Open access peer-reviewed chapter

# Technological Applications of Porphyrins and Related Compounds: Spintronics and Micro-/Nanomotors

Written By

David M. Lopes, Juliana C. Araujo-Chaves, Lucivaldo R. Menezes and Iseli L. Nantes-Cardoso

Submitted: December 3rd, 2018 Reviewed: April 4th, 2019 Published: May 10th, 2019

DOI: 10.5772/intechopen.86206

From the Edited Volume

## Metastable, Spintronics Materials and Mechanics of Deformable Bodies

Edited by Subbarayan Sivasankaran, Pramoda Kumar Nayak and Ezgi Günay

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## Abstract

The vital role played by porphyrins in cells and their use in therapeutic processes are well known. More recently, the technological applications of porphyrins have attracted the attention of researchers. Porphyrins have the property of half-metallic material, i.e., molecules that can host transition metals making feasible the production of spin-polarized electronic states at different channels. Therefore, porphyrins and hemeproteins are among the materials that have spin-filtering property to be applied in spintronics. Molecular spintronics is an emerging and highly relevant field due to their applications to the development of high-capacity information-storage devices and quantum computers. The catalytic properties of porphyrins and related compounds such as the hemeproteins are also applicable in the fabrication of micro-/nanomotors (MNMs). In this chapter, we describe the advances and future perspectives in the technological applications of porphyrins and related compounds in spintronic devices and micro-/nanomotors.

### Keywords

• porphyrins
• cytochrome c
• peroxidases
• interfaces
• micro-/nanomotors
• micro-/nanorobots
• spintronics
• semiconductors
• nanotechnology

## 1. Introduction

### 1.1 Porphyrins and hemeproteins

Porphyrins are essential compounds for the metabolism of living organisms. Porphyrins result from the substitution of porphine, which is a macrocycle formed by four pyrrole rings linked via methine bridges (Figure 1a). The tetrapyrrole ring has space for the coordination of a central transition metal ion with the four nitrogen atoms of the pyrrole rings to form a metalloporphyrin (Figure 1b) [1]. The properties of porphyrins can be modulated by substitutions at the β- and meso-positions, the central transition metal ions, and the metal ion axial ligands (Figure 1b). Another modification of porphyrin ring is the insertion of a carbene in a free-base ring to form the N,N’vinyl-bridged porphyrin and the insertion of a carbene into the metal-nitrogen bond of a metalloporphyrin [2, 3]. Carbenes can also be added to the porphyrin ring to form homoporphyrin that is also known as expanded porphyrins [4, 5]. The replacement of a nitrogen by C, O, S, Se, and Te results in core-modified porphyrins that are a platform for organometallic chemistry [6]. Two porphyrins are key groups for the energetic metabolism, oxygen transport, and photosynthesis: the iron protoporphyrin IX, the heme group, and chlorophyll (Figure 1c and d, respectively).

Metalloporphyrins are found in biological systems as the prosthetic group of proteins. Hemeproteins encompass a diversity of proteins associated with the heme group (iron protoporphyrin IX) such as respiratory cytochromes (cyt), cytoglobins (Cgb), neuroglobins (Ngb), myoglobin (Mb), hemoglobin (Hb), cytochrome P450 (CYP), cytochrome b5 (cytb5), and others [7, 8]. The biological activity of hemeproteins is modulated by the microenvironment and iron axial ligands provided by the apoprotein. The modulation of heme iron properties by the microenvironment of proteins results in the same prosthetic group responding for oxygen transport and storage [9], electron transport, NO trapping, and a variety of catalytic activities such as redox reactions, hydrogen peroxide cleavage, hydroxylation of aromatic compounds, and others [8]. Figure 1c shows the heme group of hemoglobin with histidine imidazole ring as the heme iron axial ligand at the fifth coordination position and molecular oxygen coordinated at the sixth coordination position. Other important biological metalloporphyrins are chlorophylls (magnesium complexes, Figure 1d), the plant pigment responsible for plant light harvesting, and cyanocobalamin, a vitamin B12 (cobalt complex, not shown) that participates in the lipid metabolism [10]. The remarkable chemical and photophysical properties of porphyrins have attracted the interest of researchers worldwide [1]. Biological and technological applications of porphyrins can involve the use of native hemeproteins, metallo-substituted hemeproteins, and the product of the tryptic digestion of horse heart cytochrome c, microperoxidases [11, 12, 13, 14, 15, 16, 17, 18, 19]. Inspired by nature, researchers have synthesized a diversity of nonnatural porphyrins. Theoretical studies of porphyrins have also gained relevance [4, 20, 21, 22, 23]. Synthesis of porphyrins is principally motivated by improved use in photodynamic therapy, energy, and catalysis [24, 25, 26]. The catalytic and photochemical properties of porphyrins are dependent on the presence and type of the central metal ion with axial ligands, the peripheral decoration, and microenvironment of the ring [11, 27]. In this regard, Zhang et al. [27] demonstrated that the peripheral decoration of porphyrins with simple electron withdrawing and donating groups affects the four Gouterman orbitals with a significant impact on spectroscopic properties and functions (Figure 2).

For both solar cells and PDT applications, it is essential that the electron promotion to the lowest excited state can be achieved by the absorption of red light. For energy, the chirality is also interesting because of the chiral-induced spin selectivity (CISS) effect. One example is the generation of hydrogen (H2) from water splitting by semiconductors. In a standard water splitting system by a semiconductor, the sunlight absorption produces the electron hole pair. The water oxidation by holes (h+) produces hydroxyl free radicals as intermediates of molecular oxygen evolution. The formation of hydrogen molecules requires that protons (H+), resulting from the combination of hydroxyl radicals as molecular oxygen, accept the electrons promoted to the conduction band. However, hydrogen gas production competes with the combination of hydroxyl radicals as hydrogen peroxide that is favored by spin-antiparallel photogenerated holes. In the absence of a spin filter, the combination of spin-antiparallel hydroxyl radicals produces singlet molecular oxygen and requires an overpotential of 1 eV, since molecular oxygen is a triplet species in the fundamental state. Chiral molecules act as a spin filter in the electron transfer favoring the production of spin-parallel hydroxyl free radicals and consequently oxygen evolution simultaneously with H2 production [28]. In the literature, the association of porphyrins and/or hemeproteins with nanostructures, especially for photodynamic therapy purposes, is reported [14, 29]. The reason for this association refers to an enormous quantity of studies and recent findings involving nanostructure properties and manipulation, particularly the potential for drug delivery systems [30]. Nanostructured materials have at least one dimension between 1 and 100 nm. They usually have different (electronic, mechanic, magnetic, optical, etc.) properties from the bulk material, which results in multiple potential applications [31].

### 1.2 General and basic concepts about nanotechnology, nano-/microrobots (motors), and spintronics

#### 1.2.1 Spintronic

Spintronic concept raised in the late 1980s refers to the use of spins to information transmission and computational operations [32, 33]. Spintronics is an emergent technology grounded in the information transmission by electronic charge and electron spin [34, 35, 36, 37, 38, 39]. Spintronic represents a paradigm break in the field of information to combine charge and magnetism in processing and storage. The beginning of spintronics is marked by the discovery of giant magnetoresistance (GMR) effect, in 1988, which resulted in the award of Nobel Prize in Physics in 2007 to Fert and Grunberg [40, 41]. Firstly, spintronic was associated with inorganic oxides, metals, and semiconductors because of the dependence of spin-orbit coupling (SOC). However, organic molecules have wanted properties such as biocompatibility, flexibility, abundance, the possibility of synthesis, low cost [32, 42], and rapidly gained interest in the spintronic studies. The potential applications for spintronics, particularly for electronic devices, are spin filters, spin diodes, spin transistors, spin field-effect transistors, and spin qubits in semiconductor nanostructures [42]. Spintronic has some emerging and promising subfields that are current-induced torque (CIT), spin Hall effect (SHE), spin caloritronics, silicon spintronics, spintronic aspects of graphene and topological insulators (TIs), and chiral-induced spin selectivity effect [32, 34]. The electron spins are degenerate in energy, but the level of degeneracy is broken inside the helix because the electron velocity generates an effective magnetic field that couples with the chiral potential. In a model of DNA double helix, the spin-down electrons aligned preferentially parallel to their velocity in a right-handed helix, while the same occurred with spin-up electrons in the left-handed helix. In an experimental approach, self-assembled monolayers (SAMs) of 3′ thiolated single- and double-strand DNAs (ssDNA and dsDNA, respectively) were attached on a clean 200 nm-thick polycrystalline gold film that was evaporated on glass slides. Photoelectrons were ejected from the gold film by clockwise and counterclockwise circularly polarized light and transmitted through ssDNA and dsDNA monolayers. A more intense transport of electrons ejected with a counterclockwise polarized laser in dsDNA was detected, and no spin selectivity was detected in ssDNA SAMs. Zwang et al. demonstrated that the spin selectivity in DNA is dependent on the supramolecular organization of chiral DNA moieties rather than the chirality of the individual monomers, and thus the spin selectivity can be switched by a conformational change of the molecules [32, 35, 36, 37, 38, 39, 43]. The mechanism of CISS effect is believed to be a result of evolution [37], where chiral molecules can increase the conductance of electrons with a spin channel while decreasing the other one [32, 33, 43]. Mishra et al. [44], in recent studies, demonstrated a spin-dependent electron transmission through helical structured bacteriorhodopsin proteins. The study potentially says that the spin degree of freedom may be associated with an important function in electron transport in biological systems. Einati et al. [45] and Roy et al. [46] have shown that the efficiency of electron spin filtering through purple membrane films can be reduced with a green light. So, at potential applications of spin filters, it could modulate the efficiency of the filter.

#### 1.2.2 Nanorobots

Nowadays, a new field of study involving nanotechnology is gaining importance: micro-/nanorobotics. Micro-/nanorobots (MNRs) have autonomous motion provided by micro-/nanomotors (MNMs) that are micro-/nanometer-scale devices powered with the ability to convert chemical, optical, acoustic, magnetic, and electrical energies into mechanical energy [47]. MNRs can be functionalized to perform complex tasks in a microcosm that constitutes the so-called micro-/nanorobots (MNRs) [48]. MNRs have an extensive range of potential applications such as remediation, nanofabrication, repair of materials, engineering, computing, environment monitoring, and especially in theranostics. Drug delivery systems, cell transport, and DNA and RNA insertions are some of the most numerous studies [49, 50]. The size of MNRs allows their application in minimally invasive diagnosis and treatments [51]. There is a basic classification for nanorobots. They can be biological, artificial, or biohybrid [52]. Also, they are classified according to the type of propulsion: self-propelled or external field-propelled ones. The self-propelled nanorobots convert energy from the environment to kinetic energy for independent movement, and it can be done by self-electrophoresis, self-thermophoresis, self-diffusiophoresis, and tiny bubbles [52]. Among the energy sources that self-propelled MNRs can use, light is highly attractive [47]. Light-powered MNMs can obtain energy from an external source and surrounding chemicals to get efficient propulsion through a photocatalytic process and constitute the photocatalytic micro-/nanomotors (PMNMs). Self-propelling PMNMs can be controlled in various ways such as chemical concentration or light intensity [47, 48, 53]. Furthermore, these PMNMs can be operated at low levels of optical and chemical energy input, which are highly desired scenarios. An important aspect is that the photocatalytic reactions of PMNMs can generate the superoxide radicals (O2 −•) that give these devices great potential for environmental remediation, especially in the degradation of organic pollutants. The Janus model can be used to explain the basic principles that respond to the self-propulsion of the photocatalytic MNMs (Figure 3).

The external field-propelled MNRs depend on an external force such as electric and magnetic field, light impulses, sonic waves, etc. [52]. The fabrication of MNRs can be direct, indirect, or by self-assembly [51]. The techniques used for the MNR fabrication are the same for the regular nanoparticles: top-down (lithography and scanning probe microscopy) and bottom-up (deposition, a solution with reducing agents). The materials used for MNR fabrication could be super magnetic substances, organic and inorganic compounds, and biological substances [51, 54].

## 2. Applications of porphyrins and hemeproteins in spintronics

### 2.1 Porphyrins and derivatives

Single-molecule spintronic devices have gained crescent interest for the use in advanced electronic systems. The question is to find molecular structures which, as single molecule, can exhibit the desirable properties of spintronics such as spin valve [55, 56, 57, 58, 59, 60], spin crossover [61, 62, 63], spin filtering [64, 65, 66], Kondo effect [67], and others. In the literature, porphyrins and derivatives have been described as promising candidates for molecular devices, once they have unique electronic properties [68]. Theoretical and experimental studies on the charge transport of porphyrin-based derivatives have demonstrated desirable physical properties for single-molecule spintronic such as current switching, long-range electron tunneling, current rectifying, and others [55, 69, 70, 71]. Several studies have corroborated the potential of porphyrin application in spintronics. Self-assembled porphyrin nanorods showed the mediated conduction through a UHV-STM image with differing HOMO- and LUMO-mediated conductions. The authors demonstrated a conductivity by barrier-type tunneling through distances less than 10 nm and long-distance conduction occurring only through the LUMO band. The self-assembled porphyrin nanorods are an efficient rectifying device that converts alternating current (AC), i.e., a current that periodically inverts direction, to direct current (DC), which moves in a unique direction [72]. In another study, the electronic transport of a nanowire composed by porphyrin-ethyne-benzene conjugates had its effective conductivity assigned to the coplanar conformation of phenyl and porphyrin moieties. The coplanar structure that allows amino or nitro substituent at the meta-position of the phenyl bridge that connects the π-system can provide higher current ratios of the on/off states. The switch effect of meta-substituents in the coplanar conformation disturbs the whole molecule while having only a local impact on the system with a perpendicular conformation. The nanowires formed by π-conjugated systems have potential for switch devices tunable by substituents [69]. Another evidence of porphyrin application in electronic devices was reported by Sedghi et al. [71]. Nanowires formed by porphyrin molecules linearly oligomerized (oligo-porphyrin wires) can mediate temperature-dependent electron transport. The study showed that the system conductance has temperature dependence and it suggests a long-range electron tunneling [71]. For application in spintronic devices, Cho et al. [73] proposed a theoretical organometallic framework formed by one-dimensional infinite chromium porphyrin array in which chromium atoms are located in a straight line (Figure 4a). The system exhibited spin filter property when the simulations were carried out with dimeric form, Cr-PA2, between Au electrodes (Figure 4b).

The fabrication of spin-dependent electronics, the spintronic devices, requires the external control of the magnetization of the that behaves like a magnet. In this regard, the paramagnetic porphyrin molecule is a promising active building block for spintronic devices. Wende et al. [74] studied by experimental and theoretical approach paramagnetic iron porphyrin molecules bound on ferromagnetic Ni and Co films on Cu(100). The authors investigated the porphyrin structural orientation and the magnetic coupling with the substrate. The porphyrin molecules associated with the substrate Co or Ni were ordered ferromagnetically. In the device, the magnetic moment of the porphyrin iron could be rotated in the plane and out of the plane by a magnetization reversal of the substrate. In a similar study, Scheybal et al. [75] also associated porphyrins with metallic films and studied X-ray magnetic circular dichroism (XMCD). In this case, the researchers used manganese (III)-tetraphenylporphyrin chloride (MnTPPCl) molecules adsorbed by cobalt substrate film. The results demonstrated that the film substrate induced a net magnetization on the porphyrin. Chen et al. [76] made calculations of conductance in a ferrous porphyrin. The study showed that the conductance of the iron porphyrin is tuned by mechanical distortion of the porphyrin plane and shifts the coupling state from the low spin to excited spin states. These properties of the system are interesting for sensing applications. Systems containing molecules with switchable spins are promising for the fabrication of materials with spintronic properties. Organometallic molecules such as porphyrins can be switched to on and off magnetic states when associated with the ferromagnetic substrate. Wäckerlin et al. [77] described that cobalt(II)tetraphenylporphyrin (CoTPP) ferromagnetically coupled to nickel thin film (Ni(001)) is switchable from on to off state of Co spin by the complexation with NO that is a spin trans effect. NO coordinates with Co2+ leading to the formation of a NO-CoTPP nitrosyl complex that is the off state of the Co spin. The system is restored to the on state when NO is thermally dissociated from the nitrosyl complex. Li et al. reported the construction and magnetic characterization of a fully functional system formed by the hybridization of a single magnetic porphyrin molecule with graphene nanoribbons. The fusion of the porphyrin core into graphene through the formation of new carbon rings at chemically predefined positions was demonstrated by scanning tunneling microscopy of high resolution. The authors also demonstrated that porphyrin retains the magnetic functionality and the magnetic anisotropy is modulated by the structure of the contacts [78]. In another study, Lewandowska et al. report a simple and efficient method for the fabrication of porphyrin-graphene oxide hybrids. The hybrid system has donor-acceptor properties and exhibits charge transfer between porphyrin and graphene oxide. The non-covalent interaction between the porphyrin and graphene oxide changes intensely the magnetic properties. The dramatic change in the magnetic properties probably is due to refined tuning of graphene domain magnetism that can be promoted by the modulation electron density produced by electron donor or electron acceptor substituents [79].

### 2.2 Hemeproteins

The presence of the iron protoporphyrin IX as the prosthetic group of hemeproteins endows these proteins of electronic and magnetic properties that can be applied in spintronics. The hemeproteins have an additional property that is the folding in chiral structures. [80]. The chiral structures such as the α-helices present in cytochrome c (Figure 5), for instance, can act as spin filters and respond for the chiral-induced spin selectivity (CISS) effect. To date, cytochrome c has been the unique hemeprotein used for spin filtering [28, 33, 38].

New types of spin-dependent electrochemistry measurements have been applied to probe the spin-dependent charge transport properties of nonmagnetic chiral molecules such as cytochrome c. Besides cytochrome c, the photosystems that are complexes of proteins associated with a non-heme porphyrin, the chlorophyll, also have electron transport capacity with spin selectivity [81, 82]. When the measurements were carried out with different orientations of the PSI protein complex, the dependence of spin polarization with the electron transfer path in photosystem I was proven [81, 82].

## 3. Application of porphyrins and hemeproteins in the construction and working of micro-/nanorobots

### 3.1 Porphyrins and derivatives

Several studies have been developed to produce nanodevices containing porphyrins with a potential use in MNRs to be applied in theranostics. According to Li et al. [83], porphyrins have a diversity of properties applicable to health preservation, diagnosis, and treatment. Porphyrins can amplify signals for magnetic resonance imaging (MRI), positron emission tomography (PET), infrared fluorescence imaging, and dual modal PET-MRI. Porphyrins have chemical and physical properties that allow the application of these compounds in the detection and destruction of tumors. Porphyrins can efficiently convert light into electronic excitation of molecular oxygen to produce singlet oxygen in photodynamic therapy (PDT) or light to heat for photothermal therapy (PTT). Therefore, porphyrins have been applied in the treatment of solid cancers and ocular vascularization diseases [29]. Also, there are some studies about porphyrin-nanoparticle systems employed in dentistry treatment [84, 85, 86, 87]. These systems can be used in the diagnosis of cancer by acting, for instance, as biosensors that exhibit affinity for a single molecule converting biochemical to electrical signals, detection of salivary biomarkers of oral tumors, and others [85, 88]. The capacity of self-assembly in a range of supramolecular aggregates is a crucial property for the application of porphyrins to construct MNRs [29, 89]. Ion et al. [89] demonstrated that porphyrins could self-assemble in several types of supramolecular aggregates such as linear head to tail, J-aggregates, and fractal aggregates with diverse and definite photophysical properties (Figure 6) [89].

The study of Ion et al. showed nanotubes formed by porphyrins and the importance of this technique for brain aneurysm instrumentation. They used meso-5, 10, 15, 20-sulfonate-phenyl porphyrin (TPPS4) and observed the formation of organized nanostructures by ionic self-assembly. Neurons and glial cells incubated with porphyrin nanotubes formed interconnected networks featured on the nanotube templates. The capacity of TPPS4 to form nanotubes by self-assembly demonstrates the potential of this porphyrin in the fabrication of NMRs applied to medicine. MNRs must have the capacity to self-propel that could be provided by a diversity of materials and mechanisms. Park et al. describe the fabrication of “swimmers”: microstructures with autonomous mobility at water/air interface. The particles of porphyrin-based metal–organic frameworks (MOFs) were fabricated with hydrophobic meso-tetra(4-carboxyphenyl)-porphyrin (H4-TCPP-H2, L) ligands bound to Zr-oxo clusters. The H4-TCPP-H2, L responds for the hydrophobic character of the framework [90]. Similar MOFs were described in the literature before, once they are efficient in the controlled release of surface-active substances proportionating a controlled motion. However, usually, the MOFs use high-cost surface-active substances [90]. The MOFs fabricated with meso-tetra(4-carboxyphenyl)-porphyrin ligands bound to Zr-oxo clusters use much less expensive fuels. The particles have the advantage to be refueled multiple times and attained speeds of ca. 200 mm·s−1. Interestingly, the type of fuel, the microstructure, and surface wettability of the MOF surface determine the efficiency of motion. In another study, Serrà et al. [91] reported the fabrication of a multifunctional nanorobotic platform with magnetic properties to promote the death of cancer cells by magnetic and mechanical destruction. A multi-segmented nanowire composed by nickel and gold alternating segments was produced by electrodeposition of metals inside the nanochannels of a polycarbonate membrane. In sequence, the nickel segments were transformed in core-shell Ni/NiO segments by the treatment of the nanowire with NaOH 0.5 M for 6 h. The nanowires were treated sequentially with zinc protoporphyrin IX and 1,9-nonanedithiol that displaces the porphyrin from the gold segments. The nanotubes exhibited ferromagnetism and could be manipulated by a magnet. When the bi-functionalized nanotubes attain cells, magnet or photostimulation can induce cell death that is useful for cancer treatments since the effect of some medical procedures, like hyperthermia and photodynamic therapy, could be improved by application of a rotary magnetic field [91].

### 3.2 Hemeproteins

Hemeproteins such as hemoglobin (Hb), myoglobin (Mb), horseradish peroxidase (HRP), catalase, and cytochrome c (cyt c) have the prosthetic group, ferrous or ferric protoporphyrin IX (heme group), as the redox center. The heme group makes hemeproteins useful for a medical and technological application that involves redox reactions. The use of hemeproteins in nanodevices can be impaired by denaturation or the orientation of the redox site [92]. However, literature has several examples of the use of hemeproteins in nanodevices [93, 94, 95]. Hemeproteins can also be used in the self-propelling of MNRs. Hemeproteins can act in MNMs by the bubble recoil mechanism. Catalase is the best hemeprotein for use in MNMs due to the capacity to convert hydrogen peroxide to oxygen generating propulsion bubbles [96]. Pavel et al. [97] fabricated nanorods with self-electrophoresis taking advantage of the combined catalysis of HRP and cytochrome c as illustrated in Figure 7.

One half of the nanorod was made of polypyrrole (PPy) modified with HRP, and the other half was made of gold and decorated with cyt c. [97]. The charge separation was promoted by the reaction of cytochrome c with superoxide ion (O2 −•) and HRP with H2O2. Ferric cyt c oxidizes O2 −• to O2 and is recycled to the oxidized form by transferring one electron through the nanorod to the high valence forms of HRP generated by the reaction with hydrogen peroxide (Figure 7) [97]. The study published by Pavel et al. demonstrated that the hemeproteins are robust enough to maintain the activity even immobilized on solid substrates [97].

## 4. Conclusions and perspectives

Porphyrins and hemeproteins have been widely studied because of their biological roles in energy metabolism and light harvesting in photosynthesis. More recently, with the advancement of bioelectronics and micro-/nanorobotics, porphyrins and hemoproteins have gained interest because of their specific properties. Porphyrins have desirable properties for single-molecule spintronic such as current switching, long-range electron tunneling, current rectifying, and others. Regarding the hemoproteins, they combine the presence of a porphyrin (iron protoporphyrin IX) as the redox center with the chiral protein structure that acts as a spin filter. To date, cytochrome c stands out as the hemoprotein for which the capacity to produce CISS effect has already been demonstrated experimentally. Porphyrins and hemoproteins also have proven potential for nanorobotic application. Porphyrins are particularly useful for nanorobotics applied to medicine because of their photochemical properties. Porphyrins also can self-assemble in structures such as J-aggregates to form nanotubes. On the other hand, the catalytic properties of hemoproteins are the most relevant factor that makes them applicable to self-propulsion in micro-/nanorobotics. The studies and applications of porphyrins and hemoproteins in spintronic and nanorobotic are still in their early stages, and a wide field of study of these compounds is open to the area of ​​bioelectronics. Among the numerous advances that are possible for the field of spintronic, special attention has been given to spinterface, that is, the interface between a ferromagnetic (FM) metal and an organic semiconductor, in which unique hybrid states are formed. The FM metal/molecular interfaces constitute an important building block for the future of spintronics. The unique hybrid states of spinterfaces influence magnetic properties such as magnetic anisotropy, magnetic exchange coupling, interfacial spin polarization, and others. Further, the interactions between the FM metal and organic molecules are tunable in such a way that the spinterfaces are applicable to multifunctional devices meeting the industry tendency of miniaturization using single-molecule devices. The external control of spinterface by external signals, especially light because the ultra-fast optical transmission, is a promising area for future investigations. An important challenge for the design of spintronic devices is the changeable control and switch of single molecules adsorbed on the surface of FM materials. Particularly, for the metalloporphyrins, an interesting example is the use of axial ligands of the porphyrin transition metal center to change the magnetism of the molecular component [98]. NO was able to reversibly switch the spin state of the Co and Fe of porphyrins adsorbed on Ni(001) Co substrates, respectively. Similarly, NH3 was able to induce the transition of Ni porphyrin on Co substrate from low to high spin states [99, 100]. Another emerging field of spintronics is the use of antiferromagnets that are affected by spin-polarized currents. Antiferromagnetic materials have several advantages for spintronics such as they do not create external magnetic fields and only weak interactions occur with each other and the antiferromagnets have the characteristic frequencies of switching between their states significantly higher than the values obtained for ferromagnets. Further, the occurrence of ordering in antiferromagnets it is more frequent and occurs at soft conditions than in ferromagnets. Also, these materials can behave as a conductor for a spin polarization and as an insulator for other spin polarization. The antiferromagnets can provide desirable characteristics for spintronics that are high speed of operation in terahertz range, performance, easy manipulation, high sensitivity, and low energy cost [101].

The field of micro/nanorobotics that also can take advantage of the properties of porphyrins and hemeproteins has as the principal challenge for advances as the control and powering of the movement. The crescent interest in the application of MNR in theranostic poses the additional challenge for the use of biocompatible and high-performance materials and fuels. An interesting alternative regarding the elimination of toxic fuels is the use of systems having the propulsion powered by external field that are fuel-free and allow the remote control of the movement. The MNRs with a real potential to operate in vivo are rare now and constitute an important area for future investigations that requires multi- and interdisciplinary studies [102].

## Acknowledgments

The author thanks FAPESP 2015/017688-0, 2017/02317-2, SisNano (402289/2013-7), NBB/UFABC, CAPES grant 001, and CNPq (309247/2017-9) for the financial support and CEM/UFABC for the access to facilities.

## Conflict of interest

The authors declare no conflict of interest.

## References

1. 1. Biesaga M, Pyrzyńska K, Trojanowicz M. Porphyrins in analytical chemistry. A review. Talanta. 2000;51:209-224
2. 2. Chan YW, Wood FE, Renner MW, et al. Remarkable disruption of a porphyrin. Insertion of a ruthenium atom into a pyrrole carbon-nitrogen bond of an N,N’-vinyl-bridged porphyrin. Journal of the American Chemical Society. 1984;106:3380-3381
3. 3. Latos-Grazynski L, Cheng RJ, La Mar GN, et al. Reversible migration of an axial carbene ligand into an iron-nitrogen bond of a porphyrin. Implications for high oxidation states of heme enzymes and heme catabolism. Journal of the American Chemical Society. 1981;103:4270-4272
4. 4. Mack J. Expanded, contracted, and isomeric porphyrins: Theoretical aspects. Chemical Reviews. 2017;117:3444-3478
5. 5. Anju KS, Das M, Adinarayana B, et al. meso -aryl [20]π homoporphyrin: The simplest expanded porphyrin with the smallest Möbius topology. Angewandte Chemie International Edition. 2017;56:15667-15671
6. 6. Chmielewski PJ, Latos-Grażyński L. Core modified porphyrins—A macrocyclic platform for organometallic chemistry. Coordination Chemistry Reviews. 2005;249:2510-2533
7. 7. Hening WA, Allen RP, Chokroverty S, et al. The iron metabolic system. Restless Legs Syndrome. 2009;1:50-60
8. 8. Lin YW, Wang J. Structure and function of heme proteins in non-native states: A mini-review. Journal of Inorganic Biochemistry. 2013;129:162-171
9. 9. Chakraborti AS. Interaction of porphyrins with heme proteins—A brief review. Molecular and Cellular Biochemistry. 2003;253:49-54
10. 10. Dumon H, Diez M, Nguyen P, et al. Liver lipid metabolism. Journal of Animal Physiology and Animal Nutrition (Berlin). 2008;92:272-283
11. 11. Prieto T, Santana V, AMM B, et al. Structure and catalysis of fe(III) and cu(II) microperoxidase-11 interacting with the positively charged interfaces of lipids. Molecules. 2017;22. DOI: 10.3390/molecules22081212 [Epub ahead of print]
12. 12. Araujo JC, Prieto T, Prado FM, et al. Peroxidase catalytic cycle of MCM-41-entrapped microperoxidase-11 as a mechanism for phenol oxidation. Journal of Nanoscience and Nanotechnology. 2007;7:3643-3652
13. 13. Prieto T, Marcon RO, Prado FM, et al. Reaction route control by microperoxidase-9/CTAB micelle ratios. Physical Chemistry Chemical Physics. 2006. DOI: 10.1039/b601671e [Epub ahead of print]
14. 14. Carmona-Ribeiro AM, Prieto T, Nantes IL. Nanostructures for peroxidases. Frontiers in Molecular Biosciences. 2015;2. DOI: 10.3389/fmolb.2015.00050 [Epub ahead of print]
15. 15. Stark BC, Pagilla KR, Dikshit KL. Recent applications of Vitreoscilla hemoglobin technology in bioproduct synthesis and bioremediation. Applied Microbiology and Biotechnology. 2015;99:1627-1636
16. 16. Lebedev N, Trammell SA, Spano A, et al. Conductive Wiring of Immobilized Photosynthetic Reaction Center to Electrode by Cytochrome c. 2006. DOI: 10.1021/JA063367Y [Epub ahead of print]
17. 17. Krainer FW, Glieder A. An updated view on horseradish peroxidases: Recombinant production and biotechnological applications. Applied Microbiology and Biotechnology. 2015;99:1611-1625
18. 18. McNeil CJ, Smith KA, Bellavite P, et al. Application of the electrochemistry of cytochrome c to the measurement of superoxide radical production. Free Radical Research Communications. 1989;7:89-96
19. 19. Faiella M, Maglio O, Nastri F, et al. De novo design, synthesis and characterisation of MP3, a new catalytic four-helix bundle hemeprotein. Chemistry—A European Journal. 2012;18:15960-15971
20. 20. Rybicka-Jasińska K, Shan W, Zawada K, et al. Porphyrins as photoredox catalysts: Experimental and theoretical studies. Journal of the American Chemical Society. 2016;138:15451-15458
21. 21. Mandal B, Sarkar S, Sarkar P. Theoretical studies on understanding the feasibility of porphyrin-sensitized graphene quantum dot solar cell. Journal of Physical Chemistry C. 2015;119:3400-3407
22. 22. Sirithip K, Prachumrak N, Rattanawan R, et al. Zinc–porphyrin dyes with different meso-aryl substituents for dye-sensitized solar cells: Experimental and theoretical studies. Chemistry—An Asian Journal. 2015;10:882-893
23. 23. Singh A, Lin Y, Quraishi MA, et al. Porphyrins as corrosion inhibitors for N80 steel in 3.5% NaCl solution: Electrochemical, quantum chemical, QSAR and Monte Carlo simulations studies. Molecules. 2015;2050:15122-15146
24. 24. Mugnol KCU, Martins MVA, Nascimento EC, et al. Interaction of Fe(3+)meso-tetrakis (2,6-dichloro-3-sulfonatophenyl) porphyrin with cationic bilayers: Magnetic switching of the porphyrin and magnetic induction at the interface. Theoretical Chemistry Accounts. 2011. DOI: 10.1007/s00214-011-1055-0 [Epub ahead of print]
25. 25. Araujo-Chaves JC, Kawai C, Melo AFAA, et al. Interaction and reaction of the antioxidant MnIII [Meso-Tetrakis(4-NMethyI Pyridinium)Porphyrin] with the apoptosis reporter lipid Phosphatidylserine. Current Physical Chemistry. 2013;3:187-198
26. 26. Lin VSY, DiMagno SG, Therien MJ. Highly conjugated, acetylenyl bridged porphyrins: New models for light-harvesting antenna systems. Science (80-). 1994;264:1105-1111
27. 27. Zhang A, Kwan L, Stillman MJ. The spectroscopic impact of interactions with the four Gouterman orbitals from peripheral decoration of porphyrins with simple electron withdrawing and donating groups. Organic & Biomolecular Chemistry. 2017;15:9081-9094
28. 28. Zhang W, Banerjee-Ghosh K, Tassinari F, et al. Enhanced electrochemical water splitting with chiral molecule-coated Fe3O4 Nanoparticles. ACS Energy Letters. October 2018;3(10):2308-2313
29. 29. Vargas A, Pegaz B, Debefve E, et al. Improved photodynamic activity of porphyrin loaded into nanoparticles: An in vivo evaluation using chick embryos. International Journal of Pharmaceutics. 2004;286:131-145
30. 30. Penon O, Patiño T, Barrios L, et al. A new porphyrin for the preparation of functionalized water-soluble gold nanoparticles with low intrinsic toxicity. ChemistryOpen. 2015;4:127-136
31. 31. Xia Y, Xiong Y, Lim B, et al. Shape-controlled synthesis of metal nanocrystals: Simple chemistry meets complex physics? Angewandte Chemie International Edition. 2009;48:60-103
32. 32. Naaman R, Waldeck DH. Chiral-induced spin selectivity effect. Journal of Physical Chemistry Letters. 2012;3:2178-2187
33. 33. Kumar A, Capua E, Kesharwani MK, et al. Chirality-induced spin polarization places symmetry constraints on biomolecular interactions. Proceedings of the National Academy of Sciences. 2017;114:2474 LP-2472478
34. 34. Sinova J, Žutić I. New moves of the spintronics tango. Nature Materials. 2012;11:368-371
35. 35. Zwang TJ, Hürlimann S, Hill MG, et al. Helix-dependent spin filtering through the DNA duplex. Journal of the American Chemical Society. 2016;138:15551-15554
36. 36. Xie Z, Markus TZ, Cohen SR, et al. Spin specific Electron conduction through DNA oligomers. Nano Letters. 2011;11:4652-4655
37. 37. Gannett PM, Bostick CD, Mukhopadhyay S, et al. Protein Bioelectronics: A Review of What we Do and Do Not Know. Reports on Progress in Physics. 2018;81:026601
38. 38. Mondal PC, Fontanesi C, Waldeck DH, et al. Spin-dependent transport through chiral molecules studied by spin-dependent electrochemistry. Accounts of Chemical Research. 2016;49:2560-2568
39. 39. Gutierrez R, Díaz E, Naaman R, et al. Spin-selective transport through helical molecular systems. Physical Review B. 2012;85:81404
40. 40. Fert A. Nobel lecture: Origin, development, and future of spintronics. Reviews of Modern Physics. 2008;80:1517-1530
41. 41. Baibich MN, Broto JM, Fert A, et al. Giant Magnetoresistance of (001)Fe/(001)Cr magnetic Superlattices. Physical Review Letters. 1988;61:2472-2475
42. 42. Fabian J, Das Sarma S, Žutić I. Spintronics fundamentals and applications. 2004, 2004;76. DOI: 10.1103/RevModPhys.76.323 [Epub ahead of print]
43. 43. Naaman R, Waldeck DH. Spintronics and Chirality: Spin Selectivity in Electron Transport through Chiral Molecules. Annual Review of Physical Chemistry. 2015;66:263-284
44. 44. Mishra D, Markus TZ, Naaman R, et al. Spin-dependent electron transmission through bacteriorhodopsin embedded in purple membrane. Proceedings of the National Academy of Sciences. 2013;110:14872-14876
45. 45. Einati H, Mishra D, Friedman N, et al. Light-controlled spin filtering in bacteriorhodopsin. Nano Letters. 2015;15:1052-1056
46. 46. Roy P, Kantor-Uriel N, Mishra D, et al. Spin-controlled photoluminescence in hybrid nanoparticles purple membrane system. ACS Nano. 2016;10:4525-4531
47. 47. Dong R, Cai Y, Yang Y, et al. Photocatalytic micro/nanomotors: From construction to applications. 2018. DOI: 10.1021/acs.accounts.8b00249 [Epub ahead of print]
48. 48. Dong R, Wang C, Wang Q , et al. ZnO-based microrockets with light-enhanced propulsion. Nanoscale. 2017;9:15027-15032
49. 49. JGS M, Mayorga-Martinez CC, Wang H, et al. Nano/microrobots meet electrochemistry. Advanced Functional Materials. 2017;27. DOI: 10.1002/adfm.201604759 [Epub ahead of print]
50. 50. Sengupta S, Ibele ME, Sen A. Fantastic voyage: Designing self-powered nanorobots. Angewandte Chemie International Edition. 2012;51:8434-8445
51. 51. Sharma NN, Mittal RK. Nanorobot movement: Challenges and biologically inspired solutions. International Journal of Smart Sensing and Intelligent Systems. 2008;1:87-109
52. 52. Wang B, Zhang Y, Zhang L. Recent progress on micro- and nano-robots: Towards in vivo tracking and localization. Quantitative Imaging in Medicine and Surgery. 2018;8:461-479
53. 53. Wu Y, Si T, Shao J, et al. Near-infrared light-driven Janus capsule motors: Fabrication, propulsion, and simulation. Nano Research. 2016;9:3747-3756
54. 54. Ummat A, Dubey A, Sharma G, Mavroidis C. Bio Nanorobotics: State of the Art and Future Challenges. In: Yarmush ML, editor. Tissue Engineering and Artificial Organs (The Biomedical Engineering Handbook). CRC Press. 2006:1-42
55. 55. Yang JF, Zhou L, Han Q , et al. Bias-controlled giant magnetoresistance through cyclopentadienyl-iron multidecker molecules. Journal of Physical Chemistry C. 2012;116:19996-20001
56. 56. Zhu J, Luo Z, Wu S, et al. Magnetic graphene nanocomposites: Electron conduction, giant magnetoresistance and tunable negative permittivity. Journal of Materials Chemistry. 2012;22:835-844
57. 57. Geng R, Luong HM, Daugherty TT, et al. A review on organic spintronic materials and devices: II. Magnetoresistance in organic spin valves and spin organic light emitting diodes. Journal of Science: Advanced Materials and Devices. 2016;1:256-272
58. 58. Geng R, Daugherty TT, Do K, et al. A review on organic spintronic materials and devices: I. magnetic field effect on organic light emitting diodes. Journal of Science: Advanced Materials and Devices. 2016;1:128-140
59. 59. Joshi VK. Spintronics: A contemporary review of emerging electronics devices. Engineering Science and Technology: An International Journal. 2016;19:1503-1513
60. 60. Xu X. A brief review of ferroelectric control of magnetoresistance in organic spin valves. Journal of Materials. 2018;4:1-12
61. 61. Hao H, Zheng X, Song L, et al. Electrostatic spin crossover in a molecular junction of a single-molecule magnet Fe2. Physical Review Letters. 2012;108:017202
62. 62. Sarkar S, Tarafder K, Oppeneer PM, et al. Spin-crossover in cyanide-based bimetallic coordination polymers—Insight from first-principles calculations. Journal of Materials Chemistry. 2011;21:13832
63. 63. Nakamura M, Takahashi M. Spin crossover in Iron(III) porphyrins involving the intermediate-spin state. In: Mössbauer Spectroscopy. Hoboken, New Jersey: John Wiley & Sons, Inc. pp. 177-201
64. 64. Huang B, Si C, Lee H, et al. Intrinsic half-metallic BN–C nanotubes. Applied Physics Letters. 2010;97:043115
65. 65. Parida P, Basheer EA, Pati SK. Cyclopentadienyl-benzene based sandwich molecular wires showing efficient spin filtering, negative differential resistance, and pressure induced electronic transitions. Journal of Materials Chemistry. 2012;22:14916
66. 66. Zhao W, Zou D, Sun Z, et al. Mechanical tuning of giant magnetoresistance and spin filtering in manganese diporphyrin-based molecular junction. ChemElectroChem. 2019;6:421-429
67. 67. Blakesley JC, Neher D. Relationship between energetic disorder and open-circuit voltage in bulk heterojunction organic solar cells. Physical Review B. 2011;84:075210
68. 68. Zeng J, Chen KQ. Spin filtering, magnetic and electronic switching behaviors in manganese porphyrin-based spintronic devices. Journal of Materials Chemistry C. 2013;1:4014-4019
69. 69. An YP, Yang Z, Ratner MA. High-efficiency switching effect in porphyrin-ethyne-benzene conjugates. The Journal of Chemical Physics. 2011;135:1-8
70. 70. Sedghi G, Sawada K, Esdaile LJ, et al. Single molecule conductance of porphyrin wires with ultralow attenuation. Journal of the American Chemical Society. 2008;130:8582-8583
71. 71. Sedghi G, García-Suárez VM, Esdaile LJ, et al. Long-range electron tunnelling in oligo-porphyrin molecular wires. Nature Nanotechnology. 2011;6:517-523
72. 72. Friesen BA, Wiggins B, McHale JL, et al. Differing HOMO and LUMO mediated conduction in a porphyrin nanorod. Journal of the American Chemical Society. 2010;132:8554-8556
73. 73. Cho WJ, Cho Y, Min SK, et al. Chromium porphyrin arrays as spintronic devices. Journal of the American Chemical Society. 2011;133:9364-9369
74. 74. Wende H, Bernien M, Luo J, et al. Substrate-induced magnetic ordering and switching of iron porphyrin molecules. Nature Materials. 2007;6:516-520
75. 75. Scheybal A, Ramsvik T, Bertschinger R, et al. Induced magnetic ordering in a molecular monolayer. Chemical Physics Letters. 2005;411:214-220
76. 76. Chen Y, Prociuk A, Perrine T, et al. Spin-dependent electronic transport through a porphyrin ring ligating an $\mathrm{Fe}(\mathrm{II})$ atom: An ab initio study. Physical Review B. 2006;74:245320
77. 77. Wäckerlin C, Chylarecka D, Kleibert A, et al. Controlling spins in adsorbed molecules by a chemical switch. Nature Communications. 2010;1:61
78. 78. Li J, Merino-Díez N, Carbonell-Sanromà E, et al. Survival of spin state in magnetic porphyrins contacted by graphene nanoribbons. Science Advances. 2018;4:eaaq0582
79. 79. Lewandowska K, Rosiak N, Bogucki A, et al. Supramolecular complexes of graphene oxide with porphyrins: An interplay between electronic and magnetic properties. Molecules. 2019;24:688
80. 80. Bentley R. From optical activity in quartz to chiral drugs: Molecular handedness in biology and medicine. Perspectives in Biology and Medicine. 1995;38:188-229
81. 81. Carmeli I, Kumar KS, Heifler O, et al. Spin selectivity in electron transfer in photosystem I. Angewandte Chemie International Edition. 2014;53:8953-8958
82. 82. Michaeli K, Kantor-Uriel N, Naaman R, et al. The electron’s spin and molecular chirality—How are they related and how do they affect life processes? Chemical Society Reviews. 2016;45:6478-6487
83. 83. Li Y, Lin T, Luo Y, et al. A smart and versatile theranostic nanomedicine platform based on nanoporphyrin. Nature Communications. 2014;5:4712
84. 84. Babel S, Mathur S. Nanorobotics—Headway towards dentistry. International Journal of Research in Science & Technology. 2011;1:3
85. 85. Divya U. Nanoparticles: An Emerging Trend in Dentistry. 2017 DOI: 10.5005/jp-journals-10037-1117 [Epub ahead of print]
86. 86. Lyutakov O, Hejna O, Solovyev A, et al. Polymethylmethacrylate doped with porphyrin and silver nanoparticles as light-activated antimicrobial material. RSC Advances. 2014;4:50624-50630
87. 87. González-Delgado JA, Castro PM, Machado A, et al. Hydrogels containing porphyrin-loaded nanoparticles for topical photodynamic applications. International Journal of Pharmaceutics. 2016;510:221-231
88. 88. Konan YN, Gurny R, Allémann E. State of the art in the delivery of photosensitizers for photodynamic therapy. Journal of Photochemistry and Photobiology B: Biology. 2002;66:89-106
89. 89. Ion R-M, Cocina G-C, Iantovics BL, et al. TPPS4 nanotubes architecture for nanorobots with application in cerebral aneurysm. In: AIP Conference Proceedings. 2009;1117:201-208
90. 90. Park JH, Lach S, Polev K, et al. Metal-organic framework ‘swimmers’ with energy-efficient autonomous motility. ACS Nano. 2017;11:10914-10923
91. 91. Serrà A, Vázquez-mariño G, García-torres J, et al. Magnetic actuation of multifunctional nanorobotic platforms to induce cancer cell death. Death Advanced Biosystems. 2018;1700220:1-9
92. 92. Vidotti M, Carvalhal RF, Mendes RK, et al. Biosensors based on gold nanostructures. 2011;22:3-20
93. 93. Gu H-Y, Yu A-M, Chen H-Y. Direct electron transfer and characterization of hemoglobin immobilized on a Au colloid–cysteamine-modified gold electrode. Journal of Electroanalytical Chemistry. 2001;516:119-126
94. 94. Ju H, Liu S, Ge B, et al. Electrochemistry of cytochrome c immobilized on colloidal gold modified carbon paste electrodes and its electrocatalytic activity. Electroanalysis. 2002;14:141-147
95. 95. Zhao X, Mai Z, Kang X, et al. Clay–chitosan–gold nanoparticle nanohybrid: Preparation and application for assembly and direct electrochemistry of myoglobin. Electrochimica Acta. 2008;53:4732-4739
96. 96. Bunea A-I, Pavel I-A, David S, et al. Modification with hemeproteins increases the diffusive movement of nanorods in dilute hydrogen peroxide solutions. Chemical Communications. 2013;49:8803-8805
97. 97. Pavel IA, Bunea AI, David S, et al. Nanorods with biocatalytically induced self-electrophoresis. ChemCatChem. 2014;6:866-872
98. 98. Sun M, Mi W. Progress in organic molecular/ferromagnet spinterfaces: Towards molecular spintronics. Journal of Materials Chemistry C. 2018;6:6619-6636
99. 99. Ormaza M, Abufager P, Verlhac B, et al. Controlled spin switching in a metallocene molecular junction. Nature Communications. 2017;8:1974
100. 100. Wäckerlin C, Tarafder K, Girovsky J, et al. Ammonia coordination introducing a magnetic moment in an on-surface low-spin porphyrin. Angewandte Chemie International Edition. 2013;52:4568-4571
101. 101. Jungfleisch MB, Zhang W, Hoffmann A. Perspectives of antiferromagnetic spintronics. Physics Letters A. 2018;382:865-871
102. 102. Soto F, Chrostowski R. Frontiers of medical micro/nanorobotics: In vivo applications and commercialization perspectives toward clinical uses. Frontiers in Bioengineering and Biotechnology. 2018;6:170

Written By

David M. Lopes, Juliana C. Araujo-Chaves, Lucivaldo R. Menezes and Iseli L. Nantes-Cardoso

Submitted: December 3rd, 2018 Reviewed: April 4th, 2019 Published: May 10th, 2019