Abstract
As biological agents, viruses come in an astounding range of sizes, with varied shapes and surface morphologies. The structures of viral capsids are generally assemblies of hundreds of copies of one or a few proteins which can be harnessed for use in a wide variety of applications in biotechnology, nanotechnology, and medicine. Despite their complexity, many capsid types form as homogenous populations of precise geometrical assemblies. This is important in both medicine, where well-defined therapeutics are critical for drug performance and federal approval, and nanotechnology, where precise placement affects the properties of the desired material. Here we review the production of viruses and virus-like particles with methods for selecting and manipulating the size, surface chemistry, assembly state, and interior cargo of capsid. We then discuss many of the applications used in research today and the potential commercial and therapeutic products from engineered viral capsids.
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References
Abbing A, Blaschke UK, Grein S, Kretschmar M, Stark CMB, Thies MJW, Walter J, Weigand M, Woith DC, Hess J, Reier CO (2004) Efficient intracellular delivery of a protein and a low molecular weight substance via recombinant polyomavirus-like particles. J Biol Chem 279:27410–27421
Adolph KW, Butler PJG (1974) Studies on the assembly of a spherical plant virus: I. States of aggregation of the isolated protein. J Mol Biol 88:327–341
Aljabali AAA, Barclay JE, Lomonossoff GP, Evans DJ (2010) Virus templated metallic nanoparticles. Nanoscale 2:2596–2600
Aljabali AAA, Barclay JE, Cespedes O, Rashid A, Staniland SS, Lomonossoff GP, Evans DJ (2011a) Charge modified cowpea mosaic virus particles for templated mineralization. Adv Funct Mater 21:4137–4142
Aljabali AAA, Shah SN, Evans-Gowing R, Lomonossoff GP, Evans DJ (2011b) Chemically-coupled-peptide-promoted virus nanoparticle templated mineralization. Integr Biol 3:119–125
Aljabali AAA, Barclay JE, Steinmetz NF, Lomonossoff GP, Evans DJ (2012) Controlled immobilisation of active enzymes on the cowpea mosaic virus capsid. Nanoscale 4:5640–5645
Aljabali AAA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ (2013) CPMV-DOX delivers. Mol Pharm 10:3–10
Alonso JM, Górzny MŁ, Bittner AM (2013) The physics of tobacco mosaic virus and virus-based devices in biotechnology. Trends Biotechnol 31:530–538
Anderson EA, Isaacman S, Peabody DS, Wang EY, Canary JW, Kirshenbaum K (2006) Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett 6:1160–1164
Ashley CE, Carnes EC, Phillips GK, Durfee PN, Buley MD, Lino CA, Padilla DP, Phillips B, Carter MB, Willman CL, Brinker CJ, Caldeira J, Chackerian B, Wharton W, Peabody DS (2011) Cell-specific delivery of diverse cargos by bacteriophage MS2 virus-like particles. ACS Nano 5:5729–5745
Atabekov J, Nikitin N, Arkhipenko M, Chirkov S, Karpova O (2011) Thermal transition of native tobacco mosaic virus and RNA-free viral proteins into spherical nanoparticles. J Gen Virol 92:453–456
Banerjee D, Liu AP, Voss NR, Schmid SL, Finn MG (2010a) Multivalent display and receptor-mediated endocytosis of transferrin on virus-like particles. ChemBioChem 11:1273–1279
Banerjee PS, Ostapchuk P, Hearing P, Carrico I (2010b) Chemoselective attachment of small molecule effector functionality to human adenoviruses facilitates gene delivery to cancer cells. J Am Chem Soc 132:13615–13617
Bratkovič T (2010) Progress in phage display: evolution of the technique and its applications. Cell Mol Life Sci 67:749–767
Bronstein LM (2011) Virus-based nanoparticles with inorganic cargo: what does the future hold? Small 7:1609–1618
Brown AD, Naves L, Wang X, Ghodssi R, Culver JN (2013) Carboxylate-directed in vivo assembly of virus-like nanorods and tubes for the display of functional peptides and residues. Biomacromolecules 14:3123–3129
Bruckman MA, Soto CM, McDowell H, Liu JL, Ratna BR, Korpany KV, Zahr OK, Blum AS (2011) Role of hexahistidine in directed nanoassemblies of tobacco mosaic virus coat protein. ACS Nano 5:1606–1616
Bruckman MA, Hern S, Jiang K, Flask CA, Yu X, Steinmetz NF (2013) Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. J Mater Chem B 1:1482–1490
Bundy BC, Franciszkowicz MJ, Swartz JR (2008) Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnol Bioeng 100:28–37
Butler PJG, Finch JT (1973) Structures and roles of the polymorphic forms of tobacco mosaic virus protein: VII. Lengths of the growing rods during assembly into nucleoprotein with the viral RNA. J Mol Biol 78:637–649
Cadena-Nava RD, Comas-Garcia M, Garmann RF, Rao ALN, Knobler CM, Gelbart WM (2012) Self-assembly of viral capsid protein and RNA molecules of different sizes: requirement for a specific high protein/RNA mass ratio. J Virol 86:3318–3326
Capehart SL, Coyle MP, Glasgow JE, Francis MB (2013) Controlled integration of gold nanoparticles and organic fluorophores using synthetically modified MS2 viral capsids. J Am Chem Soc 135:3011–3016
Cardinale D, Carette N, Michon T (2012) Virus scaffolds as enzyme nano-carriers. Trends Biotechnol 30:369–376
Carette N, Engelkamp H, Akpa E, Pierre SJ, Cameron NR, Christianen PCM, Maan JC, Thies JC, Weberskirch R, Rowan AE, Nolte RJM, Michon T, van Hest JCM (2007) A virus-based biocatalyst. Nat Nanotechnol 2:226–229
Carrico ZM, Romanini DW, Mehl RA, Francis MB (2008) Oxidative coupling of peptides to a virus capsid containing unnatural amino acids. Chem Commun 10:1205–1207
Caspar D, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27:1–24
Chen W, Cao Y, Liu M, Zhao Q, Huang J, Zhang H, Deng Z, Dai J, Williams DF, Zhang Z (2012) Rotavirus capsid surface protein VP4-coated Fe3O4 nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 33:7895–7902
Chen P, Dang X, Klug MT, Qi J, CourchesneN-M BFJ, Fang N, Hammond PT, Belcher AM (2013) Versatile three-dimensional virus-based template for dye-sensitized solar cells with improved electron transport and light harvesting. ACS Nano 7:6563–6574
Cielens I, Ose V, Petrovskis I, Strelnikova A, Renhofa R, Kozlovska T, Pumpens P (2000) Mutilation of RNA phage Qβ virus-like particles: from icosahedrons to rods. FEBS Lett 482:261–264
Comellas-Aragonès M, Engelkamp H, Claessen VI, Sommerdijk NAJM, Rowan AE, Christianen PCM, Maan JC, Verduin BJM, Cornelissen JJLM, Nolte RJM (2007) A virus-based single-enzyme nanoreactor. Nat Nanotechnol 2:635–639
Crookes-Goodson WJ, Slocik JM, Naik RR (2008) Bio-directed synthesis and assembly of nanomaterials. Chem Soc Rev 37:2403
De la Escosura A, Janssen PGA, Schenning APHJ, Nolte RJM, Cornelissen JJLM (2010) Encapsulation of DNA-templated chromophore assemblies within virus protein nanotubes. Angew Chem Int Ed 49:5335–5338
Dedeo MT, Duderstadt KE, Berger JM, Francis MB (2010) Nanoscale protein assemblies from a circular permutant of the tobacco mosaic virus. Nano Lett 10:181–186
Destito G, Yeh R, Rae CS, Finn MG, Manchester M (2007) Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem Biol 14:1152–1162
Durham ACH, Finch JT, Klug A (1971) States of aggregation of tobacco mosaic virus protein. Nature 229:37–42
Eber FJ, Eiben S, Jeske H, Wege C (2013) Bottom-up-assembled nanostar colloids of gold cores and tubes derived from tobacco mosaic virus. Angew Chem Int Ed 52:7203–7207
Endo M, Fujitsuka M, Majima T (2007) Porphyrin light-harvesting arrays constructed in the recombinant tobacco mosaic virus scaffold. Chem Eur J 13:8660–8666
Enomoto T, Kawano M, Fukuda H, Sawada W, Inoue T, Haw KC, Kita Y, Sakamoto S, Yamaguchi Y, Imai T, Hatakeyama M, Saito S, Sandhu A, Matsui M, Aoki I, Handa H (2013) Viral protein-coating of magnetic nanoparticles using simian virus 40 VP1. J Biotechnol 167:8–15
Farkas ME, Aanei IL, Behrens CR, Tong GJ, Murphy ST, O’Neil JP, Francis MB (2013) PET imaging and biodistribution of chemically modified bacteriophage MS2. Mol Pharm 10:69–76
Fass L (2008) Imaging and cancer: a review. Mol Oncol 2:115–152
Fiedler JD, Brown SD, Lau JL, Finn MG (2010) RNA-directed packaging of enzymes within virus-like particles. Angew Chem Int Ed 49:9648–9651
Fiedler JD, Higginson C, Hovlid ML, Kislukhin AA, Castillejos A, Manzenrieder F, Campbell MG, Voss NR, Potter CS, Carragher B, Finn MG (2012) Engineered mutations change the structure and stability of a virus-like particle. Biomacromolecules 13:2339–2348
Garimella PD, Datta A, Romanini DW, Raymond KN, Francis MB (2011) Multivalent, high-relaxivity MRI contrast agents using rigid cysteine-reactive gadolinium complexes. J Am Chem Soc 133:14704–14709
Geiger FC, Eber FJ, Eiben S, Mueller A, Jeske H, Spatz JP, Wege C (2013) TMV nanorods with programmed longitudinal domains of differently addressable coat proteins. Nanoscale 5:3808–3816
Ghosh D, Lee Y, Thomas S, Kohli AG, Yun DS, Belcher AM, Kelly KA (2012) M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat Nanotechnol 7:677–682
Gigout L, Rebollo P, Clement N, Warrington KH, Muzyczka N, Linden RM, Weber T (2005) Altering AAV tropism with mosaic viral capsids. Mol Ther 11:856–865
Glasgow JE, Capehart SL, Francis MB, Tullman-Ercek D (2012) Osmolyte-mediated encapsulation of proteins inside MS2 viral capsids. ACS Nano 6:8658–8664
Gross I, Hohenberg H, Huckhagel C, Kräusslich H-G (1998) N-Terminal extension of human immunodeficiency virus capsid protein converts the in vitro assembly phenotype from tubular to spherical particles. J Virol 72:4798–4810
Ho ML, Adler BA, Torre ML, Silberg JJ, Suh J (2013) SCHEMA computational design of virus capsid chimeras: calibrating how genome packaging, protection, and transduction correlate with calculated structural disruption. ACS Synth Biol 2:724–733
Hooker JM, O’Neil JP, Romanini DW, Taylor SE, Francis MB (2008) Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol Imaging Biol 10:182–191
Hu Y, Zandi R, Anavitarte A, Knobler CM, Gelbart WM (2008) Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys J 94:1428–1436
Huang X, Bronstein LM, Retrum J, Dufort C, Tsvetkova I, Aniagyei S, Stein B, Stucky G, McKenna B, Remmes N, Baxter D, Kao CC, Dragna B (2007) Self-assembled virus-like particles with magnetic cores. Nano Lett 7:2407–2416
Huang RK, Steinmetz NF, Fu C, Manchester M, Johnson JE (2011) Transferrin-mediated targeting of bacteriophage HK97 nanoparticles into tumor cells. Nanomedicine (Lond) 6:55–68
Hung PP, Ling CM, Overby LR (1969) Self assembly of QB and MS2 phage particles: possible function of initiation complexes. Science 166:1638–1640
Jiang W, Li Z, Zhang Z, Baker ML, Prevelige PE, Chiu W (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Mol Biol 10:131–135
Kadri A, Maiß E, Amsharov N, Bittner AM, Balci S, Kern K, Jeske H, Wege C (2011) Engineered tobacco mosaic virus mutants with distinct physical characteristics in planta and enhanced metallization properties. Virus Res 157:35–46
Kaiser CR, Flenniken ML, Gillitzer E, Harmsen AL, Harmsen AG, Jutila MA, Douglas T, Young MJ (2007) Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int J Nanomedicine 2:715–733
Katen S, Zlotnick A (2009) The Thermodynamics of Virus Capsid Assembly. In: Johnson ML, Holt JM, Ackers GK (eds) Methods in Enzymology, Chapter 14 Academic Press, 455:395–417
Kay MA (2011) State-of-the-art gene-based therapies: the road ahead. Nat Rev Genet 12:316–328
Khayat R, Brunn N, Speir JA, Hardham JM, Ankenbauer RG, Schneemann A, Johnson JE (2011) The 2.3-angstrom structure of porcine circovirus 2. J Virol 85:7856–7862
King NP, Lai Y (2013) Practical approaches to designing novel protein assemblies. Curr Opin Struct Biol 23:632–638
Klem MT, Young M, Douglas T (2008) Biomimetic synthesis of β-TiO2 inside a viral capsid. J Mater Chem 18:3821
Kler S, Wang JC, Dhason M, Oppenheim A, Zlotnick A (2013) Scaffold properties are a key determinant of the size and shape of self-assembled virus-derived particles. ACS Chem Biol 8:2753–2761
Koshiyama T, Yokoi N, Ueno T, Kanamaru S, Nagano S, Shiro Y, Arisaka F, Watanabe Y (2008) Molecular design of heteroprotein assemblies providing a bionanocup as a chemical reactor. Small 4:50–54
Krol MA, Olson NH, Tate J, Johnson JE, Baker TS, Ahlquist P (1999) RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc Natl Acad Sci U S A 96:13650–13655
Kwon I, Schaffer DV (2008) Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm Res 25:489–499
Lee S, Lim J, Harris MT (2012a) Synthesis and application of virus-based hybrid nanomaterials. Biotechnol Bioeng 109:16–30
Lee Y, Kim J, Yun DS, Nam YS, Shao-Horn Y, Belcher AM (2012b) Virus-templated Au and Au–Pt core–shell nanowires and their electrocatalytic activities for fuel cell applications. Energy Environ Sci 5:8328
Li F, Wang Q (2013) Fabrication of nanoarchitecturestemplated by virus-based nanoparticles: strategies and applications. Small 10:230–245
Li Z, Jin Q, Huang C, Dasa S, Chen L, Yap L, Liu S, Cai H, Park R, Conti PS (2011) Trackable and targeted phage as positron emission tomography (PET) agent for cancer imaging. Theranostics 1:371–380
Lim J, Kim S, Lee S, Stach EA, Culver JN, Harris MT (2010) Biotemplated aqueous-phase palladium crystallization in the absence of external reducing agents. Nano Lett 10:3863–3867
Liu Z, Qiao J, Niu Z, Wang Q (2012) Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem Soc Rev 41:6178
Lockney DM, Guenther RN, Loo L, Overton W, Antonelli R, Clark J, Hu M, Luft C, Lommel SA, Franzen S (2011) The red clover necrotic mosaic virus capsid as a multifunctional cell targeting plant viral nanoparticle. Bioconj Chem 22:67–73
Lomonossoff GP, Evans DJ (2011) Applications of plant viruses in bionanotechnology. Springer, Berlin, pp 1–27
Low PS, Kularatne SA (2009) Folate-targeted therapeutic and imaging agents for cancer. Curr Opin Chem Biol 13:256–262
Lucas RW, Kuznetsov YG, Larson SB, McPherson A (2001) Crystallization of brome mosaic virus and T = 1 brome mosaic virus particles following a structural transition. Virology 286:290–303
Lucon J, Qazi S, Uchida M, Bedwell GJ, LaFrance B, Prevelige PE, Douglas T (2012) 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 4:781–788
Ma Y, Nolte RJM, Cornelissen JJLM (2012) Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev 64:811–825
Manocchi AK, Horelik NE, Lee B, Yi H (2010) Simple, readily controllable palladium nanoparticle formation on surface-assembled viral nanotemplates. Langmuir 26:3670–3677
Mateu MG (2013) Assembly, stability and dynamics of virus capsids. Arch Biochem Biophys 531:65–79
Miller RA, Presley AD, Francis MB (2007) Self-assembling light-harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J Am Chem Soc 129:3104–3109
Miller RA, Stephanopoulos N, McFarland JM, Rosko AS, Geissler PL, Francis MB (2010) Impact of assembly state on the defect tolerance of TMV-based light harvesting arrays. J Am Chem Soc 132:6068–6074
Min J, Jung H, Shin H, Cho G, Cho H, Kang S (2013) Implementation of P22 viral capsids as intravascular magnetic resonance T1 contrast conjugates via site-selective attachment of Gd(III)-chelating agents. Biomacromolecules 14:2332–2339
Minten IJ, Ma Y, Hempenius MA, Vancso GJ, Nolte RJM, Cornelissen JJLM (2009) CCMV capsid formation induced by a functional negatively charged polymer. Org Biomol Chem 7:4685–4688
Minten IJ, Claessen VI, Blank K, Rowan AE, Nolte RJM, Cornelissen JJLM (2011) Catalytic capsids: the art of confinement. Chem Sci 2:358–362
Mukherjee S, Pfeifer CM, Johnson JM, Liu J, Zlotnick A (2006) Redirecting the coat protein of a spherical virus to assemble into tubular nanostructures. J Am Chem Soc 128:2538–2539
Nam YS, Magyar AP, Lee D, Kim J, Yun DS, Park H, Pollom TS, Weitz DA, Belcher AM (2010) Biologically templatedphotocatalytic nanostructures for sustained light-driven water oxidation. Nat Nanotechnol 5:340–344
Newton-Northup JR, Figueroa SD, Quinn TP, Deutscher SL (2009) Bifunctional phage-based pretargeted imaging of human prostate carcinoma. Nucl Med Biol 36:789–800
O’Neil A, Reichhardt C, Johnson B, Prevelige PE, Douglas T (2011) Genetically programmed in vivo packaging of protein cargo and its controlled release from bacteriophage P22. Angew Chem Int Ed 50:7425–7428
O’Neil A, Prevelige PE, Douglas T (2013) Stabilizing viral nano-reactors for nerve-agent degradation. Biomater Sci 1:881–886
Oh D, Qi J, Lu Y, Zhang Y, Shao-Horn Y, Belcher AM (2013) Biologically enhanced cathode design for improved capacity cycle life for lithium–oxygen batteries. Nat Commun 4. doi:10.1038/ncomms3756
Palaniappan KK, Ramirez RM, Bajaj VS, Wemmer DE, Pines A, Francis MB (2013) Molecular imaging of cancer cells using a bacteriophage-based 129Xe NMR biosensor. Angew Chem 125:4949–4953
Patel KG, Swartz JR (2011) Surface functionalization of virus-like particles by direct conjugation using azide−alkyne clickchemistry. Bioconjug Chem 22:376–387
Pattenden LK, Middelberg APJ, Niebert M, Lipin DI (2005) Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol 23:523–529
Patterson DP, Prevelige PE, Douglas T (2012a) Nanoreactors by programmed enzyme encapsulation inside the capsid of the bacteriophage P22. ACS Nano 6:5000–5009
Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T (2012b) Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8:10158–10166
Pfeiffer P, Hirth L (1974) Aggregation states of Brome mosaic virus protein. Virology 61:160–167
Philippe N, Legendre M, Doutre G, Couté Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie J, Abergel C (2013) Pandoraviruses: Amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341:281–286
Pille J, Cardinale D, Carette N, Di Primo C, Besong-Ndika J, Walter J, Lecoq H, van Eldijk MB, Smits FCM, Schoffelen S, van Hest JCM, Mäkinen K, Michon T (2013) General strategy for ordered noncovalent protein assembly on well-defined nanoscaffolds. Biomacromolecules 14:4351–4359
Plummer EM, Manchester M (2011) Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomedicine Nanobiotechnol 3:174–196
Plummer EM, Manchester M (2013) Endocytic uptake pathways utilized by CPMV nanoparticles. Mol Pharm 10:26–32
Pokorski JK, Hovlid ML, Finn MG (2011) Cell targeting with hybrid Qβ virus-like particles displaying epidermal growth factor. ChemBioChem 12:2441–2447
Prasuhn DE Jr, Yeh RM, Obenaus A, Manchester M, Finn MG (2007) Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide–alkyne cycloaddition. Chem Commun 12:1269–1271
Qazi S, Liepold LO, Abedin MJ, Johnson B, Prevelige P, Frank JA, Douglas T (2013) P22 Viral capsids as nanocompositehigh-relaxivity MRI contrast agents. Mol Pharm 10:11–17
Rabindran S, Dawson WO (2001) Assessment of recombinants that arise from the use of a TMV-based transient expression vector. Virology 284:182–189
Rakonjac J, Bennett NJ, Spagnuolo J, Gagic D, Russel M (2011) Filamentous bacteriophage: biology, phage display and nanotechnology applications. Curr Issues Mol Biol 13:51–76
Reichhardt C, Uchida M, O’Neil A, Li R, Prevelige PE, Douglas T (2011) Templated assembly of organic–inorganic materials using the core shell structure of the P22 bacteriophage. Chem Commun 47:6326–6328
Ren Y, Wong SM, Lim L (2007) Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjug Chem 18:836–843
Ren Y, Wong SM, Lim LY (2010) Application of plant viruses as nanodrug delivery systems. Pharm Res 27:2509–2513
Rhee J, Baksh M, Nycholat C, Paulson JC, Kitagishi H, Finn MG (2012) Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules 13:2333–2338
Rice G, Stedman K, Snyder J, Wiedenheft B, Willits D, Brumfield S, McDermott T, Young MJ (2001) Viruses from extreme thermal environments. Proc Natl Acad Sci U S A 98:13341–13345
Roldão A, Mellado MCM, Castilho LR, Carrondo MJ, Alves PM (2010) Virus-like particles in vaccine development. Expert Rev Vaccines 9:1149–1176
Rong J, Oberbeck F, Wang X, Li X, Oxsher J, Niu Z, Wang Q (2009) Tobacco mosaic virus templated synthesis of one dimensional inorganic–polymer hybrid fibres. J Mater Chem 19:2841–2845
Rumnieks J, Ose V, Tars K, Dislers A, Strods A, Cielens I, Renhofa R (2009) Assembly of mixed rod-like and spherical particles from group I and II RNA bacteriophage coat proteins. Virology 391:187–194
Rusckowski M, Gupta S, Liu G, Dou S, Hnatowich DJ (2008) Investigation of four 99mTc-labeled bacteriophages for infection-specific imaging. Nucl Med Biol 35:433–440
Sainsbury F, Cañizares MC, Lomonossoff GP (2010) Cowpea mosaic virus: the plant virus–based biotechnology workhorse. Annu Rev Plant Physiol Plant Mol Biol 48:437–455
Saunders K, Sainsbury F, Lomonossoff GP (2010) Efficient generation of cowpea mosaic virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 393:329–337
Schmidt U, Günther C, Rudolph R, Böhm G (2001) Protein and peptide delivery via engineered polyomavirus-like particles. FASEB J 15:1646–1648
Shen L, Bao N, Prevelige PE, Gupta A (2010) Fabrication of ordered nanostructures of sulfide nanocrystal assemblies over self-assembled genetically engineered P22 coat protein. J Am Chem Soc 132:17354–17357
Sherman MB, Guenther RH, Tama F, Sit TL, Brooks CL, Mikhailov AM, Orlova EV, Baker TS, Lommel SA (2006) Removal of divalent cations induces structural transitions in red clover necrotic mosaic virus, revealing a potential mechanism for RNA release. J Virol 80:10395–10406
Shriver LP, Plummer EM, Thomas DM, Ho S, Manchester M (2013) Localization of gadolinium-loaded CPMV to sites of inflammation during central nervous system autoimmunity. J Mater Chem B 1:5256–5263
Shukla S, Ablack AL, Wen AM, Lee KL, Lewis JD, Steinmetz NF (2013) Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle potato virus X. Mol Pharm 10:33–42
Singh P, Prasuhn D, Yeh RM, Destito G, Rae CS, Osborn K, Finn MG, Manchester M (2007) Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J Control Release 120:41–50
Smith MT, Hawes AK, Bundy BC (2013) Reengineering viruses and virus-like particles through chemical functionalization strategies. Curr Opin Biotechnol 24:620–626
Soto CM, Ratna BR (2010) Virus hybrids as nanomaterials for biotechnology. Curr Opin Biotechnol 21:426–438
Steinmetz NF, Bize A, Findlay KC, Lomonossoff GP, Manchester M, Evans DJ, Prangishvili D (2008) Site-specific and spatially controlled addressability of a new viral nanobuilding block: Sulfolobus islandicus rod-shaped virus 2. Adv Funct Mater 18:3478–3486
Stephanopoulos N, Tong GJ, Hsiao SC, Francis MB (2010) Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano 4:6014–6020
Strable E, Prasuhn DE, Udit AK, Brown S, Link AJ, Ngo JT, Lander G, Quispe J, Potter CS, Carragher B, Tirrell D, Finn MG (2008) Unnatural amino acid incorporation into virus-like particles. Bioconjug Chem 19:866–875
Stubenrauch K, Gleiter S, Brinkmann U, Rudolph R, Lilie H (2001) Conjugation of an antibody Fv fragment to a virus coat protein: cell-specific targeting of recombinant polyoma-virus-like particles. Biochem J 356:867–873
Teunissen EA, de Raad M, Mastrobattista E (2013) Production and biomedical applications of virus-like particles derived from polyomaviruses. J Control Release 172:305–321
Tong GJ, Hsiao SC, Carrico ZM, Francis MB (2009) Viral capsid DNA aptamer conjugates as multivalent cell-targeting vehicles. J Am Chem Soc 131:11174–11178
Udit AK, Hollingsworth W, Choi K (2010) Metal- and metallocycle-binding sites engineered into polyvalent virus-like scaffolds. Bioconjug Chem 21:399–404
van Eldijk MB, Wang JC, Minten IJ, Li C, Zlotnick A, Nolte RJM, Cornelissen JJLM, van Hest JCM (2012) Designing two self-assembly mechanisms into one viral capsid protein. J Am Chem Soc 134:18506–18509
Wörsdörfer B, Pianowski Z, Hilvert D (2012) Efficient in vitro encapsulation of protein cargo by an engineered protein container. J Am Chem Soc 134:909–911
Wu M, Brown WL, Stockley PG (1995) Cell-specific delivery of bacteriophage-encapsidated ricin A chain. Bioconjug Chem 6:587–595
Yang C, Manocchi AK, Lee B, Yi H (2011) Viral-templated palladium nanocatalysts for Suzuki coupling reaction. J Mater Chem 21:187–194
Yildiz I, Shukla S, Steinmetz NF (2011) Applications of viral nanoparticles in medicine. Curr Opin Biotechnol 22:901–908
Yildiz I, Tsvetkova I, Wen AM, Shukla S, Masarapu MH, Dragnea B, Steinmetz NF (2012) Engineering of Brome mosaic virus for biomedical applications. RSC Adv 2:3670–3677
Zahr OK, Blum AS (2012) Solution phase gold nanorings on a viral protein template. Nano Lett 12:629–633
Zeltins A (2013) Construction and characterization of virus-like particles: a review. Mol Biotechnol 53:92–107
Zeng Q, Wen H, Wen Q, Chen X, Wang Y, Xuan W, Liang J, Wan S (2013) Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 34:4632–4642
Zeltins A (2013) Construction and characterization of virus-like particles: a review. Mol Biotechnol 53:92–107
Zeng Q, Wen H, Wen Q, Chen X, Wang Y, Xuan W, Liang J, Wan S (2013) Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 34:4632–4642
Zhang S, Li J, Lykotrafitis G, Bao G, Suresh S (2009) Size-dependent endocytosis of nanoparticles. Adv Mater 21:419–424
Zhao X, Fox JM, Olson NH, Baker TS, Young MJ (1995) In vitro assembly of cowpea chlorotic mottle virus from coat protein expressed in Escherichia coli and in vitro-transcribed viral cDNA. Virology 207:486–494
Zhao Q, Chen W, Chen Y, Zhang L, Zhang J, Zhang Z (2011) Self-assembled virus-like particles from rotavirus structural protein VP6 for targeted drug delivery. Bioconjug Chem 22:346–352
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Glasgow, J., Tullman-Ercek, D. Production and applications of engineered viral capsids. Appl Microbiol Biotechnol 98, 5847–5858 (2014). https://doi.org/10.1007/s00253-014-5787-3
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DOI: https://doi.org/10.1007/s00253-014-5787-3