antigen-presenting cells (APCs). For example, miR-214 was reported to target phosphatase and tensin homolog (PTEN) and increase proliferation and the activation of T-cells [10], while miR-150, -155, and let-7 have been shown to be involved in the development of T-cells into memory cells [11]. In addition, miR-184 was shown to inhibit nuclear factor of activated T-cells-1 (NFAT-1) in the activation of CD4 T-cell in the early stage of adaptive immune responses [12] and miR-181-a could promote CD4 and CD8 double positive T-cell development [13]. For B-cells, miR-155 is required for their normal function such as production of isotype-switched, high-affinity antibodies and for memory responses [14]. It has also been demonstrated that miR-155 is induced by B-cell receptor (BCR) [15]. However, overexpression of miR-155 can immortalize B-cells and lead to transformation, for instance, EBV was shown to have induced miR-155 expression and transformed B-cells [16, 17]. In addition, miR-150 is important in B-cell development [18] and so is miR-17 [19, 20].
For dendritic cells (DCs), a recent review summarized the need of miRNAs in their lineage commitment from bone marrow progenitors and for the development of subsets such as plasmacytoid DCs and conventional DCs [21]. Liu et al. (2010) used software to predict and then conducted experiments to confirm that three members of the miR-148 family, miR-148a, miR-148b, and miR-152 are negative regulators of the innate immune response and antigen-presenting capacity of DCs. They showed that miR-148/152 expression was upregulated in DCs on maturation and activation induced by TLR3, TLR4, and TLR9 agonists. These miRNAs in turn inhibited the production of cytokines including IL-12, IL-6, TNF-alpha, and IFN-beta and upregulation of MHC class II expression and DC-initiated antigen-specific T-cell proliferation by targeting Calcium/calmodulin-dependent protein kinase II alpha (CaMKIIα) [22]. In addition, miR-150 and miR-223 has been shown to play an important regulatory role in Langerhans cells (LCs) by cross-presenting a soluble antigen to antigen-specific CD8(+) T-cells [23, 24]. Beside APCs such as DC and LC, miRNA is shown to be directly involved in antigen presentation. For example, Bartoszewski et al. (2011) demonstrated that the mRNA of human endoplasmic reticulum (ER) antigen peptide transporter 1 (TAP1) is a direct target of miR-346. They showed that the 3\'-UTR (un-translational region) of TAP1 contains a 6-mer seeding region for miR-346 and the ER stress-associated reduction of TAP1 mRNA and protein levels could be reversed by inhibitory miRNA of miR-346 [25]. As TAP plays an important role in MHC class I-associated antigen presentation, their data provide an insight for miRNA-regulating MHC class-I-associated antigen presentation during ER stress.
The above-highlighted results clearly indicate miRNA’s regulatory role in many aspects of adaptive immunity. However, is it possible that miRNA also takes part in host immunity through mRNA fragments produced after RNAi just like shRNA described in section 2 and 3? Normally, miRNAs target the 3\' UTR and lead to the translation block or degradation of the targeted mRNAs. So when they degrade mRNAs, it is supposed to produce long 5\' mRNA fragments and may also produce truncated proteins. If this is true, the translated defective proteins could be treated as truncated protein and be processed by proteasome. If there is a CTL epitope in the defective structure, it could be coupled with the MHC class I molecule and presented to T-cells by DCs through antigen cross-presentation, as described above with shRNA. This could be a link between RNAi pathway and antigen presentation or adaptive immune response.
In the shRNA case discussed above, the target should be at the downstream of a CTL epitope to induce immunity. When miRNAs target 3\' UTR, a site certainly at the downstream site of any possible CTL epitopes, it is assumed to have the ability to produce truncated proteins and so to induce immune responses. Therefore, an important question for miRNA biology is whether miRNAs can routinely induce immune responses by degrading mRNA at 3\' UTR and generating 5\' mRNA fragments or truncated proteins that contain CTL epitopes? So far, there is no answer for this question. Another critical question is: what is the difference between blocking and degrading mRNA by miRNAs at 3\' UTR? Does this relate to antigen presentation of different proteins?
Because it has been shown that miRNA can act as siRNA and shRNA can be produced in the same pathway as miRNA [26], it is important and interesting to investigate if miRNA can induce the same immune response as shRNA. The systems of HPV 16 E7/TC1 and OVA/EG7 can be used as good models to investigate this. As miRNAs are routinely transcribed and involved in interacting with mRNA, this mechanism can be considered as a routine way in cells to generate CTL containing truncated proteins. However, because most mRNAs in cells are for self-proteins, their CTL epitopes will not be presented to T-cells. This leaves the question of whether this is a mechanism just for cells that express viral genes (such as HPV E7 in TC1 and C2 as above) or for cells expressing foreign genes/antigens (such as OVA in EG7)? The next question is: can this be generalized to any tumor antigens including self-antigens? This is an interesting subject to investigate and will facilitate our understanding of how RNAi pathways interact with and are involved in adaptive immune responses (antigen presentation) to utilize them for cancer immunotherapy.
Although some miRNA are highly conserved between lower animals and higher animals, mammals have far more miRNAs compared to nonmammals. This suggests that during evolution, as gene regulation became so complex and important in higher animals, miRNA or RNAi pathway gradually specialized into gene regulation. At the same time, as the adaptive immune system became well developed and highly specialized, these two systems got separated, but as described above, they still have some links. Future investigations leading to insight into these links will provide answers to the above questions.
5. Conclusion
In summary, RNAi-induced immunity opens a new perspective in which to explore the relationship between RNAi pathways and the immune system, especially its involvement in antigen presentation in the adaptive immune response. For RNAi biology, it will provide an insight into the understanding of function roles of RNAi (including miRNA and siRNA) in host defense. In the field of gene therapy for cancers, RNAi can be used as an approach to silence oncogenes as well as a strategy to enhance immunity against cancer antigens (at least viral infection related cancers) and further explored as a novel cancer immunotherapy. Finally, for intracellar pathogens, it can be used as a strategy for developing new vaccine through RNAi reactivating their antigens to the immune system.
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We have previously reported that a small hairpin RNA (shRNA) targeted the downstream site of a dominant cytotoxic T lymphocyte (CTL) epitope of human papillomavirus (HPV) type 16 oncogene E7 can stimulate an immune response against E7 expressing tumors in C57BL/6 mice. This results in the elimination of tumor growth in vivo, whereas an shRNA that targets the upstream site does not. Our recent data further confirm the long half-life of the 5'-mRNA fragment after shRNA degradation and its involvement in protein synthesis. This chapter summarizes these findings and provides some updated explanations for the findings.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/49434",risUrl:"/chapter/ris/49434",book:{slug:"rna-interference"},signatures:"Wenyi Gu",authors:[{id:"176822",title:"Dr.",name:"Wenyi",middleName:null,surname:"Gu",fullName:"Wenyi Gu",slug:"wenyi-gu",email:"w.gu@uq.edu.au",position:null,institution:{name:"University of Queensland",institutionURL:null,country:{name:"Australia"}}}],sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. The discovery of RNAi-induced adaptive immunity against tumors",level:"1"},{id:"sec_3",title:"3. Confirmation of mRNA fragments and truncated proteins in treated cells",level:"1"},{id:"sec_4",title:"4. Possible models for explaining RNAi-induced immunity",level:"1"},{id:"sec_5",title:"5. Conclusion",level:"1"}],chapterReferences:[{id:"B1",body:'Sharp, P.A., RNA interference--2001. Genes Dev, 2001. 15(5): p. 485-90. doi:10.1101/gad.880001.'},{id:"B2",body:'Elbashir, S.M., et al., Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature, 2001. 411(6836): p. 494-8. doi:10.1038/35078107.'},{id:"B3",body:'Jacque, J.M., K. Triques, and M. Stevenson, Modulation of HIV-1 replication by RNA interference. Nature, 2002. 418(6896): p. 435-8. doi:10.1038/nature00896.'},{id:"B4",body:'Harper, S.Q., et al., RNA interference improves motor and neuropathological abnormalities in a Huntington\'s disease mouse model. Proc Natl Acad Sci U S A, 2005. 102(16): p. 5820-5. doi:0501507102.'},{id:"B5",body:'Putral, L.N., et al., RNA interference against human papillomavirus oncogenes in cervical cancer cells results in increased sensitivity to cisplatin. Mol Pharmacol, 2005. 68(5): p. 1311-9. doi:10.1124/mol.105.014191.'},{id:"B6",body:'Bitko, V., et al., Inhibition of respiratory viruses by nasally administered siRNA. 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J Immunol, 2010. 185(2): p. 990-7. doi: 10.4049/jimmunol.1000793.'},{id:"B11",body:'Almanza, G., et al., Selected microRNAs define cell fate determination of murine central memory CD8 T cells. PLoS One, 2010. 5(6): p. e11243. doi: 10.1371/journal.pone.0011243.'},{id:"B12",body:'Weitzel, R.P., et al., microRNA 184 regulates expression of NFAT1 in umbilical cord blood CD4+ T cells. Blood, 2009. 113(26): p. 6648-57. doi: 10.1182/blood-2008-09-181156.'},{id:"B13",body:'Liu, G., et al., Pre-miRNA loop nucleotides control the distinct activities of mir-181a-1 and mir-181c in early T cell development. PLoS One, 2008. 3(10): p. e3592. doi: 10.1371/journal.pone.0003592.'},{id:"B14",body:'Calame, K., MicroRNA-155 function in B Cells. Immunity, 2007. 27(6): p. 825-7. doi:10.1016/j.immuni.2007.11.010.'},{id:"B15",body:'Yin, Q., et al., B-cell receptor activation induces BIC/miR-155 expression through a conserved AP-1 element. J Biol Chem, 2008. 283(5): p. 2654-62. doi: 10.1074/jbc.M708218200.'},{id:"B16",body:'Rahadiani, N., et al., Latent membrane protein-1 of Epstein-Barr virus induces the expression of B-cell integration cluster, a precursor form of microRNA-155, in B lymphoma cell lines. Biochem Biophys Res Commun, 2008. 377(2): p. 579-83. doi:S0006-291X(08)01984-0.'},{id:"B17",body:'Linnstaedt, S.D., et al., Virally induced cellular microRNA miR-155 plays a key role in B-cell immortalization by Epstein-Barr virus. J Virol, 2010. 84(22): p. 11670-8. doi:JVI.01248-10.'},{id:"B18",body:'Xiao, C., et al., MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell, 2007. 131(1): p. 146-59. doi:10.1016/j.cell.2007.07.021.'},{id:"B19",body:'Koralov, S.B., et al., Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. Cell, 2008. 132(5): p. 860-74. doi:S0092-8674(08)00268-7.'},{id:"B20",body:'Mendell, J.T., miRiad roles for the miR-17-92 cluster in development and disease. Cell, 2008. 133(2): p. 217-22. doi:S0092-8674(08)00449-2.'},{id:"B21",body:'Smyth, L.A., et al., MicroRNAs affect dendritic cell function and phenotype. Immunology, 2015. 144(2): p. 197-205. doi:10.1111/imm.12390.'},{id:"B22",body:'Liu, X., et al., MicroRNA-148/152 impair innate response and antigen presentation of TLR-triggered dendritic cells by targeting CaMKIIalpha. J Immunol, 2010. 185(12): p. 7244-51. doi:10.4049/jimmunol.1001573.'},{id:"B23",body:'Mi, Q.S., et al., Lack of microRNA miR-150 reduces the capacity of epidermal Langerhans cell cross-presentation. Exp Dermatol, 2012. 21(11): p. 876-7. doi:10.1111/exd.12008.'},{id:"B24",body:'Mi, Q.S., et al., Deletion of microRNA miR-223 increases Langerhans cell cross-presentation. Int J Biochem Cell Biol, 2013. 45(2): p. 395-400. doi:10.1016/j.biocel.2012.11.004.'},{id:"B25",body:'Bartoszewski, R., et al., The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem, 2011. 286(48): p. 41862-70. doi:10.1074/jbc.M111.304956.'},{id:"B26",body:'Zeng, Y., R. Yi, and B.R. Cullen, MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci, 2003. 100(17): p. 9779-9784. doi: 10.1073/pnas.1630797100.'}],footnotes:[],contributors:[{corresp:"yes",contributorFullName:"Wenyi Gu",address:"w.gu@uq.edu.au",affiliation:'
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V. inodora) (Orchidaceae) in the Island of Guadeloupe",slug:"microsatellite-markers-confirm-self-pollination-and-autogamy-in-wild-populations-of-vanilla-mexicana",signatures:"Rodolphe Laurent Gigant, Narindra Rakotomanga, Chloe Goulié,\nDenis Da Silva, Nicolas Barre, Gervais Citadelle, Daniel Silvestre,\nMichel Grisoni and Pascale Besse",authors:[{id:"61359",title:"Prof.",name:"Rodolphe",middleName:null,surname:"Gigant",fullName:"Rodolphe Gigant",slug:"rodolphe-gigant"},{id:"61361",title:"Dr.",name:"Michel",middleName:null,surname:"Grisoni",fullName:"Michel Grisoni",slug:"michel-grisoni"},{id:"174732",title:"Prof.",name:"Pascale",middleName:null,surname:"Besse",fullName:"Pascale Besse",slug:"pascale-besse"},{id:"186332",title:"MSc.",name:"Narindra",middleName:null,surname:"Rakotomanga",fullName:"Narindra Rakotomanga",slug:"narindra-rakotomanga"},{id:"186333",title:"MSc.",name:"Chloé",middleName:null,surname:"Goulié",fullName:"Chloé Goulié",slug:"chloe-goulie"},{id:"186511",title:"Dr.",name:"Nicolas",middleName:null,surname:"Barre",fullName:"Nicolas Barre",slug:"nicolas-barre"},{id:"186512",title:"Mr.",name:"Gervais",middleName:null,surname:"Citadelle",fullName:"Gervais Citadelle",slug:"gervais-citadelle"},{id:"186513",title:"MSc.",name:"Daniel",middleName:null,surname:"Silvestre",fullName:"Daniel Silvestre",slug:"daniel-silvestre"},{id:"186514",title:"MSc.",name:"Denis",middleName:null,surname:"Da Silva",fullName:"Denis Da Silva",slug:"denis-da-silva"}]},{id:"51943",title:"Microsatellite Markers in Analysis of Forest‐Tree Populations",slug:"microsatellite-markers-in-analysis-of-forest-tree-populations",signatures:"Justyna Anna Nowakowska",authors:[{id:"171846",title:"Prof.",name:"Justyna",middleName:null,surname:"Nowakowska",fullName:"Justyna Nowakowska",slug:"justyna-nowakowska"}]},{id:"52283",title:"Application of Microsatellites in Genetic Diversity Analysis and Heterotic Grouping of Sorghum and Maize",slug:"application-of-microsatellites-in-genetic-diversity-analysis-and-heterotic-grouping-of-sorghum-and-m",signatures:"Beyene Amelework, Demissew Abakemal, Hussein Shimelis and\nMark Laing",authors:[{id:"85318",title:"Dr.",name:"Hussein",middleName:null,surname:"Shimelis",fullName:"Hussein Shimelis",slug:"hussein-shimelis"},{id:"186753",title:"Dr.",name:"Amelework Beyene",middleName:null,surname:"Assefa",fullName:"Amelework Beyene Assefa",slug:"amelework-beyene-assefa"},{id:"187045",title:"Prof.",name:"Mark",middleName:null,surname:"Laing",fullName:"Mark Laing",slug:"mark-laing"},{id:"187046",title:"Dr.",name:"Demissew",middleName:null,surname:"Abakemal",fullName:"Demissew Abakemal",slug:"demissew-abakemal"}]},{id:"51833",title:"Practical Applications of Microsatellite Markers in Goat Breeding",slug:"practical-applications-of-microsatellite-markers-in-goat-breeding",signatures:"Yuta Seki, Kenta Wada and Yoshiaki Kikkawa",authors:[{id:"186086",title:"Dr.",name:"Yoshiaki",middleName:null,surname:"Kikkawa",fullName:"Yoshiaki Kikkawa",slug:"yoshiaki-kikkawa"},{id:"193884",title:"Dr.",name:"Yuta",middleName:null,surname:"Seki",fullName:"Yuta Seki",slug:"yuta-seki"},{id:"193885",title:"Dr.",name:"Kenta",middleName:null,surname:"Wada",fullName:"Kenta Wada",slug:"kenta-wada"}]},{id:"52589",title:"Microsatellites for the Amazonian Fish Hypophthalmus marginatus",slug:"microsatellites-for-the-amazonian-fish-hypophthalmus-marginatus",signatures:"Emil J. 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Bacher, Linda Clipson, Leta S. Steffen and Richard B.\nHalberg",authors:[{id:"43769",title:"Prof.",name:"Richard",middleName:null,surname:"Halberg",fullName:"Richard Halberg",slug:"richard-halberg"},{id:"186456",title:"Dr.",name:"Jeff",middleName:null,surname:"Bacher",fullName:"Jeff Bacher",slug:"jeff-bacher"},{id:"194172",title:"Ms.",name:"Linda",middleName:null,surname:"Clipson",fullName:"Linda Clipson",slug:"linda-clipson"},{id:"194173",title:"Dr.",name:"Leta",middleName:null,surname:"Steffen",fullName:"Leta Steffen",slug:"leta-steffen"}]},{id:"52558",title:"Microsatellite Instability in Colorectal Cancer",slug:"microsatellite-instability-in-colorectal-cancer",signatures:"Narasimha Reddy Parine, Reddy Sri Varsha and Mohammad Saud\nAlanazi",authors:[{id:"185797",title:"Dr.",name:"Narasimha Reddy",middleName:null,surname:"Parine",fullName:"Narasimha Reddy Parine",slug:"narasimha-reddy-parine"},{id:"186429",title:"Prof.",name:"Mohammad",middleName:null,surname:"Alanazi",fullName:"Mohammad Alanazi",slug:"mohammad-alanazi"}]}]}]},onlineFirst:{chapter:{type:"chapter",id:"72645",title:"Synthesis and Biological Evaluation of Thiazole Derivatives",doi:"10.5772/intechopen.93037",slug:"synthesis-and-biological-evaluation-of-thiazole-derivatives",body:'
1. Introduction
Thiazoles are five-membered heterocyclic compounds containing nitrogen and sulfur atoms with isothiazole isomer. Thiazoles are a basic scaffold found in many natural compounds as vitamin B1-thiamine, alkaloids, anabolic steroids, flavones [1].
The interest in the synthesis of compounds containing the thiazole moiety has been increasing steadily in view of their utility in the field of photosensitizers, rubber vulcanization [2], liquid crystals [3, 4], sensors [5], sunscreens [6], catalysts [7], dyes [8], pigments [1], and chromophores [9, 10]. Moreover, thiazoles occupy a prominent place in current medicinal chemistry due to their wide range of applications in the field of drug design and discovery [11]. They appear in the bacitracin, penicillin antibiotics [12], and various synthetic drugs as short-acting sulfa drug sulfathiazole [1]. Also, they are used as an antidepressant drug (pramipexole) [13], antiulcer agent (nizatidine) [14], anti-inflammatory drug (meloxicam) [15], HIV/AIDS drug (ritonavir) [16], and cancer treatment drug (tiazofurin) [17]. In fact, thiazole is a more common component of FDA-approved pharmaceuticals than related five-membered heterocycles such as isothiazole, thiophene, furan, isoxazole, and oxazole. On the other hand, the metal complexes of thiazole are widely used in photocatalysis [18]. 1,3-Thiazoles undergo different types of reactions to yield various biologically active fused heterocyclic moieties as thiazolopyrimidine, imidazothiazoles, thiazolopyridine, etc. [19, 20, 21].
2. Synthesis strategies of 1,3-thiazole derivatives
Thiazole ring system were easily synthesized by well-known methods of Hantzsch [22], Cook-Heilbron [23], and Gabriel [24]. A number of compounds may serve as nucleophilic reagent in this reaction, such as thioamides, thiourea, ammonium thiocarbamate or dithiocarbamate, and their derivatives. Hantzsch synthesized the simple thiazole nucleus in 1887 [25]. This synthesis approach involves cyclization and condensation of haloketones with thioamide, and it is considered the most widely popular process for the synthesis of thiazole moiety. In contrast, Gabriel synthesized thiazoles by treating α-acylaminoketones with stoichiometric amounts of P2S5 or Lawesson’s reagent [26]. Also, Cook-Heilbron used versatile methods for the synthesis of substituted aminothiazoles involving the reaction of α-aminonitriles with dithioacids or esters, carbon disulfide, carbonyl sulfide, and isothiocyanates under mild conditions [27].
Lately, thiazole derivatives were synthesized in the presence of various catalysts [28, 29, 30, 31] and with the use of a microwave irradiation technique [32].
2.1 Synthesis from α-halocarbonyl compounds (Hantzsch’s synthesis) (type I)
2.1.1 Reactions with thioamides
Thioamides and various α-halocarbonyl compounds were reacted to give numerous thiazoles with alkyl, aryl, arylalkyl, or heteroaryl of several functional groups at position 2, 4, or 5 (2.1.1) [33, 34] (Figure 1).
Figure 1.
Synthesis of 2-, 4-, 5-trisubstituted thiazole.
2.1.2 Reactions with N-substituted thiourea
2-Monosubstituted or disubstituted aminothiazoles (2.1.2) were obtained by the reaction of halocarbonyl compounds with N-substituted thiourea compounds [35] (Figure 2).
Figure 2.
Synthesis of substituted aminothiazoles.
2.1.3 Reaction with esters of thiocarbamic acid
The condensation of α-halocarbonyl compounds with thiocarbamates gave 2-hydroxythiazole derivatives (2.1.3) [36, 37] (Figure 3).
Figure 3.
Synthesis of 2-hydroxythiazole derivatives.
2.2 Synthesis from α-aminonitrile compounds (Cook-Heilbron’s synthesis) (Type II)
This class of synthesis gives 5-aminothiazole with different substituted in position 2 by interacting aminonitrile with salts and esters of dithioacids carbon oxysulfide, carbon disulfide, and isothiocyanates significantly [38, 39, 40].
2.2.1 Reaction with carbon disulfide
The condensation of carbon disulfide with α-aminonitriles gave 2-mercapto-5-amino thiazoles, which can be converted to 5-amino thiazoles substituted in position 2 (2.2.1) [41, 42] (Figure 4).
Figure 4.
Synthesis of 5-aminothiazole derivatives.
2.3 Reaction with esters and salts of dithioacids
The salts or the esters of both dithioformic and dithiophenacetic acids were reacted with α-aminonitriles to give 5-aminothiazoles (2.3) in good yields [43] (Figure 5).
Figure 5.
Synthesis of 5-aminothiazoles derivatives.
2.4 Reaction with acylaminocarbonyl compounds and phosphorus pentasulfide and related condensation (Gabriel’s synthesis) (Type III)
This reaction was originally designated by Gabriel in 1910. The reaction of phosphorus pentasulfide with acylaminoketone gave 2-phenyl-5-alkyl-thiazole in good yield (2.4) [44] (Figure 6).
Figure 6.
Synthesis of 2-phenyl-5-alkyl-thiazole derivatives.
2.5 Synthesis with eco-friendly methods
2.5.1 Using microwave-assisted synthesis (MAOS)
The synthesis of thiazole derivatives involves vigorous reaction conditions and wastage of solvents and catalysts. To overcome these shortcomings, eco-friendly methods as microwave irradiation technique are commonly used for synthesis of thiazole derivatives [45]. Rapid and elegant synthesis of a series of thiazoles (2.5.1) uses microwave heating under solvent-free conditions [32, 46, 47] (Figure 7).
Figure 7.
Synthesis of thiazoles under microwave irradiation.
2.5.2 One-pot multicomponent reaction in aqueous medium
Water is economically viable, nontoxic, and the most friendly reaction medium available, making it an environmentally acceptable solvent for the design and development of green chemistry technique. A three-component reaction of phenyl acetylene, N-bromosuccinimide, and thiourea in aqueous medium gave substituted thiazole derivatives (2.5.2) in good yield [48] (Figure 8).
Figure 8.
Synthesis of 2-aminothiazole in aqueous medium.
2.5.3 Using silica-supported tungstosilisic acid
An efficient and green method has been developed for the synthesis of new substituted Hantzsch thiazole derivatives (2.5.3) by one-pot multicomponent procedure. 3-(Bromoacetyl)-4-hydroxy-6-methyl-2H-pyran-2-one was reacted with thiourea and substituted benzaldehydes in the presence of silica-supported tungstosilisic acid as a catalyst under conventional heating or under ultrasonic irradiation technique [46, 49] (Figure 9).
Figure 9.
Synthesis of thiazole derivatives using silica.
2.6 Miscellaneous methods
Hantzsch construction of thiazole derivatives (2.6) was established by the reaction of α-chloroglycinate esters with thioamides or thioureas. Targeted compounds are obtained from readily available and inexpensive building blocks through an environmentally benign process and without catalysts [50] (Figure 10).
Figure 10.
Synthesis of thiazole derivatives.
The C − H substitution reaction of thiazole by the catalysis of the palladium/copper system is carried out in the presence of tetrabutylammonium fluoride under mild conditions. Various 2,5-diarylthiazole derivatives (2.6.1) were synthesized in good yields [51] (Figure 11).
Figure 11.
Synthesis of thiazole derivatives using palladium/copper.
2.7 Using oxidizing agents and thiourea
The mixtures of thiourea and acetophenone were treated with various oxidizing gents as sulfuryl chloride, chlorosulfonic acid, thionyl chloride, sulfur monochloride, sulfur trioxide, sulfuric acid, nitric acid, and sulfur. In each case a large amount of 2-amino-4-phenylthiazole (2.7) was obtained [52] (Figure 12).
Figure 12.
Synthesis of thiazole derivatives using oxidizing agents.
3. Biological importance of thiazoles
Thiazole and its derivatives are among the most active classes of compounds that are known for their broad spectrum of activity, e.g., antibacterial [53], antifungal [54], antimalarial [55], antitubercular [56], antiviral [57], anti-inflammatory [58], antidiabetic [59], anthelmintic [60], anticonvulsant [61], antioxidant [62], anticancer [63], and cardiovascular activities [64], and known as new inhibitors of bacterial DNA gyrase B [65]. Some drugs that already are on the market including the recent entry dasatinib possess thiazoles nucleus [66].
3.1 Antitumor activity
Compounds containing thiazole have marked their presence in a number of clinically available anticancer drugs such as tiazofurin [67], dasatinib [68], dabrafenib [69], patellamide A [70], ixabepilone [71], and epothilone [72].
Ramla et al. synthesized a variety of 4-amino-3-methyl-5-(2-methyl-1H-benzo[d]imidazol-1-yl)thiazol-2(3H)-one (3.1.1) and evaluated them for antitumor activity [73] (Figure 13).
Figure 13.
Structure of compound 3.1.1.
Popsavin et al. reported a set of 2-(2,3-anhydrofuranosyl) thiazole-4-carboxamide (2′,3′-anhydrotiazofurin) derivatives (3.1.2) and screened them for their antitumor activity [74] (Figure 14).
Figure 14.
Structure of compound 3.1.2.
A series of 5-arylidene derivatives were synthesized and evaluated for their antitumor activity. Compound 2-{2-[3-(benzothiazol-2-ylamino)-4-oxo-2-thioxothiazolidin-5-ylidenemethyl]-4-chlorophenoxy}-N-(4-methoxyphenyl)-acetamide (3.1.3) was found to be the most active among the tested compounds [75] (Figure 15).
Figure 15.
Structure of compound 3.1.3.
In another approach towards triple-negative breast cancer, Zhou et al. synthesized and optimized a series of hybrids of 2,4-diaminopyrimidine and thiazole derivatives (3.1.4). These compounds showed anti-proliferative properties against two breast cancer cell lines, MCF-7 and MDA-MB-231. Several of these compounds also exhibited potent activities against tumor cell colony [76] (Figure 16).
Figure 16.
Structure of compound 3.1.4.
A series of 2-(4-benzoyl-phenoxy)-N-(4-phenyl-thiazol-2-yl)-acetamides were synthesized by Prashanth et al. The authors suggest that the effect of compound (3.1.5) could be due to methyl, fluoro, and methoxy groups which are attached to phenoxy, benzoyl, and the phenyl ring of thiazole, respectively [77] (Figure 17).
Figure 17.
Structure of compound 3.1.5.
Dae-Kee K et al. produced a set of 5-(pyridin-2-yl)thiazoles enclosing a p- and/or m-carboxamide or carbonitrile-substituted phenylmethylamino moiety at position 2 of the thiazole ring (3.1.6). This series is evaluated for its ALK5 inhibitory activity [78, 79] (Figure 18).
Figure 18.
Structure of compound 3.1.6.
A series of 2,4-disubstituted thiazole compounds containing N-n-butyl or N-cyclohexyl thioureido synthon at position 2 and N-substituted thiosemicarbazone moiety (3.1.7) at position 4 were synthesized by HI El-Subbagh et al. and verified for their antitumor activity. All of the established derivatives revealed antineoplastic activity [80] (Figure 19).
Figure 19.
Structure of compound 3.1.7.
Santos et al. synthesized 6,7-bis(hydroxymethyl)-1H,3H-pyrrolo[1,2-c]thiazole (3.1.8) which showed activity for the triple-negative breast cancer, the most challenging tumor in clinical practice [81] (Figure 20).
Figure 20.
Structure of compound 3.1.8.
El-Borai et al. synthesized a series of 2 6-substituted-3-(pyridin-3-yl)imidazo[2,1-b]thiazole (3.1.9) which are tested for anticancer activity against human cancer cell lines HEPG2 (liver cancer) and MCF7 using sulforhodamine B (SRB) assay. All the synthesized compounds displayed more anticancer activity towards the selected cell line cancer, suggesting that it might be a potential alternative agent for human hepatic cancer therapy [82] (Figure 21).
Figure 21.
Structure of compound 3.1.9.
3.2 Antimicrobial activity
Fungal and bacterial resistance to antimicrobial drugs is increasing rapidly due to nonselective antimicrobial activities and a limited number of drugs. To overcome this situation, several molecules containing thiazole are synthesized to treat bacterial and fungal infections [83, 84].
El-Borai et al. work on an ongoing program in the field of synthesis and evaluated antimicrobial activity of medicinally important new compounds, taking the fused thiazole compounds as thiazolopyrimidines (3.2.1), imidazolothiazoles (3.2.2), and their derivatives as new examples in this domain [82] (Figure 22).
Figure 22.
Structure of compounds 3.2.1 and 3.2.2.
Vicini et al. synthesized a new set of 2-thiazolylimino-5-arylidene-4-thiazolidinones which were assayed in vitro for their antimicrobial activity against Gram-positive and Gram-negative bacteria and yeast. Compound (3.2.3) exhibited activity against Gram-positive bacteria [85] (Figure 23).
Figure 23.
Structure of compound 3.2.3.
A series of thiazolyl thiazolidine-2,4-dione derivatives were synthesized by Dundar et al. These compounds were screened for their antibacterial and antifungal activities against methicillin-resistant S. aureus, E. coli, and C. albicans. All the compounds particularly (3.2.4) were found to be moderately potent against screened microorganisms [86] (Figure 24).
Figure 24.
Structure of compound 3.2.4.
Abdel-Wahab et al. synthesized 3-(benzofuran-2-yl)-4,5-dihydro-5-aryl-1-[4-(aryl)-1,3-thiazol-2-yl]-1H-pyrazoles (3.2.5). The synthesized compounds were screened for their antibacterial and antifungal activities and showed a significant activity against E. coli higher than that of the control drug, whereas antifungal activity against Aspergillus niger was also exhibited and equal to that of the reference drug [87] (Figure 25).
Figure 25.
Structure of compound 3.2.5.
Bera et al. Synthesized pyridinyl thiazole ligand having hydrazone moiety and its cobalt complex. Both ligand and its complex were tested for antibacterial properties towards Gram-positive and Gram-negative bacteria. The results revealed that the ligand (3.2.6) exhibited excellent antibacterial activity. The presence of pyridinium ion in the ligand showed increased solubility of the ligand which enhances the cell penetrating ability and cell binding activity of the ligand. Hydrolysis of ligand decreases the pH of the medium which facilitates easy penetration of ligand into the cell [88] (Figure 26).
Figure 26.
Structure of compound 3.2.6.
3.3 Antifungal activity
Narayana et al. synthesized a series of 5-(2-substituted–1,3-thiazol-5-yl)-2-alkoxybenzamides and 5-(2-N-(substituted aryl)-1,3-thiazol-5-yl)-2-alkoxy benzamides. The synthesized compounds were screened for their antifungal activity. The derivatives of compound (3.3.1) exhibited significant activity [89] (Figure 27).
Figure 27.
Structure of compound 3.3.1.
Chimenti et al. reported the synthesis of a novel series of 2-thiazolylhydrazone derivatives and the influence of the substituents on the thiazole ring and on antifungal activity. Some of the tested compounds were found to possess significant antifungal activity when compared to clotrimazole, in particular compound (3.3.2) which exhibited higher potency against most of the Candida [90] (Figure 28).
Figure 28.
Structure of compound 3.3.2.
3.4 Antioxidant activity
Antioxidants are of great interest due to their participation in important biological and industrial processes. They are generated in the human body and may cause damage to lipids, proteins, and DNA and thus may lead to various diseases such as cancer, atherosclerosis, diabetes, cirrhosis, and Alzheimer’s and inflammatory diseases [91]. Thiazole and derivatives are the core structure in a variety of pharmaceuticals with a wide range of biological activity [92, 93, 94].
The antioxidant potential compounds (3.4.1) was evaluated by spectrophotometric method, using DPPH radical or Fe (TPTZ)3+ complex, and EPR spectroscopy and revealed that the synthesized compounds were showing potent antioxidant activity [95] (Figure 29).
Figure 29.
Structure of compound 3.4.1.
Bozdag-Dundar et al. synthesized a series of 2, 4-dichlorothiazolyl thiazolidine-2,4-dione and 4-chloro-2-benzylsulfanylthiazolyl-thiazolidine-2,4-dione derivatives, and they were tested for their antioxidant properties. Compound (3.4.2) showed the best superoxide anion scavenging activity [96] (Figure 30).
Figure 30.
Structure of compound 3.4.2.
Gouda et al. synthesized 2-amino thiazole derivatives and evaluated their antioxidant activity. They reported that the three compounds (3.4.3) showed potent antioxidant activity after postulating the structure–activity relationship (SAR) [97] (Figure 31).
Figure 31.
Structure of compound 3.4.3.
A series of N2-[2-chloro-4(3,4,5-trimethoxy phenyl) azetidin-1-yl)]-N4-(substituted aryl)-1,3-thioazol-2,4-diamine (3.4.4) were synthesized and screened for their in vitro antioxidant properties. The IC50 values revealed that some of the synthesized compounds were showing potent antioxidant activity [98] (Figure 32).
Figure 32.
Structure of compound 3.4.4.
4. Conclusion
Thiazole moieties have occupied a pivotal position in the modern organic and medicinal chemistry due to its broad-spectrum pharmacological and medicinal activities such as antimicrobial, anticancer, and antioxidant. The presence of thiazole ring in many drugs such as penicillin, pramipexole, tiazofurin, meloxicam, and nizatidine motivates the chemists to design new thiazole scaffolds. Thiazole nucleus exhibited an important role in finding new leads and drugs for various diseases. This chapter has illustrated the commonly used approaches to synthesize subsisted thiazole derivatives, described their key electronic properties, and highlighted their most important chemical reactivity. A particular focus has been on the use of thiazole in dyes and their metal complexes and miscellaneous applications of thiazole dyes. Also we have focused our attention on the biological application of thiazole derivatives.
List of abbreviations
FDA
Food and Drug Administration (USA)
SAR
structure–activity relationships
MAOS
microwave-assisted synthesis
HTIB
[hydroxy-(tosyloxy)-iodo] benzene
TBAF
tetrabutylammonium fluoride
\n',keywords:"azole heterocycles, thiazoles, biological activities, antioxidants, antimicrobial, anticancer, anti-Alzheimer, antihypertensive",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/72645.pdf",chapterXML:"https://mts.intechopen.com/source/xml/72645.xml",downloadPdfUrl:"/chapter/pdf-download/72645",previewPdfUrl:"/chapter/pdf-preview/72645",totalDownloads:305,totalViews:0,totalCrossrefCites:0,dateSubmitted:"December 27th 2019",dateReviewed:"May 26th 2020",datePrePublished:"June 29th 2020",datePublished:null,dateFinished:"June 29th 2020",readingETA:"0",abstract:"Thiazoles belong to the group of azole heterocycles. They are aromatic five-membered heterocycles containing one sulfur and one nitrogen atom. In recent years thiazoles, their derivatives, and isomers have gained considerable attention because of their broad applications in different fields, such as agrochemicals, industrial, and photographic sensitizers. Also, they have pharmaceutical and biological activities that include antimicrobial (sulfazole), antiretroviral (ritonavir), antifungal (abafungin), anticancer (tiazofurin), antidiabetic, anti-inflammatory, anti-Alzheimer, antihypertensive, antioxidant, and hepatoprotective activities. The compounds containing thiazole moieties are a prominent structural feature in a variety of natural products, such as vitamin B and penicillin. Thus, in this chapter several types of thiazole-based heterocyclic scaffolds such as monocyclic or bicyclic systems synthesis and their biological activities studies are presented. Furthermore modification of thiazole-based compounds at different positions to generate new molecules with potent antitumor, antioxidant, and antimicrobial activities is described.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/72645",risUrl:"/chapter/ris/72645",signatures:"Seham A. Ibrahim and Hala F. Rizk",book:{id:"9953",title:"Azoles - Synthesis, Properties, Applications and Perspectives",subtitle:null,fullTitle:"Azoles - Synthesis, Properties, Applications and Perspectives",slug:null,publishedDate:null,bookSignature:"Prof. Aleksey Kuznetsov",coverURL:"https://cdn.intechopen.com/books/images_new/9953.jpg",licenceType:"CC BY 3.0",editedByType:null,isbn:"978-1-83968-180-6",printIsbn:"978-1-83968-179-0",pdfIsbn:"978-1-83968-181-3",editors:[{id:"201033",title:"Prof.",name:"Aleksey",middleName:null,surname:"Kuznetsov",slug:"aleksey-kuznetsov",fullName:"Aleksey Kuznetsov"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:null,sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Synthesis strategies of 1,3-thiazole derivatives",level:"1"},{id:"sec_2_2",title:"2.1 Synthesis from α-halocarbonyl compounds (Hantzsch’s synthesis) (type I)",level:"2"},{id:"sec_2_3",title:"2.1.1 Reactions with thioamides",level:"3"},{id:"sec_3_3",title:"2.1.2 Reactions with N-substituted thiourea",level:"3"},{id:"sec_4_3",title:"2.1.3 Reaction with esters of thiocarbamic acid",level:"3"},{id:"sec_6_2",title:"2.2 Synthesis from α-aminonitrile compounds (Cook-Heilbron’s synthesis) (Type II)",level:"2"},{id:"sec_6_3",title:"2.2.1 Reaction with carbon disulfide",level:"3"},{id:"sec_8_2",title:"2.3 Reaction with esters and salts of dithioacids",level:"2"},{id:"sec_9_2",title:"2.4 Reaction with acylaminocarbonyl compounds and phosphorus pentasulfide and related condensation (Gabriel’s synthesis) (Type III)",level:"2"},{id:"sec_10_2",title:"2.5 Synthesis with eco-friendly methods",level:"2"},{id:"sec_10_3",title:"2.5.1 Using microwave-assisted synthesis (MAOS)",level:"3"},{id:"sec_11_3",title:"2.5.2 One-pot multicomponent reaction in aqueous medium",level:"3"},{id:"sec_12_3",title:"2.5.3 Using silica-supported tungstosilisic acid",level:"3"},{id:"sec_14_2",title:"2.6 Miscellaneous methods",level:"2"},{id:"sec_15_2",title:"2.7 Using oxidizing agents and thiourea",level:"2"},{id:"sec_17",title:"3. Biological importance of thiazoles",level:"1"},{id:"sec_17_2",title:"3.1 Antitumor activity",level:"2"},{id:"sec_18_2",title:"3.2 Antimicrobial activity",level:"2"},{id:"sec_19_2",title:"3.3 Antifungal activity",level:"2"},{id:"sec_20_2",title:"3.4 Antioxidant activity",level:"2"},{id:"sec_22",title:"4. Conclusion",level:"1"},{id:"sec_23",title:"List of abbreviations",level:"1"}],chapterReferences:[{id:"B1",body:'Borisenko VE, Koll A, Kolmakov EE, Rjasnyi AG. Hydrogen bonds of 2-aminothiazoles in intermolecular complexes (1,1 and 1,2) with proton acceptors in solutions. Journal of Molecular Structure. 2006;783(1):101-115'},{id:"B2",body:'Milne GWA. Handbook of Antineoplastic Agents. London, UK: Gower/Ashgate; 2000'},{id:"B3",body:'Kiryanov AA, Sampson P, Seed AJ. Synthesis of 2-alkoxysubstituted thiophenes, 1,3-thiazoles, and related S-heterocycles via Lawesson\'s reagent-mediated cyclization under microwave irradiation: Applications for liquid crystal synthesis. 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Department of Chemistry, Faculty of Science, Tanta University, Tanta, Egypt
'},{corresp:null,contributorFullName:"Hala F. Rizk",address:null,affiliation:'
Department of Chemistry, Faculty of Science, Tanta University, Tanta, Egypt
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Openness - We communicate honestly and transparently. We are open to constructive criticism and committed to learning from it.
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