How to cite this WIREs title:
WIREs Nanomed Nanobiotechnol

Impact Factor: 9.182

Viral chemistry: the chemical functionalization of viral architectures to create new technology

Advanced Review

Zhuo Chen, Na Li, Shaobo Li, Madushani Dharmarwardana, Anna Schlimme, Jeremiah J Gassensmith

Published Online: Dec 10 2015

DOI: 10.1002/wnan.1379

Full article on Wiley Online Library: HTML PDF

Can't access this content? Tell your librarian.

The modification of viruses using chemical conjugation techniques has brought the distant worlds of virology right into the center of nanotechnology. Viruses are naturally resilient biomolecules and this makes them exceptional templates for the creation of higher order polymers and as scaffolds for biological imaging and targeted drug delivery. In this review, we highlight progress in utilizing chemical strategies to interface viruses with synthetic polymers, to create bright bionanoparticles using synthetic fluorescent dyes, and how orthogonal chemical transformations allow for targeted drug delivery. WIREs Nanomed Nanobiotechnol 2016, 8:512–534. doi: 10.1002/wnan.1379 This article is categorized under: Diagnostic Tools > Diagnostic Nanodevices Diagnostic Tools > In Vivo Nanodiagnostics and Imaging Implantable Materials and Surgical Technologies > Nanomaterials and Implants Biology-Inspired Nanomaterials > Protein and Virus-Based Structures

(a) Targeting strategies using electrostatic (left) or biological interaction (right). PS: photosensitizer; NP: nanoparticle; PLL: poly‐L‐lysine; Sa: S. aureus cell; SpA: protein A; Ab: anti‐SpA‐mAb‐B; B: bitotin; StAv: streptavidin. (Reprinted with permission from Ref . Copyright 2007 American Chemical Society)

[ Normal View | Magnified View ]

The combination of CCMV and photosensitizer for PDT. (Left) FESEM image of CCMV‐PS‐biotin conjugate covering on the cell wall through complementary biological interaction; (upper middle) CCMV; (lower middle) zoomed in micrograph of targeted cell wall; (upper right) photosensitizer (Ru(bpy2)phen‐IA); (lower right) cartoon represents the ROS generation upon illumination on the CCMV‐PS conjugate. (Reprinted with permission from Ref . Copyright 2007 American Chemical Society)

[ Normal View | Magnified View ]

(a) Azido‐functionalized polymer hybrid Qβ particle coupled with Doxorubicin with hydrazone linker via CuAAC reaction. (b) in vivo Doxorubicin release profile from Qβ‐polymer conjugate at pH 5.5 and 7.4; (C) MTT assay for HeLa cell viability with particle conjugates and free Doxorubicin alone. (Reprinted with permission from Ref . Copyright 2011 American Chemical Society)

[ Normal View | Magnified View ]

Different chemical modification approaches of M13 virus and structures of small molecules that were covalently bonding to M13. (Reprinted with permission from Ref . Copyright 2010 American Chemical Society)

[ Normal View | Magnified View ]

Modification of PVX with PEG linker (SM(PEG)₄), Alexa Fluor 647 NHS ester and subsequent labeled by GE11 peptide. (Reprinted with permission from Ref . Copyright 2015 American Chemical Society)

[ Normal View | Magnified View ]

(a) Chemical structure of the bombesin analog covalently bound with a PEG linker. (b) Sythetic processes of Dye‐labeled CPMV–PEG and CPMV–PEG–bombesin. (Reprinted with permission from Ref . Copyright 2011 John Wiley and Sons)

[ Normal View | Magnified View ]

Synthesis of Fluorescein‐F56 complex and conjugation to CPMV. (Reprinted with permission from Ref . Copyright 2010 American Chemical Society)

[ Normal View | Magnified View ]

Scheme of ATRP of pDMAEMA within T93 Qβ interior. (Reprinted with permission from Ref . Copyright 2014 American Chemical Society)

[ Normal View | Magnified View ]

Scheme of internal initiator‐attachment followed by ATRP of pAEMA and crosslinked with bisacrylamide (bis). The final step demonstrated the appended amine groups functionalized with FITC and Gd complex. (Reprinted with permission from Ref . Copyright 2012 Nature Publishing Group)

[ Normal View | Magnified View ]

Scheme of ATRP of poly(OEGMA) on outer shell of Qβ. (Reprinted with permission from Ref . Copyright 2011 American Chemical Society)

[ Normal View | Magnified View ]

(a) Schematic presentation of the attachment of poly(2‐oxazoline) onto azide‐functionalized Qβ exterior. PBS represents phosphate‐buffered saline. (b) Molecular composition of poly(2‐oxazoline) derivatives possessing various amounts of alkyne attachment points. (Reprinted with permission from Ref . Copyright 2011 John Wiley and Sons)

[ Normal View | Magnified View ]

Scheme of ATRP of neoglycopolymer (1→3), fluorescein attached to polymer termini via alkyne‐azide coupling (3→5), and fluorescein‐labeled polymer attached to CPMV exterior(6→9). (Reprinted with permission from Ref . Copyright 2005 Royal Society of Chemistry)

[ Normal View | Magnified View ]

Azo conjugation strategies developed on VLPs. (a) The initial strategy developed by Francis and coworkers involving hetero‐Diels‐Alder to place substituents. (b) Second generation Francis azo coupling utilizing oximes to place substituents. (c) Wang azo coupling using an alkyne‐functionalized diazonium for CuAAC chemistry to place substituents.

[ Normal View | Magnified View ]

Crystallographically obtained structures of common VLPs Qβ, MS2, Cowpea Mosaic Virus (CPMV), Cowpea Chlorotic Mottle Virus (CCMV), and Tobacco Mosaic Virus (TMV). TMV is not illustrated to scale.

[ Normal View | Magnified View ]

Dual‐surface modified bacteriophage MS2 capsid with photosensitizer and targeting ligands for photodynamic therapy, which significantly and specifically killed target cells. (Reprinted with permission from Ref . Copyright 2010 American Chemical Society)

[ Normal View | Magnified View ]

References

Nam, KT, Kim, D‐W, Yoo, PJ, Chiang, C‐Y, Meethong, N, Hammond, PT, Chiang, Y‐M, Belcher, AM. Virus‐enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 2006, 312:885–888.
Chen, X, Gerasopoulos, K, Guo, J, Brown, A, Wang, C, Ghodssi, R, Culver, JN. Virus‐enabled silicon anode for lithium‐ion batteries. ACS Nano 2010, 4:5366–5372.
Pomerantseva, E, Gerasopoulos, K, Chen, X, Rubloff, G, Ghodssi, R. Electrochemical performance of the nanostructured biotemplated V2o5 cathode for lithium‐ion batteries. J Power Sources 2012, 206:282–287.
Nam, KT, Wartena, R, Yoo, PJ, Liau, FW, Lee, YJ, Chiang, Y‐M, Hammond, PT, Belcher, AM. Stamped microbattery electrodes based on self‐assembled M13 viruses. Proc Natl Acad Sci USA 2008, 105:17227–17231.
Royston, E, Ghosh, A, Kofinas, P, Harris, MT, Culver, JN. Self‐assembly of virus‐structured high surface area nanomaterials and their application as battery electrodes. Langmuir 2008, 24:906–912.
Scolaro, LM, Castriciano, MA, Romeo, A, Micali, N, Angelini, N, Lo Passo, C, Felici, F. Supramolecular binding of cationic porphyrins on a filamentous bacteriophage template: toward a noncovalent antenna system. J Am Chem Soc 2006, 128:7446–7447.
Miller, RA, Presley, AD, Francis, MB. Self‐assembling light‐harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J Am Chem Soc 2007, 129:3104–3109.
Nam, YS, Shin, T, Park, H, Magyar, AP, Choi, K, Fantner, G, Nelson, KA, Belcher, AM. Virus‐templated assembly of porphyrins into light‐harvesting nanoantennae. J Am Chem Soc 2010, 132:1462–1463.
Niu, Z, Bruckman, MA, Li, S, Lee, LA, Lee, B, Pingali, SV, Thiyagarajan, P, Wang, Q. Assembly of tobacco mosaic virus into fibrous and macroscopic bundled arrays mediated by surface aniline polymerization. Langmuir 2007, 23:6719–6724.
Stephanopoulos, N, Tong, GJ, Hsiao, SC, Francis, MB. Dual‐surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano 2010, 4:6014–6020.
Carette, N, Engelkamp, H, Akpa, E, Pierre, SJ, Cameron, NR, Christianen, PCM, Maan, JC, Thies, JC, Weberskirch, R, Rowan, AE, et al. A virus‐based biocatalyst. Nat Nanotechnol 2007, 2:226–229.
Patterson, DP, Schwarz, B, Waters, RS, Gedeon, T, Douglas, T. Encapsulation of an enzyme cascade within the bacteriophage P22 virus‐like particle. ACS Chem Biol 2014, 9:359–365.
Steinmetz, NF. Viral nanoparticles as platforms for next‐generation therapeutics and imaging devices. WIREs Nanomed Nanobiotechnol 2010, 6:634–641.
Dragnea, B, Chen, C, Kwak, E‐S, Stein, B, Kao, CC. Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses. J Am Chem Soc 2003, 125:6374–6375.
Qazi, S, Liepold, LO, Abedin, MJ, Johnson, B, Prevelige, P, Frank, JA, Douglas, T. P22 viral capsids as nanocomposite high‐relaxivity Mri contrast agents. Mol Pharm 2013, 10:11–17.
Stevens, TK, Palaniappan, KK, Ramirez, RM, Francis, MB, Wemmer, DE, Pines, A. Hypercest detection of a 129xe‐based contrast agent composed of cryptophane‐a molecular cages on a bacteriophage scaffold. Magn Reson Med 2012, 69:1245–1252.
Brasch, M, Voets, IK, Koay, MST, Cornelissen, JJLM. Phototriggered cargo release from virus‐like assemblies. Faraday Discuss 2013, 166:47–57.
Tong, GJ, Hsiao, SC, Carrico, ZM, Francis, MB. Viral capsid DNA aptamer conjugates as multivalent cell‐targeting vehicles. J Am Chem Soc 2009, 131:11174–11178.
Steinmetz, NF. Viral nanoparticles in drug delivery and imaging. Mol Pharm 2013, 10:1–2.
Ohtake, N, Niikura, K, Suzuki, T, Nagakawa, K, Mikuni, S, Matsuo, Y, Kinjo, M, Sawa, H, Ijiro, K. Low Ph‐triggered model drug molecule release from virus‐like particles. ChemBioChem 2010, 11:959–962.
West, KR, Otto, S. Reversible covalent chemistry in drug delivery. Curr Drug Discov Technol 2005, 2:123–160.
Ma, Y, Nolte, RJM, Cornelissen, JJLM. Virus‐based nanocarriers for drug delivery. Adv Drug Deliver Rev 2012, 64:811–825.
Sitasuwan, P, Lee, LA, Li, K, Nguyen, HG, Wang, Q. Rgd‐conjugated rod‐like viral nanoparticles on 2d scaffold improve bone differentiation of mesenchymal stem cells. Front Chem 2014, 2:31.
Zan, X, Feng, S, Balizan, E, Lin, Y, Wang, Q. Facile method for large scale alignment of one dimensional nanoparticles and control over myoblast orientation and differentiation. ACS Nano 2013, 7:8385–8396.
Fowler, CE, Shenton, W, Stubbs, G, Mann, S. Tobacco mosaic virus liquid crystals as templates for the interior design of silica mesophases and nanoparticles. Adv Mater 2001, 13:1266–1269.
Radloff, C, Vaia, RA, Brunton, J, Bouwer, GT, Ward, VK. Metal nanoshell assembly on a virus bioscaffold. Nano Lett 2005, 5:1187–1191.
Hovlid, ML, Lau, JL, Breitenkamp, K, Higginson, CJ, Laufer, B, Manchester, M, Finn, MG. Encapsidated atom‐transfer radical polymerization in Qβ virus‐like nanoparticles. ACS Nano 2014, 8:8003–8014.
Manzenrieder, F, Luxenhofer, R, Retzlaff, M, Jordan, R, Finn, MG. Stabilization of virus‐like particles with poly(2‐oxazoline)S. Angew Chem Int Ed 2011, 50:2601–2605.
Speir, JA, Munshi, S, Wang, G, Baker, TS, Johnson, JE. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X‐ray crystallography and cryo‐electron microscopy. Structure 1995, 3:63–78.
Wei, N, Heaton, LA, Morris, TJ, Harrison, SC. Structure and assembly of turnip crinkle virus: Vi. Identification of coat protein binding sites on the RNA. J Mol Biol 1990, 214:85–95.
Butler, PJG. Self‐assembly of tobacco mosaic virus: the role of an intermediate aggregate in generating both specificity and speed. Phil Trans R Soc Lond 1999, 354:537–550.
Wang, Q, Lin, T, Tang, L, Johnson, JE, Finn, MG. Icosahedral virus particles as addressable nanoscale building blocks. Angew Chem Int Ed 2002, 41:459–462.
Lammers, T, Kiessling, F, Hennink, WE, Storm, G. Drug targeting to tumors: principles, pitfalls and (pre‐) clinical progress. J Control Release 2012, 161:175–187.
Soo Choi, H, Liu, W, Misra, P, Tanaka, E, Zimmer, JP, Itty Ipe, B, Bawendi, MG, Frangioni, JV. Renal clearance of quantum dots. Nat Biotechnol 2007, 25:1165–1170.
Prasuhn, DE, Singh, P, Strable, E, Brown, S, Manchester, M, Finn, MG. Plasma clearance of bacteriophage Qβ particles as a function of surface charge. J Am Chem Soc 2008, 130:1328–1334.
Schwarz, B, Douglas, T. Development of virus‐like particles for diagnostic and prophylactic biomedical applications. WIREs Nanomed Nanobiotechnol 2015, 7:722–735.
Stephanopoulos, N, Francis, MB. Choosing an effective protein bioconjugation strategy. Nat Chem Biol 2011, 7:876–884.
Debets, MF, van Berkel, SS, Dommerholt, J, Dirks, AJ, Rutjes, FPJT, van Delft, FL. Bioconjugation with strained alkenes and alkynes. Acc Chem Res 2011, 44:805–815.
Sunasee, R, Narain, R. Covalent and noncovalent bioconjugation strategies. In: Chemistry of Bioconjugates. Hoboken, NJ: John Wiley %26 Sons, Inc; 2014, 1–75. doi: 10.1002/9781118775882.ch1.
Francis, MB, Bernard, JML. Chemical strategies for the covalent modification of filamentous phage. Front Microbiol 2014, 5:734.
Chung, W‐J, Lee, D‐Y, Yoo, SY. Chemical modulation of M13 bacteriophage and its functional opportunities for nanomedicine. Int J Nanomedicine 2014, 9:5825–5836.
Bundy, BC, Swartz, JR. Efficient disulfide bond formation in virus‐like particles. J Biotechnol 2011, 154:230–239.
Golmohammadi, R, Fridborg, K, Bundule, M, Valegård, K, Liljas, L. The crystal structure of bacteriophage Qβ at 3.5 Å resolution. Structure 1996, 4:543–554.
Pauly, H. Über Die Konstitution Des Histidins. I. Mitteilung. Hoppe‐Seyler`s Z Physiol Chem 1904, 42:508–518.
Pauly, H. Zur Kenntnis Der Diazoreaktion Des Eiweißes. Hoppe‐Seyler`s Z Physiol Chem 1915, 94:284–290.
Hooker, JM, Kovacs, EW, Francis, MB. Interior surface modification of bacteriophage Ms2. J Am Chem Soc 2004, 126:3718–3719.
Schlick, TL, Ding, Z, Kovacs, EW, Francis, MB. Dual‐surface modification of the tobacco mosaic virus. J Am Chem Soc 2005, 127:3718–3723.
Kovacs, EW, Hooker, JM, Romanini, DW, Holder, PG, Berry, KE, Francis, MB. Dual‐surface‐modified bacteriophage Ms2 as an ideal scaffold for a viral capsid‐based drug delivery system. Bioconjug Chem 2007, 18:1140–1147.
Steinmetz, NF, Manchester, M. Pegylated viral nanoparticles for biomedicine: the impact of peg chain length on Vnp cell interactions in vitro and ex vivo. Biomacromolecules 2009, 10:784–792.
Fisher, KD, Stallwood, Y, Green, NK, Ulbrich, K, Mautner, V, Seymour, LW. Polymer‐coated adenovirus permits efficient retargeting and evades neutralising antibodies. Gene Ther 2001, 8:341–348.
Green, NK, Herbert, CW, Hale, SJ, Hale, AB, Mautner, V, Harkins, R, Hermiston, T, Ulbrich, K, Fisher, KD, Seymour, LW. Extended plasma circulation time and decreased toxicity of polymer‐coated adenovirus. Gene Ther 2004, 11:1256–1263.
Holder, PG, Finley, DT, Stephanopoulos, N, Walton, R, Clark, DS, Francis, MB. Dramatic thermal stability of virus–polymer conjugates in hydrophobic solvents. Langmuir 2010, 26:17383–17388.
Comellas‐Aragonès, M, de la Escosura, A, Dirks, AJ, van der Ham, A, Fusté‐Cuñé, A, Cornelissen, JJLM, Nolte, RJM. Controlled integration of polymers into viral capsids. Biomacromolecules 2009, 10:3141–3147.
Gupta, SS, Raja, KS, Kaltgrad, E, Strable, E, Finn, MG. Virus‐glycopolymer conjugates by copper(I) catalysis of atom transfer radical polymerization and azide‐alkyne cycloaddition. Chem Commun 2005, 34:4315–4317.
Raja, KS, Wang, Q, Gonzalez, MJ, Manchester, M, Johnson, JE, Finn, MG. Hybrid virus–polymer materials. 1. Synthesis and properties of peg‐decorated cowpea mosaic virus. Biomacromolecules 2003, 4:472–476.
Lucon, J, Edwards, E, Qazi, S, Uchida, M, Douglas, T. Atom transfer radical polymerization on the interior of the P22 capsid and incorporation of photocatalytic monomer crosslinks. Eur Polym J 2013, 49:2976–2985.
Lucon, J, Qazi, S, Uchida, M, Bedwell, GJ, LaFrance, B, Prevelige, PE, Douglas, T. Use of the interior cavity of the P22 capsid for site‐specific initiation of atom‐transfer radical polymerization with high‐density cargo loading. Nat Chem 2012, 4:781–788.
Pokorski, JK, Breitenkamp, K, Liepold, LO, Qazi, S, Finn, MG. Functional virus‐based polymer–protein nanoparticles by atom transfer radical polymerization. J Am Chem Soc 2011, 133:9242–9245.
Hong, V, Presolski, SI, Ma, C, Finn, MG. Analysis and optimization of copper‐catalyzed azide–alkyne cycloaddition for bioconjugation. Angew Chem Int Ed 2009, 48:9879–9883.
Astronomo, RD, Kaltgrad, E, Udit, AK, Wang, S‐K, Doores, KJ, Huang, C‐Y, Pantophlet, R, Paulson, JC, Wong, C‐H, Finn, MG, et al. Defining criteria for oligomannose immunogens for hiv using icosahedral virus capsid scaffolds. Chem Biol 2010, 17:357–370.
de Gennes, PG. Polymers at an interface; a simplified view. Adv Colloid Interface Sci 1987, 27:189–209.
Lewis, JD, Destito, G, Zijlstra, A, Gonzalez, MJ, Quigley, JP, Manchester, M, Stuhlmann, H. Viral nanoparticles as tools for intravital vascular imaging. Nat Med 2006, 12:354–360.
Destito, G, Yeh, R, Rae, CS, Finn, MG, Manchester, M. Folic acid‐mediated targeting of cowpea mosaic virus particles to tumor cells. Chem Biol 2007, 14:1152–1162.
Shukla, S, Ablack, AL, Wen, AM, Lee, KL, Lewis, JD, Steinmetz, NF. Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle potato virus X. Mol Pharm 2013, 10:33–42.
Lee, KL, Shukla, S, Wu, M, Ayat, NR, El Sanadi, CE, Wen, AM, Edelbrock, JF, Pokorski, JK, Commandeur, U, Dubyak, GR, et al. Stealth filaments: polymer chain length and conformation affect the in vivo fate of pegylated potato virus X. Acta Biomater 2015, 19:166–179.
Li, F, Wang, Q. Fabrication of nanoarchitectures templated by virus‐based nanoparticles: strategies and applications. Small 2014, 10:230–245.
Li, K, Nguyen, HG, Lu, X, Wang, Q. Viruses and their potential in bioimaging and biosensing applications. Analyst 2010, 135:21–27.
Bruckman, MA, Yu, X, Steinmetz, NF. Engineering Gd‐loaded nanoparticles to enhance mri sensitivity via T1 shortening. Nanotechnology 2013, 24:462001–462021.
Michael, AB, Xin, Y, Nicole, FS. Engineering Gd‐loaded nanoparticles to enhance Mri sensitivity via T1 shortening. Nanotechnology 2013, 24:462001.
Rae, CS, Wei Khor, I, Wang, Q, Destito, G, Gonzalez, MJ, Singh, P, Thomas, DM, Estrada, MN, Powell, E, Finn, MG, et al. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 2005, 343:224–235.
Brunel, FM, Lewis, JD, Destito, G, Steinmetz, NF, Manchester, M, Stuhlmann, H, Dawson, PE. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett 2010, 10:1093–1097.
Steinmetz, NF, Ablack, AL, Hickey, JL, Ablack, J, Manocha, B, Mymryk, JS, Luyt, LG, Lewis, JD. Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin‐releasing peptide receptors. Small 2011, 7:1664–1672.
Chariou, PL, Lee, KL, Wen, AM, Gulati, NM, Stewart, PL, Steinmetz, NF. Detection and imaging of aggressive cancer cells using an epidermal growth factor receptor (Egfr)‐Targeted filamentous plant virus‐based nanoparticle. Bioconjug Chem 2015, 26:262–269.
Li, K, Chen, Y, Li, S, Nguyen, HG, Niu, Z, You, S, Mello, CM, Lu, X, Wang, Q. Chemical modification of M13 bacteriophage and its application in cancer cell imaging. Bioconjug Chem 2010, 21:1369–1377.
Decuzzi, P, Godin, B, Tanaka, T, Lee, SY, Chiappini, C, Liu, X, Ferrari, M. Size and shape effects in the biodistribution of intravascularly injected particles. J Control Release 2010, 141:320–327.
Geng, Y, Dalhaimer, P, Cai, S, Tsai, R, Tewari, M, Minko, T, Discher, DE. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2007, 2:249–255.
Jennings, GT, Bachmann, MF. Immunodrugs: therapeutic Vlp‐based vaccines for chronic diseases. Annu Rev Pharmacol Toxicol 2009, 49:303–326.
Jegerlehner, A, Tissot, A, Lechner, F, Sebbel, P, Erdmann, I, Kündig, T, Bächi, T, Storni, T, Jennings, G, Pumpens, P, et al. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 2002, 20:3104–3112.
Ambühl, PM, Tissot, AC, Fulurija, A, Maurer, P, Nussberger, J, Sabat, R, Nief, V, Schellekens, C, Sladko, K, Roubicek, K, et al. A vaccine for hypertension based on virus‐like particles: preclinical efficacy and phase i safety and immunogenicity. J Hypertens 2007, 25:63–72.
Maurer, P, Jennings, GT, Willers, J, Rohner, F, Lindman, Y, Roubicek, K, Renner, WA, Müller, P, Bachmann, MF. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and phase I safety and immunogenicity. Eur J Immunol 2005, 35:2031–2040.
Tachibana, R, Harashima, H, Shono, M, Azumano, M, Niwa, M, Futaki, S, Kiwada, H. Intracellular regulation of macromolecules using Ph‐sensitive liposomes and nuclear localization signal: qualitative and quantitative evaluation of intracellular trafficking. Biochem Biophys Res Commun 1998, 251:538–544.
Gullotti, E, Yeo, Y. Extracellularly activated nanocarriers: a new paradigm of tumor targeted drug delivery. Mol Pharm 2009, 6:1041–1051.
Ulbrich, K, Etrych, T, Chytil, P, Pechar, M, Jelinkova, M, Rihova, B. Polymeric anticancer drugs with Ph‐controlled activation. Int J Pharm 2004, 277:63–72.
Suci, PA, Varpness, Z, Gillitzer, E, Douglas, T, Young, M. Targeting and photodynamic killing of a microbial pathogen using protein cage architectures functionalized with a photosensitizer. Langmuir 2007, 23:12280–12286.
Hooker, JM, O`Neil, JP, Romanini, DW, Taylor, SE, Francis, M. Genome‐free viral capsids as carriers for positron emission tomography radiolabels. Mol Imaging Biol 2008, 10:182–191.
Datta, A, Hooker, JM, Botta, M, Francis, MB, Aime, S, Raymond, KN. High relaxivity gadolinium hydroxypyridonate−viral capsid conjugates: nanosized Mri contrast agents 1. J Am Chem Soc 2008, 130:2546–2552.
Capehart, SL, ElSohly, AM, Obermeyer, AC, Francis, MB. Bioconjugation of gold nanoparticles through the oxidative coupling of ortho‐aminophenols and anilines. Bioconjug Chem 2014, 25:1888–1892.
Capehart, SL, Coyle, MP, Glasgow, JE, Francis, MB. Controlled integration of gold nanoparticles and organic fluorophores using synthetically modified Ms2 viral capsids. J Am Chem Soc 2013, 135:3011–3016.
Obermeyer, AC, Capehart, SL, Jarman, JB, Francis, MB. Multivalent viral capsids with internal cargo for fibrin imaging. PLoS One 2014, 9:e100678.
Carrico, ZM, Romanini, DW, Mehl, RA, Francis, MB. Oxidative coupling of peptides to a virus capsid containing unnatural amino acids. Chem Commun 2008, 10:1205–1207.
Farkas, ME, Aanei, IL, Behrens, CR, Tong, GJ, Murphy, ST, O`Neil, JP, Francis, MB. Pet imaging and biodistribution of chemically modified bacteriophage Ms2. Mol Pharm 2013, 10:69–76.
Stephanopoulos, N, Carrico, ZM, Francis, MB. Nanoscale integration of sensitizing chromophores and porphyrins with bacteriophage Ms2. Angew Chem Int Ed 2009, 48:9498–9502.
El Muslemany, KM, Twite, AA, ElSohly, AM, Obermeyer, AC, Mathies, RA, Francis, MB. Photoactivated bioconjugation between Ortho‐azidophenols and anilines: a facile approach to biomolecular photopatterning. J Am Chem Soc 2014, 136:12600–12606.
Garimella, PD, Datta, A, Romanini, DW, Raymond, KN, Francis, MB. Multivalent, high‐relaxivity Mri contrast agents using rigid cysteine‐reactive gadolinium complexes. J Am Chem Soc 2011, 133:14704–14709.
Wu, W, Hsiao, SC, Carrico, ZM, Francis, MB. Genome‐free viral capsids as multivalent carriers for taxol delivery. Angew Chem Int Ed 2009, 48:9493–9497.
Wu, M, Shi, J, Fan, D, Zhou, Q, Wang, F, Niu, Z, Huang, Y. Biobehavior in normal and tumor‐bearing mice of tobacco mosaic virus. Biomacromolecules 2013, 14:4032–4037.
Bruckman, MA, Hern, S, Jiang, K, Flask, CA, Yu, X, Steinmetz, NF. Tobacco mosaic virus rods and spheres as supramolecular high‐relaxivity Mri contrast agents. J Mater Chem B 2013, 1:1482–1490.
Bruckman, MA, Kaur, G, Lee, LA, Xie, F, Sepulveda, J, Breitenkamp, R, Zhang, X, Joralemon, M, Russell, TP, Emrick, T, et al. Surface modification of tobacco mosaic virus with “click” chemistry. ChemBioChem 2008, 9:519–523.
Yin, Z, Nguyen, HG, Chowdhury, S, Bentley, P, Bruckman, MA, Miermont, A, Gildersleeve, JC, Wang, Q, Huang, X. Tobacco mosaic virus as a new carrier for tumor associated carbohydrate antigens. Bioconjug Chem 2012, 23:1694–1703.
Hu, J, Wang, P, Zhao, X, Lv, L, Yang, S, Song, B, Wang, Q. Charge‐transfer interactions for the fabrication of multifunctional viral nanoparticles. Chem Commun 2014, 50:14125–14128.
Wang, Q, PONGKWAN, S, Lee, LA, Li, K, Nguyen, HG. Rgd‐Conjugated rod‐like viral nanoparticles on 2d scaffold improved bone differentiation of mesenchymal stem cells. Front Chem 2014, 2:31.
Chen, L, Zhao, X, Lin, Y, Huang, Y, Wang, Q. A supramolecular strategy to assemble multifunctional viral nanoparticles. Chem Commun 2013, 49:9678–9680.
Bruckman, MA, Liu, J, Koley, G, Li, Y, Benicewicz, B, Niu, Z, Wang, Q. Tobacco mosaic virus based thin film sensor for detection of volatile organic compounds. J Mater Chem 2010, 20:5715–5719.
Bruckman, MA, Jiang, K, Simpson, EJ, Randolph, LN, Luyt, LG, Yu, X, Steinmetz, NF. Dual‐modal magnetic resonance and fluorescence imaging of atherosclerotic plaques in vivo using Vcam‐1 targeted tobacco mosaic virus. Nano Lett 2014, 14:1551–1558.
Miller, RA, Stephanopoulos, N, McFarland, JM, Rosko, AS, Geissler, PL, Francis, MB. Impact of assembly state on the defect tolerance of TMV‐based light harvesting arrays. J Am Chem Soc 2010, 132:6068–6074.
Obermeyer, AC, Jarman, JB, Francis, MB. N‐terminal modification of proteins with O‐aminophenols. J Am Chem Soc 2014, 136:9572–9579.
Yin, Z, Comellas‐Aragones, M, Chowdhury, S, Bentley, P, Kaczanowska, K, BenMohamed, L, Gildersleeve, JC, Finn, MG, Huang, X. Boosting immunity to small tumor‐associated carbohydrates with bacteriophage Qβ capsids. ACS Chem Biol 2013, 8:1253–1262.
Mead, G, Hiley, M, Ng, T, Fihn, C, Hong, K, Groner, M, Miner, W, Drugan, D, Hollingsworth, W, Udit, AK. Directed polyvalent display of sulfated ligands on virus nanoparticles elicits heparin‐like anticoagulant activity. Bioconjug Chem 2014, 25:1444–1452.
Pokorski, JK, Hovlid, ML, Finn, MG. Cell targeting with hybrid Qβ virus‐like particles displaying epidermal growth factor. ChemBioChem 2011, 12:2441–2447.
Banerjee, D, Liu, AP, Voss, NR, Schmid, SL, Finn, MG. Multivalent display and receptor‐mediated endocytosis of transferrin on virus‐like particles. ChemBioChem 2010, 11:1273–1279.
Steinmetz, NF, Hong, V, Spoerke, ED, Lu, P, Breitenkamp, K, Finn, MG, Manchester, M. Buckyballs meet viral nanoparticles: candidates for biomedicine. J Am Chem Soc 2009, 131:17093–17095.
Kaltgrad, E, O`Reilly, MK, Liao, L, Han, S, Paulson, JC, Finn, MG. On‐virus construction of polyvalent glycan ligands for cell‐surface receptors. J Am Chem Soc 2008, 130:4578–4579.
Prasuhn, JDE, Yeh, RM, Obenaus, A, Manchester, M, Finn, MG. Viral Mri contrast agents: coordination of gd by native virions and attachment of Gd complexes by azide‐alkyne cycloaddition. Chem Commun 2007, 12:1269–1271.

Resources

Access to this WIREs title is by subscription only.

Recommend to Your
Librarian Now!

The latest WIREs articles in your inbox

Sign Up for Article Alerts