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WIREs Nanomed Nanobiotechnol

Viral‐based nanomaterials for plasmonic and photonic materials and devices

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Over the last decade, viruses have established themselves as a powerful tool in nanotechnology. Their proteinaceous capsids benefit from biocompatibility, chemical addressability, and a variety of sizes and geometries, while their ability to encapsulate, scaffold, and self‐assemble enables their use for a wide array of purposes. Moreover, the scaling up of viral‐based nanotechnologies is facilitated by high capsid production yield and speed, which is particularly advantageous when compared with slower and costlier lithographic techniques. These features enable the bottom‐up fabrication of photonic and plasmonic materials, which relies on the precise arrangement of photoactive material at the nanoscale to control phenomena such as electromagnetic wave propagation and energy transfer. The interdisciplinary approach required for the fabrication of such materials combines techniques from the life sciences and device engineering, thus promoting innovative research. Materials with applications spanning the fields of sensing (biological, chemical, and physical sensors), nanomedicine (cellular imaging, drug delivery, phototherapy), energy transfer and conversion (solar cells, light harvesting, photocatalysis), metamaterials (negative refraction, artificial magnetism, near‐field amplification), and nanoparticle synthesis are considered with exclusive emphasis on viral capsids and protein cages.

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  • Biology‐Inspired Nanomaterials > Protein and Virus‐Based Structures
Sizes, shapes, and functionalities of viral capsids. (a) Capsids exist in various sizes, geometrical shapes, and possess unique surface irregularities. Most capsids adopt either a spherical or helical structure, with geometries varying from icosahedral to cylindrical. Paramecium bursaria chlorella virus type 1 (left‐most), Murine polyoma virus (center top), Cowpea mosaic virus (CPMV) (center, below Murine polyoma virus), Cowpea chlorotic mottle virus (center, below CPMV), Satelite tobacco mosaic virus (center bottom), a section of the rod‐shaped tobacco mosaic virus (top right), and Sulfolobus turreted icosahedral virus (bottom right). (Reprinted with permission from Douglas and Young (). Copyright 2006 AAAS). (b) Capsids can serve as encapsulating, interfacing, and scaffolding agents. These functionalities have numerous applications in the field of nanotechnology. (Reprinted with permission from Douglas and Young (). Copyright 2006 AAAS)
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Virus‐templated plasmonic nanoparticle (NP) fabrication. (a) Crystal structure of pyrococcus furiosus ferritin capsid and residue‐coordinated silver ions. E, D, H, and mostly M residues are involved in the coordination. (Reprinted with permission from Kasyutich et al. (). Copyright 2010 American Chemical Society). (b) AgNP formation scheme based on information collect from the crystal structure to the left. (Reprinted with permission from Kasyutich et al. (). Copyright 2010 American Chemical Society). (c) Simultaneous reduction of Au and Pd on the surface of tobacco mosaic virus (TMV) rods produces NP alloys (Au:Pd) with variable composition. (Reprinted with permission from Lim et al. (). Copyright 2010 Hindawi Publishing Corporation). (d) Genetically engineered P22 capsids can nucleate the formation of cadmium sulfide nanoparticles (CdS NPs) on specific residues in the interior of the capsid. Subsequently, formation of gold NPs can occur on the exterior of the capsid via residues present in the wild‐type sequence of the capsid. (Reprinted with permission from Zhou, Bedwell et al. (). Copyright 2015 The Royal Society of Chemistry). (e) Coating of negative Cowpea mosaic virus (CPMV) capsids with positive poly(allylamine) hydrochloride polymer can nucleate the formation of a thin layer of gold over the surface of the capsid. Gold ion adsorption on the polymer and slow reduction is key for the formation of a continuous layer. (Reprinted with permission from Aljabali, Lomonossoff, and Evans (). Copyright 2011 American Chemical Society). (f) A peptide sequence isolated via phage display studies and immobilized to a carbon substrate nucleates the formation of twisted silver nanowires in the presence of HEPES and light. Such unique structures have not yet been observed using peptide templates. (Reprinted with permission from Carter, Ackerson, and Feldheim (). Copyright 2010 American Chemical Society)
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One‐dimensional/two‐dimensional/two‐dimensional (1D/2D/3D) materials with optical properties. (a) Coassembly of aFer and PAMAM dendrimers generate superlattice with tunable lattice constant and lattice structure. Varying dendrimer size can control the lattice constant, while varying dendrimer generation and the solution ionic strength can control the lattice structure. (Reprinted with permission from Liljeström et al. (). Copyright 2015 American Chemical Society). (b) Tobacco mosaic virus (TMV) modified with poly‐His at the C‐terminus self‐assembles into 1D‐elongated rafts of rods and 2D hexagonally packed arrays of disks depending on the pH and ionic strength. (Reprinted with permission from Bruckman et al. (). Copyright 2011 American Chemical Society). (c) A 2D DNA origami sheet can serve as a command surface for the attachment of plasmonic particles and dye‐containing MS2 viral capsids. Hybridization schemes afford tight control over the nanoparticle (NP)‐capsid distance and allow the study of plasmonic near fields on the neighboring dye as a function of distance. (Reprinted with permission from Wang et al. (). Copyright 2014 American Chemical Society). (d) Labeling of an MS2 capsid with fluorophore‐tagged DNA strands of various base‐pair lengths. After encapsulation of a plasmonic NP in MS2, this platform can be used to study the effect of plasmonic near fields on dye emission as a function of dye‐NP distance. (Reprinted with permission from Capehart et al. (). Copyright 2013 American Chemical Society). (e) M13 phages assemble into smectic helicoidal filament bundles that expand or contract with changes in temperature. These PC structures can achieve the full range of red‐green‐blue (RGB) colors on exposure to heat‐producing potentials. (Reprinted with permission from Kim et al. (). Copyright 2015 Nature Publishing Group). (f) M13 rods adopt a chiral nematic liquid crystal phase and can be infiltrated with hydrogel precursors. After polymerization and in‐gel etching of the phages, void spaces left behind generate an inverse chiral nematic phase. (Reprinted with permission from Pei et al. (). Copyright 2015 American Chemical Society)
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Meta‐molecules and three‐dimensional (3D) metamaterials. (a) Electrostatic adsorption of plasmonic nanoparticles (NPs) onto the face of the tobacco mosaic virus (TMV) disk can take the shape of a ring or a doughnut, depending on the pH. (Reprinted with permission from Zahr and Blum (). Copyright 2012 American Chemical Society). (b) A red shift of the plasmon band along with a novel band at higher energies is suggestive of plasmon coupling between particles that motivate further research into magnetic properties due to ring‐like charge displacement. (Reprinted with permission from Zahr and Blum (). Copyright 2012 American Chemical Society). (c) A Cowpea mosaic virus (CPMV) capsid decorated with plasmonic particles on its surface was modeled upon interaction with a plasmon‐inducing field. Both electric and magnetic responses were elicited, possibly due to plasmon coupling and plasmon‐induced charge displacement, respectively. (Reprinted with permission from Fontana et al. (). Copyright 2014 John Wiley & Sons, Inc). (d) Effective medium theory calculations determined the index of refraction of a binary alloy of interpenetrating diamond lattices of gold nanoparticles (AuNPs) and spherical viral capsids. Indeed, a negative refractive index was achieved and was shown to span the entire visible regime upon tuning of the electric permittivity of the capsid. (Reprinted with permission from Yannopapas (). Copyright 2015 Elsevier). (e) This binary alloy material displayed an eightfold electric field enhancement after the passage of an incident wave through a thin slab of this material, suggesting near‐field amplification. (Reprinted with permission from Yannopapas (). Copyright 2015 Elsevier). (f) Cowpea chlorotic mottle virus (CCMV) and avidin self‐assemble into a 3D structure that can be further functionalized with AuNPs (or other nanoobjects) at the specific sites of the virus or the avidin, thus producing a stable 3D optical material. (Reprinted with permission from Liljeström et al. (). Copyright 2014 Nature Publishing Group). (g) Temperature drives the transition between the chiral nematic liquid crystal phase of M13 and relatively disordered phase. AuNRs are shown to align along the phage main axis and induce changes in circular dichroism absorption upon heating/cooling. (Reprinted with permission from Liu et al. (). Copyright 2016 Materials Research Society). (h) Dendrons and MFs can coassemble in an fcc superlattice with magnetic properties. Ultra violet (UV) irradiation breaks the dendritic arms and releases the particles from the lattice. (Reprinted with permission from Kostiainen et al. (). Copyright 2011 American Chemical Society). (i) The hysteresis curves of the magnetic supperlatice shows that significantly lower magnetic fields are required to invert magnetization (green curve) compared with free particles (black and red curves). (Reprinted with permission from Kostiainen et al. (). Copyright 2011 American Chemical Society)
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Light harvesting and photocatalysis. (a) The organic landscape on the surface of the M13 phage can direct energy transfer between amine‐conjugated porphyrins by exploiting electronic coupling between residues and excited porphyrins. Negatively charged, positively charged, neutral hydrophilic, and hydrophobic residues are highlighted in red, blue, yellow, and white, respectively. (Reprinted with permission from Nam, Shin et al. (). Copyright 2010 American Chemical Society). (b) A tobacco mosaic virus (TMV) circular permutant in the disk phase can be conjugated with either Texas Red donor (green dots) or Alex Fluor 647 acceptor (red dots) to yield highly symmetric fluorophore arrangements. Energy transfer is evidenced by the changes in the emission peak intensities between donor and donor–acceptor systems. (Reprinted with permission from Dedeo et al. (). Copyright 2010 American Chemical Society). (c) Coassembly of Oregon Green 488 donor‐ and Alexa Fluor 594 acceptor‐tagged monomers into chiral rods presents another geometry that allows energy transfer. Energy transfer can occur through multiple paths which can be deconvoluted through kinetic studies. (Reprinted with permission from Miller et al. (). Copyright 2007 American Chemical Society). (d) Porphyrin‐conjuagted M13 phages were functionalized with IrO2‐binding peptide. An IrO2 layer was grown around the well‐spaced porphyrins, which promoted effective charge transfer between the oxidized photosensitizer and the catalyst. (Reprinted with permission from Nam, Magyar et al. (). Copyright 2010 Nature Publishing Group). (e) Plasmon‐assisted photodegradation of methylene blue by cadmium sulfide nanoparticles (CdS NPs) (green curve) exhibits rates one order of magnitude higher compared with gold‐coated capsids alone (red curve). (Reprinted with permission from Zhou, Bedwell et al. (). Copyright 2015 The Royal Society of Chemistry)
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Solid‐state and dye‐sensitized solar cells. (a) Annealing of M13 phages coated with Ti precursors and embedded in a cellulose polymer produced porous anatase TiO2 NW networks devoid of phage. These porous networks were be filled with electron‐donating materials (dye or perovskites) and enhance electron lifetimes by reducing the opportunity for electron recombination. (Reprinted with permission from Chen et al. (). Copyright 2015 American Chemical Society). (b) Diagram of electron transfer in a dye‐sensitized solar cells (DSSC). (Reprinted with permission from Chen et al. (). Copyright 2015 American Chemical Society). (c) Porous nanowires 30‐ and 40‐nm wide display larger electron diffusion lengths than the nanoparticle (NP)‐based DSSC. (Reprinted with permission from Chen et al. (). Copyright 2015 American Chemical Society). (d) Addition of plasmonic NPs to the M13‐templated TiO2 nanowires (NWs) enhances the photon flux on nearby dyes and improves carrier generation and therefore subsequent charge separation in a similar DSSC. (Reprinted with permission from Chen et al. (). Copyright 2013 American Chemical Society). (e) Ferritin cages afford selective adsorption of silica‐coated gold nanoparticles (AuNPs) onto Ti substrates used for the fabrication of DSSCs. (Reprinted with permission from Saijo et al. (). Copyright 2013 The Japan Society for Applied Physics). (f) Virus‐templated TiO2 NWs provide direct pathways for charge transport in the active layer of thin‐film solar cells. Addition of plasmonic particles enhances photon flux onto nearby quantum dots which in turn enhances charge generation. (Reprinted with permission from Dorval Courchesne et al. (). Copyright 2015 American Chemical Society)
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Bioimaging via fluorescence or scattering. (a) Cowpea mosaic virus (CPMV)‐Cy5 uptake by HeLa cells confirmed via colocalization studies of CPMV‐Cy5 (red), nuclei (blue), endolysosomes (green). CPMV is known to interact with membrane vimentin membrane receptors, which may facilitate cell entry. (Reprinted with permission from Wen, Infusino et al. (). Copyright 2015 American Chemical Society). (b) An M13‐fluorophore complex conjugated to antibacterial antibodies can differentiate between bacterial strains and whole body diffuse fluorescence can localize the site of infection in living mice. (Reprinted with permission from Bardhan, Ghosh, and Belcher (). Copyright 2014. John Wiley & Sons, Inc). (c) High‐yield encapsulation of fluorescent proteins inside Qβ capsids is made possible by anchoring proteins to the inner membrane of the capsid via complementary RNA strands prior to coassembly. (Reprinted with permission from Rhee et al. (). Copyright 2011 American Chemical Society). (d) Respiratory syncytial virus (RSV) capsid was functionalized with gold nanoparticles (AuNPs) using biotin‐streptavidin chemistry to image infection via dark‐field microscopy. (Reprinted with permission from Wan et al. (). Copyright 2014 Nature Publishing Group). (e) Viral capsids coated with a thin layer of gold act as biochemical sensors in two ways: (1) they can transfer plasmon energy to neighboring biomolecules that have overlapping absorption bands and (2) they can act as surface‐enhanced Raman scattering (SERS) sensors due to the strong near‐field enhancements generated by the irregular surface of the capsids. (Reprinted with permission from Hong et al. (). Copyright 2015 Nature Publishing Group)
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Magnetic contrast bioimaging, phototherapy, and photocatalysis. (a) Magneto‐ferritin (MF) superlattice exhibits larger relaxivity rates when T2‐weighted, making it an ideal candidate for magnetic resonance imaging. (Reprinted with permission from Kostiainen et al. (). Copyright 2013 Nature Publishing Group). (b) Two‐dimensional magnetic resonance images are stacked to produce a three‐dimensional (3D) reconstruction of the superlattice dispersion in a gel medium. (Reprinted with permission from Kostiainen et al. (). Copyright 2013 Nature Publishing Group). (c) Cowpea chlorotic mottle virus (CCMV) capsid geometries dictate the arrangement of ZnPc inside the capsid for different photodynamic therapy (PDT) results. The T = 1 geometry produces ZnPc nanoparticles (NPs) while the T = 3 geometry generates regularly spaced ZnPc molecules following the symmetry of the capsid. (Reprinted with permission from Luque et al. (). Copyright 2014 The Royal Society of Chemistry). (d) Tobacco mosaic virus (TMV) rods containing ZnPor required significantly less porphyrin to produce 50% cell death upon PDT. (Reprinted with permission from Lee et al. (). Copyright 2016 American Chemical Society). (e) Adeno‐associated virus (AAV) can be designed to display a phytochrome interacting factor (PIF) upon red‐light exposure. Phytochromes can subsequently bind the capsid and translocate it to the nucleus, where capsid cargo can be released after degradation or capsid disassembly. The ratio of near‐infrared (NIR) to red light can tune the amount material translocated, while patterned illumination with a photomask can target specific cells. (Reprinted with permission from Gomez et al. (). Copyright 2016 American Chemical Society)
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surface‐enhanced Raman scattering (SERS)‐based sensors. (a) Attachment of gold nanoparticles (AuNPs) to surface thiols on Cowpea mosaic virus produces plasmonic nanoclusters. (Reprinted with permission from Lebedev et al. (). Copyright 2016 Elsevier). (b) Strong near‐field amplifications due to the number of nanoparticles (NPs) makes this platform sensitive to DNA Raman signatures in the 1500–1650 cm−1 region, with unique signatures for different DNA content. (Reprinted with permission from Lebedev et al. (). Copyright 2016 Elsevier). (c) M13 modified with antibody and plasmonic nanocubes can recognize specific targets and produce Raman signals from NP‐bound reporter molecules. (Reprinted with permission from Lee et al. (). Copyright 2014. John Wiley & Sons, Inc). (d) These plasmon coupling‐enhanced signals are sensitive to single‐digit pg/mL concentrations and can be observed via scanning electron microscopy (SEM) on target probes used to separate unbound from bound AuNC‐phages. (Reprinted with permission from Lee et al. (). Copyright 2014. John Wiley & Sons, Inc). (e) M13 modified with gold‐coated iron oxide nanoparticles (IONPs) are clustered using magnets and polymerized to produce tightly packed bundles. After calcination, the sepsis antibodies coated on the NPs are revealed allowing biomarkers to come in close contact with the SERS platform and produce strong biomarker Raman signatures. (Reprinted with permission from Nguyen et al. (). Copyright 2016 Elsevier). (f) Successful sensing was evidenced for three antibody–antigen systems. (Reprinted with permission from Nguyen et al. (). Copyright 2016 Elsevier). (g) Four different spherical capsids coated with a thin layer of gold possess unique multimodal spectral features due to each capsid's distinct surface irregularities. Band resonances span the entire visible region. (Reprinted with permission from Hong et al. (). Copyright 2015 Nature Publishing Group). (h) Amphiphatic peptide derived from hepatitis C virus NS5A protein destabilizes lipovesicles and drives the formation of a stable bilayer on the gold surface of surface plasmon resonance (SPR) chips for the analysis of biochemical interactions of otherwise insoluble transmembrane elements. (Reprinted with permission from Cho et al. (). Copyright 2007 American Chemical Society)
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Sensors based on photonic crystals, plasmon absorption and plasmon coupling. (a) Modified M13 phages self‐assemble into smectic helicoidal nanofilament bundles of various diameters and fiber spacings via a pulling method. Swelling or shrinking of bundles upon adsorption of volatile organic compounds produced by cells cause changes in coherent light scattering, inducing cell‐specific color‐coded photonic signature on the film stripes. (Reprinted with permission from Moon et al. (). Copyright 2017 The Royal Society of Chemistry). (b) DNA‐ and antibody‐functionalized M13 can detect femtomolar concentrations of antigen via hybridization with DNA‐decorated gold nanoparticles (AuNPs). (Reprinted with permission from Lee et al. (). Copyright 2012 American Chemical Society). (c) Temperature drives the transition between a chiral nematic liquid crystal phase of M13 phages and a disordered nonchiral phase. Alignment of AuNRs along the M13 rods in the chiral phase produces circular dichroism absorption which is sensitive to single digit changes in temperature. (Reprinted with permission from Liu et al. (). Copyright 2015 American Chemical Society). (d) Vesicular phospholipid concentrations can be determined from the extent of plasmon coupling between AuNPs bound to neutravidin‐conjugated surface lipids. (Reprinted with permission from Feizpour et al. (). Copyright 2015 John Wiley & Sons, Inc). (e) Plasmon band shift upon z‐axis compression of nanoparticle (NP)‐containing Brome mosaic virus (BMV) capsid. The amount of strain is related to the amount of plasmon coupling between AuNPs encapsulated at well‐defined locations inside the BMV capsid. (Reprinted with permission from Zahedian et al. (). Copyright 2016 American Chemical Society). (f) Scattering spectra change dramatically upon varying the polarization of incident light, thus providing information on the axis of deformation. (Reprinted with permission from Zahedian et al. (). Copyright 2016 American Chemical Society). (g) M13 phages modified with integrins, a biotin‐like peptide, and an aspartate motif tightly bind cysteamine self‐assembled monolayers of surface plasmon resonance (SPR) chips, and provide attachment sites for overlying cells. More importantly, growth factors conjugated to the phages provide control over the chemical environment of the cells, thereby facilitating systematic study of their growth and morphology via SPR. (Reprinted with permission from Yoo et al. (). Copyright 2012 American Chemical Society)
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