1932

Abstract

Nanoscale engineering is revolutionizing the way we prevent, detect, and treat diseases. Viruses have played a special role in these developments because they can function as prefabricated nanoscaffolds that have unique properties and are easily modified. The interiors of virus particles can encapsulate and protect sensitive compounds, while the exteriors can be altered to display large and small molecules in precisely defined arrays. These properties of viruses, along with their innate biocompatibility, have led to their development as actively targeted drug delivery systems that expand on and improve current pharmaceutical options. Viruses are naturally immunogenic, and antigens displayed on their surface have been used to create vaccines against pathogens and to break self-tolerance to initiate an immune response to dysfunctional proteins. Densely and specifically aligned imaging agents on viruses have allowed for high-resolution and noninvasive visualization tools to detect and treat diseases earlier than previously possible. These and future applications of viruses have created an exciting new field within the disciplines of both nanotechnology and medicine.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-100114-055141
2015-11-09
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/virology/2/1/annurev-virology-100114-055141.html?itemId=/content/journals/10.1146/annurev-virology-100114-055141&mimeType=html&fmt=ahah

Literature Cited

  1. Desai N. 1.  2012. Challenges in development of nanoparticle-based therapeutics. AAPS J. 14:282–95 [Google Scholar]
  2. Franca R, Zhang XF, Veres T, Yahia L, Sacher E. 2.  2013. Core-shell nanoparticles as prodrugs: possible cytotoxicological and biomedical impacts of batch-to-batch inconsistencies. J. Colloid Interface Sci. 389:292–97 [Google Scholar]
  3. Guenther CM, Kuypers BE, Lam MT, Robinson TM, Zhao J, Suh J. 3.  2014. Synthetic virology: engineering viruses for gene delivery. WIRES Nanomed. Nanobiotechnol. 6:548–58 [Google Scholar]
  4. Wirth T, Parker N, Ylä-Herttuala S. 4.  2013. History of gene therapy. Gene 525:162–69 [Google Scholar]
  5. Ylä-Herttuala S. 5.  2012. Endgame: Glybera finally recommended for approval as the first gene therapy drug in the European Union. Mol. Ther. 20:1831–32 [Google Scholar]
  6. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM. 6.  et al. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605–12 [Google Scholar]
  7. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. 7.  2007. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2:751–60 [Google Scholar]
  8. Steinmetz NF. 8.  2010. Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. Nanomedicine 6:634–41 [Google Scholar]
  9. Wang Q, Lin T, Johnson JE, Finn MG. 9.  2002. Natural supramolecular building blocks: cysteine-added mutants of Cowpea mosaic virus. Chem. Biol. 9:813–19 [Google Scholar]
  10. Peabody DS. 10.  2003. A viral platform for chemical modification and multivalent display. J. Nanobiotechnol. 1:5 [Google Scholar]
  11. Miller RA, Presley AD, Francis MB. 11.  2007. Self-assembling light-harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J. Am. Chem. Soc. 129:3104–9 [Google Scholar]
  12. Klem MT, Willits D, Young M, Douglas T. 12.  2003. 2-D array formation of genetically engineered viral cages on Au surfaces and imaging by atomic force microscopy. J. Am. Chem. Soc. 125:10806–7 [Google Scholar]
  13. Udit AK, Brown S, Baksh MM, Finn MG. 13.  2008. Immobilization of bacteriophage Qβ on metal-derivatized surfaces via polyvalent display of hexahistidine tags. J. Inorg. Biochem. 102:2142–46 [Google Scholar]
  14. Medintz IL, Sapsford KE, Konnert JH, Chatterji A, Lin T. 14.  et al. 2005. Decoration of discretely immobilized cowpea mosaic virus with luminescent quantum dots. Langmuir 21:5501–10 [Google Scholar]
  15. Chatterji A, Ochoa WF, Ueno T, Lin T, Johnson JE. 15.  2005. A virus-based nanoblock with tunable electrostatic properties. Nano Lett. 5:597–602 [Google Scholar]
  16. Douglas T, Strable E, Willits D. 16.  2002. Protein engineering of a viral cage for constrained material synthesis. Adv. Mater. 14:415–18 [Google Scholar]
  17. Plummer EM, Manchester M. 17.  2010. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. WIRES Nanomed. Nanobiotechnol. 3:174–96 [Google Scholar]
  18. Yildiz I, Shukla S, Steinmetz NF. 18.  2011. Applications of viral nanoparticles in medicine. Curr. Opin. Biotechnol. 22:901–8 [Google Scholar]
  19. Strable E, Prasuhn DE Jr, Udit AK, Brown S, Link AJ. 19.  et al. 2008. Unnatural amino acid incorporation into virus-like particles. Bioconjug. Chem. 19:866–75 [Google Scholar]
  20. Daniel MC, Tsvetkova IB, Quinkert ZT, Murali A, De M. 20.  et al. 2010. Role of surface charge density in nanoparticle-templated assembly of bromovirus protein cages. ACS Nano 4:3853–60 [Google Scholar]
  21. Dixit SK, Goicochea NL, Daniel MC, Murali A, Bronstein L. 21.  et al. 2006. Quantum dot encapsulation in viral capsids. Nano Lett. 6:1993–99 [Google Scholar]
  22. Huang X, Bronstein LM, Retrum J, Dufort C, Tsvetkova I. 22.  et al. 2007. Self-assembled virus-like particles with magnetic cores. Nano Lett. 7:2407–16 [Google Scholar]
  23. Sun J, DuFort C, Daniel MC, Murali A, Chen C. 23.  et al. 2007. Core-controlled polymorphism in virus-like particles. PNAS 104:1354–59 [Google Scholar]
  24. Brown WL, Mastico RA, Wu M, Heal KG, Adams CJ. 24.  et al. 2002. RNA bacteriophage capsid-mediated drug delivery and epitope presentation. Intervirology 45:371–80 [Google Scholar]
  25. Wu M, Brown WL, Stockley PG. 25.  1995. Cell-specific delivery of bacteriophage-encapsidated ricin A chain. Bioconjug. Chem. 6:587–95 [Google Scholar]
  26. Pokorski JK, Steinmetz NF. 26.  2011. The art of engineering viral nanoparticles. Mol. Pharm. 8:29–43 [Google Scholar]
  27. Wen AM, Shukla S, Saxena P, Aljabali AA, Yildiz I. 27.  et al. 2012. Interior engineering of a viral nanoparticle and its tumor homing properties. Biomacromolecules 13:3990–4001 [Google Scholar]
  28. Prasuhn DE Jr, Yeh RM, Obenaus A, Manchester M, Finn MG. 28.  2007. Viral MRI contrast agents: coordination of Gd by native virions and attachment of Gd complexes by azide-alkyne cycloaddition. Chem. Commun. 2007:1269–71 [Google Scholar]
  29. Yildiz I, Lee KL, Chen K, Shukla S, Steinmetz NF. 29.  2013. Infusion of imaging and therapeutic molecules into the plant virus-based carrier cowpea mosaic virus: cargo-loading and delivery. J. Control. Release 172:568–78 [Google Scholar]
  30. Young M, Willits D, Uchida M, Douglas T. 30.  2008. Plant viruses as biotemplates for materials and their use in nanotechnology. Annu. Rev. Phytopathol. 46:361–84 [Google Scholar]
  31. Kovacs EW, Hooker JM, Romanini DW, Holder PG, Berry KE, Francis MB. 31.  2007. Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjug. Chem. 18:1140–47 [Google Scholar]
  32. Schlick TL, Ding Z, Kovacs EW, Francis MB. 32.  2005. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 127:3718–23 [Google Scholar]
  33. Bruckman MA, Kaur G, Lee LA, Xie F, Sepulveda J. 33.  et al. 2008. Surface modification of tobacco mosaic virus with “click” chemistry. ChemBioChem 9:519–23 [Google Scholar]
  34. Hong V, Presolski SI, Ma C, Finn MG. 34.  2009. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. 48:9879–83 [Google Scholar]
  35. Steinmetz NF, Hong V, Spoerke ED, Lu P, Breitenkamp K. 35.  et al. 2009. Buckyballs meet viral nanoparticles: candidates for biomedicine. J. Am. Chem. Soc. 131:17093–95 [Google Scholar]
  36. Steinmetz NF, Mertens ME, Taurog RE, Johnson JE, Commandeur U. 36.  et al. 2010. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 10:305–12 [Google Scholar]
  37. Uchida M, Morris DS, Kang S, Jolley CC, Lucon J. 37.  et al. 2012. Site-directed coordination chemistry with P22 virus-like particles. Langmuir 28:1998–2006 [Google Scholar]
  38. Datta A, Hooker JM, Botta M, Francis MB, Aime S, Raymond KN. 38.  2008. High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosized MRI contrast agents. J. Am. Chem. Soc. 130:2546–52 [Google Scholar]
  39. Hooker JM, Datta A, Botta M, Raymond KN, Francis MB. 39.  2007. Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies. Nano Lett. 7:2207–10 [Google Scholar]
  40. Hooker J, O'Neil J, Romanini D, Taylor S, Francis M. 40.  2008. Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol. Imaging Biol. 10:182–91 [Google Scholar]
  41. Venter PA, Dirksen A, Thomas D, Manchester M, Dawson PE, Schneemann A. 41.  2011. Multivalent display of proteins on viral nanoparticles using molecular recognition and chemical ligation strategies. Biomacromolecules 12:2293–301 [Google Scholar]
  42. Carrico ZM, Farkas ME, Zhou Y, Hsiao SC, Marks JD. 42.  et al. 2012. N-Terminal labeling of filamentous phage to create cancer marker imaging agents. ACS Nano 6:6675–80 [Google Scholar]
  43. Gatto D, Ruedl C, Odermatt B, Bachmann MF. 43.  2004. Rapid response of marginal zone B cells to viral particles. J. Immunol. 173:4308–16 [Google Scholar]
  44. Singh P, Prasuhn D, Yeh RM, Destito G, Rae CS. 44.  et al. 2007. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J. Control. Release 120:41–50 [Google Scholar]
  45. Srivastava AS, Kaido T, Carrier E. 45.  2004. Immunological factors that affect the in vivo fate of T7 phage in the mouse. J. Virol. Methods 115:99–104 [Google Scholar]
  46. Kwon OJ, Kang E, Choi JW, Kim SW, Yun CO. 46.  2013. Therapeutic targeting of chitosan-PEG-folate-complexed oncolytic adenovirus for active and systemic cancer gene therapy. J. Control. Release 169:257–65 [Google Scholar]
  47. Pasut G, Veronese FM. 47.  2009. PEG conjugates in clinical development or use as anticancer agents: an overview. Adv. Drug Deliv. Rev. 61:1177–88 [Google Scholar]
  48. Tesfay MZ, Kirk AC, Hadac EM, Griesmann GE, Federspiel MJ. 48.  et al. 2013. PEGylation of vesicular stomatitis virus extends virus persistence in blood circulation of passively immunized mice. J. Virol. 87:3752–59 [Google Scholar]
  49. Zeng Q, Wen H, Wen Q, Chen X, Wang Y. 49.  et al. 2013. Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 34:4632–42 [Google Scholar]
  50. Galaway FA, Stockley PG. 50.  2013. MS2 viruslike particles: a robust, semisynthetic targeted drug delivery platform. Mol. Pharm. 10:59–68 [Google Scholar]
  51. Huang RK, Steinmetz NF, Fu CY, Manchester M, Johnson JE. 51.  2011. Transferrin-mediated targeting of bacteriophage HK97 nanoparticles into tumor cells. Nanomedicine 6:55–68 [Google Scholar]
  52. Chariou PL, Lee KL, Wen AM, Gulati NM, Stewart PL, Steinmetz NF. 52.  2015. Detection and imaging of aggressive cancer cells using an epidermal growth factor receptor (EGFR)-targeted filamentous plant virus-based nanoparticle. Bioconjug. Chem. 26:262–69 [Google Scholar]
  53. Pokorski JK, Hovlid ML, Finn MG. 53.  2011. Cell targeting with hybrid Qβ virus-like particles displaying epidermal growth factor. ChemBioChem 12:2441–47 [Google Scholar]
  54. Hovlid ML, Steinmetz NF, Laufer B, Lau JL, Kuzelka J. 54.  et al. 2012. Guiding plant virus particles to integrin-displaying cells. Nanoscale 4:3698–705 [Google Scholar]
  55. Shukla S, Ablack AL, Wen AM, Lee KL, Lewis JD, Steinmetz NF. 55.  2013. Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle Potato virus X. Mol. Pharm. 10:33–42 [Google Scholar]
  56. Wen AM, Wang Y, Jiang K, Hsu GC, Gao H. 56.  et al. 2015. Shaping bio-inspired nanotechnologies to target thrombosis for dual optical-magnetic resonance imaging. J. Mater. Chem. B 3:6037–45 [Google Scholar]
  57. Shukla S, Eber FJ, Nagarajan AS, DiFranco NA, Schmidt N. 57.  et al. 2015. The impact of aspect ratio on the biodistribution and tumor homing of rigid soft-matter nanorods. Adv. Healthc. Mater. 4:874–82 [Google Scholar]
  58. Cao J, Guenther RH, Sit TL, Opperman CH, Lommel SA, Willoughby JA. 58.  2014. Loading and release mechanism of Red clover necrotic mosaic virus derived plant viral nanoparticles for drug delivery of doxorubicin. Small 10:5126–36 [Google Scholar]
  59. Choi KM, Kim K, Kwon IC, Kim IS, Ahn HJ. 59.  2012. Systemic delivery of siRNA by chimeric capsid protein: tumor targeting and RNAi activity in vivo. Mol. Pharm. 10:18–25 [Google Scholar]
  60. Azizgolshani O, Garmann RF, Cadena-Nava R, Knobler CM, Gelbart WM. 60.  2013. Reconstituted plant viral capsids can release genes to mammalian cells. Virology 441:12–17 [Google Scholar]
  61. Aljabali AA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ. 61.  2013. CPMV-DOX delivers. Mol. Pharm. 10:3–10 [Google Scholar]
  62. Ren Y, Wong SM, Lim LY. 62.  2007. Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjug. Chem. 18:836–43 [Google Scholar]
  63. Pokorski JK, Breitenkamp K, Liepold LO, Qazi S, Finn MG. 63.  2011. Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J. Am. Chem. Soc. 133:9242–45 [Google Scholar]
  64. Hovlid ML, Lau JL, Breitenkamp K, Higginson CJ, Laufer B. 64.  et al. 2014. Encapsidated atom-transfer radical polymerization in Qβ virus-like nanoparticles. ACS Nano 8:8003–14 [Google Scholar]
  65. Rhee JK, Baksh M, Nycholat C, Paulson JC, Kitagishi H, Finn MG. 65.  2012. Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules 13:2333–38 [Google Scholar]
  66. Millán JG, Brasch M, Anaya-Plaza E, de la Escosura A, Velders AH. 66.  et al. 2014. Self-assembly triggered by self-assembly: optically active, paramagnetic micelles encapsulated in protein cage nanoparticles. J. Inorg. Biochem. 136:140–46 [Google Scholar]
  67. Everts M, Saini V, Leddon JL, Kok RJ, Stoff-Khalili M. 67.  et al. 2006. Covalently linked Au nanoparticles to a viral vector: potential for combined photothermal and gene cancer therapy. Nano Lett. 6:587–91 [Google Scholar]
  68. Greenwood B, Salisbury D, Hill AV. 68.  2011. Vaccines and global health. Philos. Trans. R. Soc. B 366:2733–42 [Google Scholar]
  69. Levine MM, Robins-Browne R. 69.  2009. Vaccines, global health and social equity. Immunol. Cell Biol. 87:274–78 [Google Scholar]
  70. McElrath MJ, Walker BD. 70.  2012. Is an HIV vaccine possible?. JAIDS 60:Suppl. 2S41–43 [Google Scholar]
  71. Ottenhoff TH, Kaufmann SH. 71.  2012. Vaccines against tuberculosis: Where are we and where do we need to go?. PLOS Pathog. 8:e1002607 [Google Scholar]
  72. Thera MA, Plowe CV. 72.  2012. Vaccines for malaria: How close are we?. Annu. Rev. Med. 63:345–57 [Google Scholar]
  73. Chackerian B, Rangel M, Hunter Z, Peabody DS. 73.  2006. Virus and virus-like particle-based immunogens for Alzheimer's disease induce antibody responses against amyloid-β without concomitant T cell responses. Vaccine 24:6321–31 [Google Scholar]
  74. Kushnir N, Streatfield SJ, Yusibov V. 74.  2012. Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 31:58–83 [Google Scholar]
  75. Miermont A, Barnhill H, Strable E, Lu X, Wall KA. 75.  et al. 2008. Cowpea mosaic virus capsid: a promising carrier for the development of carbohydrate based antitumor vaccines. Chemistry 14:4939–47 [Google Scholar]
  76. Yin Z, Nguyen HG, Chowdhury S, Bentley P, Bruckman MA. 76.  et al. 2012. Tobacco mosaic virus as a new carrier for tumor associated carbohydrate antigens. Bioconjug. Chem. 23:1694–703 [Google Scholar]
  77. Parmiani G, Russo V, Maccalli C, Parolini D, Rizzo N, Maio M. 77.  2014. Peptide-based vaccines for cancer therapy. Hum. Vaccines Immunother. 10:3175–78 [Google Scholar]
  78. Geynisman D, Chien CR, Smieliauskas F, Shen C, Tina Shih YC. 78.  2014. Economic evaluation of therapeutic cancer vaccines and immunotherapy: a systematic review. Hum. Vaccines Immunother. 10:3415–24 [Google Scholar]
  79. Tagliamonte M, Petrizzo A, Tornesello ML, Buonaguro FM, Buonaguro L. 79.  2014. Antigen-specific vaccines for cancer treatment. Hum. Vaccines Immunother. 10:3332–46 [Google Scholar]
  80. Winter H, Fox BA, Ruttinger D. 80.  2014. Future of cancer vaccines. Methods Mol. Biol. 1139:555–64 [Google Scholar]
  81. Garcea RL, Gissmann L. 81.  2004. Virus-like particles as vaccines and vessels for the delivery of small molecules. Curr. Opin. Biotechnol. 15:513–17 [Google Scholar]
  82. Grgacic EV, Anderson DA. 82.  2006. Virus-like particles: passport to immune recognition. Methods 40:60–65 [Google Scholar]
  83. Ludwig C, Wagner R. 83.  2007. Virus-like particles—universal molecular toolboxes. Curr. Opin. Biotechnol. 18:537–45 [Google Scholar]
  84. Folb PI, Bernatowska E, Chen R, Clemens J, Dodoo AN. 84.  et al. 2004. A global perspective on vaccine safety and public health: the Global Advisory Committee on Vaccine Safety. Am. J. Public Health 94:1926–31 [Google Scholar]
  85. Kelso JM. 85.  2012. Safety of influenza vaccines. Curr. Opin. Allergy Clin. Immunol. 12:383–88 [Google Scholar]
  86. Tozzi AE, Asturias EJ, Balakrishnan MR, Halsey NA, Law B, Zuber PL. 86.  2013. Assessment of causality of individual adverse events following immunization (AEFI): a WHO tool for global use. Vaccine 44:5041–46 [Google Scholar]
  87. Klinman DM, Takeno M, Ichino M, Gu M, Yamshchikov G. 87.  et al. 1997. DNA vaccines: safety and efficacy issues. Springer Semin. Immunopathol. 19:245–56 [Google Scholar]
  88. Aguilar JC, Rodriguez EG. 88.  2007. Vaccine adjuvants revisited. Vaccine 25:3752–62 [Google Scholar]
  89. Awate S, Babiuk LA, Mutwiri G. 89.  2013. Mechanisms of action of adjuvants. Front. Immunol. 4:114 [Google Scholar]
  90. Bramwell VW, Perrie Y. 90.  2005. The rational design of vaccines. Drug Discov. Today 10:1527–34 [Google Scholar]
  91. Leleux J, Roy K. 91.  2013. Micro and nanoparticle-based delivery systems for vaccine immunotherapy: an immunological and materials perspective. Adv. Healthc. Mater. 2:72–94 [Google Scholar]
  92. De Temmerman ML, Rejman J, Demeester J, Irvine DJ, Gander B, De Smedt SC. 92.  2011. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 16:569–82 [Google Scholar]
  93. Banchereau J, Steinman RM. 93.  1998. Dendritic cells and the control of immunity. Nature 392:245–52 [Google Scholar]
  94. Neefjes J, Jongsma ML, Paul P, Bakke O. 94.  2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11:823–36 [Google Scholar]
  95. Vyas JM, Van der Veen AG, Ploegh HL. 95.  2008. The known unknowns of antigen processing and presentation. Nat. Rev. Immunol. 8:607–18 [Google Scholar]
  96. Pushko P, Pumpens P, Grens E. 96.  2013. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology 56:141–65 [Google Scholar]
  97. Roldao A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. 97.  2010. Virus-like particles in vaccine development. Expert Rev. Vaccines 9:1149–76 [Google Scholar]
  98. Chan JK, Berek JS. 98.  2007. Impact of the human papilloma vaccine on cervical cancer. J. Clin. Oncol. 25:2975–82 [Google Scholar]
  99. Sominskaya I, Skrastina D, Dislers A, Vasiljev D, Mihailova M. 99.  et al. 2010. Construction and immunological evaluation of multivalent hepatitis B virus (HBV) core virus-like particles carrying HBV and HCV epitopes. Clin. Vaccine Immunol. 17:1027–33 [Google Scholar]
  100. Cheong WS, Reiseger J, Turner SJ, Boyd R, Netter HJ. 100.  2009. Chimeric virus-like particles for the delivery of an inserted conserved influenza A-specific CTL epitope. Antiviral Res. 81:113–22 [Google Scholar]
  101. Brennan FR, Gilleland LB, Staczek J, Bendig MM, Hamilton WD, Gilleland HE Jr. 101.  1999. A chimaeric plant virus vaccine protects mice against a bacterial infection. Microbiology 145:2061–67 [Google Scholar]
  102. Brennan K, McSherry EA, Hudson L, Kay EW, Hill AD. 102.  et al. 2013. Junctional adhesion molecule-A is co-expressed with HER2 in breast tumors and acts as a novel regulator of HER2 protein degradation and signaling. Oncogene 32:2799–804 [Google Scholar]
  103. Koo M, Bendahmane M, Lettieri GA, Paoletti AD, Lane TE. 103.  et al. 1999. Protective immunity against murine hepatitis virus (MHV) induced by intranasal or subcutaneous administration of hybrids of tobacco mosaic virus that carries an MHV epitope. PNAS 96:7774–79 [Google Scholar]
  104. Nuzzaci M, Piazzolla G, Vitti A, Lapelosa M, Tortorella C. 104.  et al. 2007. Cucumber mosaic virus as a presentation system for a double hepatitis C virus-derived epitope. Arch. Virol. 152:915–28 [Google Scholar]
  105. Rennermalm A, Li YH, Bohaufs L, Jarstrand C, Brauner A. 105.  et al. 2001. Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat. Vaccine 19:3376–83 [Google Scholar]
  106. Wu L, Jiang L, Zhou Z, Fan J, Zhang Q. 106.  et al. 2003. Expression of foot-and-mouth disease virus epitopes in tobacco by a tobacco mosaic virus-based vector. Vaccine 21:4390–98 [Google Scholar]
  107. Yusibov V, Mett V, Mett V, Davidson C, Musiychuk K. 107.  et al. 2005. Peptide-based candidate vaccine against respiratory syncytial virus. Vaccine 23:2261–65 [Google Scholar]
  108. Caldeira JdC, Medford A, Kines RC, Lino CA, Schiller JT. 108.  et al. 2010. Immunogenic display of diverse peptides, including a broadly cross-type neutralizing human papillomavirus L2 epitope, on virus-like particles of the RNA bacteriophage PP7. Vaccine 28:4384–93 [Google Scholar]
  109. Richert LE, Rynda-Apple A, Harmsen AL, Han S, Wiley JA. 109.  et al. 2014. CD11c+ cells primed with unrelated antigens facilitate an accelerated immune response to influenza virus in mice. Eur. J. Immunol. 44:397–408 [Google Scholar]
  110. Manayani DJ, Thomas D, Dryden KA, Reddy V, Siladi ME. 110.  et al. 2007. A viral nanoparticle with dual function as an anthrax antitoxin and vaccine. PLOS Pathog. 3:1422–31 [Google Scholar]
  111. Bhatia BD, Chug S, Narang P, Singh MN. 111.  1988. Bacterial flora of newborns at birth and 72 hours of age. Indian Pediatr. 25:1058–65 [Google Scholar]
  112. Schiller JT, Lowy DR. 112.  2001. Papillomavirus-like particle vaccines. J. Natl. Cancer Inst. Monogr. 2000:50–54 [Google Scholar]
  113. Skrastina D, Petrovskis I, Petraityte R, Sominskaya I, Ose V. 113.  et al. 2013. Chimeric derivatives of hepatitis B virus core particles carrying major epitopes of the rubella virus E1 glycoprotein. Clin. Vaccine Immunol. 20:1719–28 [Google Scholar]
  114. Schneemann A, Speir JA, Tan GS, Khayat R, Ekiert DC. 114.  et al. 2012. A virus-like particle that elicits cross-reactive antibodies to the conserved stem of influenza virus hemagglutinin. J. Virol. 86:11686–97 [Google Scholar]
  115. Rynda-Apple A, Patterson DP, Douglas T. 115.  2014. Virus-like particles as antigenic nanomaterials for inducing protective immune responses in the lung. Nanomedicine 9:1857–68 [Google Scholar]
  116. Yaddanapudi K, Mitchell RA, Eaton JW. 116.  2013. Cancer vaccines: looking to the future. Oncoimmunology 2:e23403 [Google Scholar]
  117. Ryan SO, Turner MS, Gariepy J, Finn OJ. 117.  2010. Tumor antigen epitopes interpreted by the immune system as self or abnormal-self differentially affect cancer vaccine responses. Cancer Res. 70:5788–96 [Google Scholar]
  118. Rosenberg SA. 118.  2000. The identification of cancer antigens: impact on the development of cancer vaccines. Cancer J. 6:Suppl. 2S142–49 [Google Scholar]
  119. Shukla S, Wen AM, Commandeur U, Steinmetz NF. 119.  2014. Presentation of HER2 epitopes using a filamentous plant virus-based vaccination platform. J. Mater. Chem. B 2:6249–58 [Google Scholar]
  120. Chackerian B. 120.  2010. Virus-like particle based vaccines for Alzheimer disease. Hum. Vaccines 6:926–30 [Google Scholar]
  121. Jin H, Wang W, Zhao S, Yang W, Qian Y. 121.  et al. 2014. Aβ-HBc virus-like particles immunization without additional adjuvant ameliorates the learning and memory and reduces Aβ deposit in PDAPP mice. Vaccine 32:4450–56 [Google Scholar]
  122. Feng G, Wang W, Qian Y, Jin H. 122.  2013. Anti-Aβ antibodies induced by Aβ-HBc virus-like particles prevent Aβ aggregation and protect PC12 cells against toxicity of Aβ1−40. J. Neurosci. Methods 218:48–54 [Google Scholar]
  123. Maurer P, Jennings GT, Willers J, Rohner F, Lindman Y. 123.  et al. 2005. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and phase I safety and immunogenicity. Eur. J. Immunol. 35:2031–40 [Google Scholar]
  124. Cornuz J, Zwahlen S, Jungi WF, Osterwalder J, Klingler K. 124.  et al. 2008. A vaccine against nicotine for smoking cessation: a randomized controlled trial. PLOS ONE 3:e2547 [Google Scholar]
  125. Robertson KL, Liu JL. 125.  2012. Engineered viral nanoparticles for flow cytometry and fluorescence microscopy applications. WIRES Nanomed. Nanobiotechnol. 4:511–24 [Google Scholar]
  126. Koudelka KJ, Manchester M. 126.  2010. Chemically modified viruses: principles and applications. Curr. Opin. Chem. Biol. 14:810–17 [Google Scholar]
  127. Schoonen L, van Hest JC. 127.  2014. Functionalization of protein-based nanocages for drug delivery applications. Nanoscale 6:7124–41 [Google Scholar]
  128. Ghosh D, Kohli AG, Moser F, Endy D, Belcher AM. 128.  2012. Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth. Biol. 1:576–82 [Google Scholar]
  129. Shukla S, Dickmeis C, Nagarajan AS, Fischer R, Commandeur U, Steinmetz NF. 129.  2014. Molecular farming of fluorescent virus-based nanoparticles for optical imaging in plants, human cells and mouse models. Biomater. Sci. 2:784–97 [Google Scholar]
  130. Koudelka KJ, Ippoliti S, Medina E, Shriver LP, Trauger SA. 130.  et al. 2013. Lysine addressability and mammalian cell interactions of bacteriophage λ procapsids. Biomacromolecules 14:4169–76 [Google Scholar]
  131. Chang JR, Song EH, Nakatani-Webster E, Monkkonen L, Ratner DM, Catalano CE. 131.  2014. Phage lambda capsids as tunable display nanoparticles. Biomacromolecules 15:4410–19 [Google Scholar]
  132. Tsvetkova IB, Cheng F, Ma Z, Moore AW, Howard B. 132.  et al. 2013. Fusion of mApple and Venus fluorescent proteins to the Sindbis virus E2 protein leads to different cell-binding properties. Virus Res. 177:138–46 [Google Scholar]
  133. Cheng F, Tsvetkova IB, Khuong YL, Moore AW, Arnold RJ. 133.  et al. 2012. The packaging of different cargo into enveloped viral nanoparticles. Mol. Pharm. 10:51–58 [Google Scholar]
  134. Jin HE, Farr R, Lee SW. 134.  2014. Collagen mimetic peptide engineered M13 bacteriophage for collagen targeting and imaging in cancer. Biomaterials 33:9236–45 [Google Scholar]
  135. Grove J. 135.  2014. Super-resolution microscopy: a virus' eye view of the cell. Viruses 6:1365–78 [Google Scholar]
  136. Obermeyer AC, Capehart SL, Jarman JB, Francis MB. 136.  2014. Multivalent viral capsids with internal cargo for fibrin imaging. PLOS ONE 9:e100678 [Google Scholar]
  137. Jung B, Rao AL, Anvari B. 137.  2011. Optical nano-constructs composed of genome-depleted brome mosaic virus doped with a near infrared chromophore for potential biomedical applications. ACS Nano 5:1243–52 [Google Scholar]
  138. Jung B, Anvari B. 138.  2013. Virus-mimicking optical nanomaterials: near infrared absorption and fluorescence characteristics and physical stability in biological environments. ACS Appl. Mater. Interfaces 5:7492–500 [Google Scholar]
  139. Leeuw TK, Reith RM, Simonette RA, Harden ME, Cherukuri P. 139.  et al. 2007. Single-walled carbon nanotubes in the intact organism: near-IR imaging and biocompatibility studies in Drosophila. Nano Lett 7:2650–54 [Google Scholar]
  140. Yi H, Ghosh D, Ham MH, Qi J, Barone PW. 140.  et al. 2012. M13 phage-functionalized single-walled carbon nanotubes as nanoprobes for second near-infrared window fluorescence imaging of targeted tumors. Nano Lett 12:1176–83 [Google Scholar]
  141. Ghosh D, Bagley AF, Na YJ, Birrer MJ, Bhatia SN, Belcher AM. 141.  2014. Deep, noninvasive imaging and surgical guidance of submillimeter tumors using targeted M13-stabilized single-walled carbon nanotubes. PNAS 111:13948–53 [Google Scholar]
  142. Qazi S, Liepold LO, Abedin MJ, Johnson B, Prevelige P. 142.  et al. 2013. P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. Mol. Pharm. 10:11–17 [Google Scholar]
  143. Min J, Jung H, Shin HH, Cho G, Cho H, Kang S. 143.  2013. Implementation of P22 viral capsids as intravascular magnetic resonance T1 contrast conjugates via site-selective attachment of Gd(III)-chelating agents. Biomacromolecules 14:2332–39 [Google Scholar]
  144. Qazi S, Uchida M, Usselman R, Shearer R, Edwards E, Douglas T. 144.  2014. Manganese(III) porphyrins complexed with P22 virus-like particles as T1-enhanced contrast agents for magnetic resonance imaging. J. Biol. Inorg. Chem 19:237–46 [Google Scholar]
  145. Bruckman MA, Hern S, Jiang K, Flask CA, Yu X, Steinmetz NF. 145.  2013. Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. J. Mater. Chem. B 1:1482–90 [Google Scholar]
  146. Bruckman MA, Jiang K, Simpson EJ, Randolph LN, Luyt LG. 146.  et al. 2014. Dual-modal magnetic resonance and fluorescence imaging of atherosclerotic plaques in vivo using VCAM-1 targeted tobacco mosaic virus. Nano Lett. 14:1551–58 [Google Scholar]
  147. Ghosh D, Lee Y, Thomas S, Kohli AG, Yun DS. 147.  et al. 2012. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat. Nanotechnol. 7:677–82 [Google Scholar]
  148. Huang X, Stein BD, Cheng H, Malyutin A, Tsvetkova IB. 148.  et al. 2011. Magnetic virus-like nanoparticles in N. benthamiana plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 5:4037–45 [Google Scholar]
  149. Meldrum T, Seim KL, Bajaj VS, Palaniappan KK, Wu W. 149.  et al. 2010. A xenon-based molecular sensor assembled on an MS2 viral capsid scaffold. J. Am. Chem. Soc. 132:5936–37 [Google Scholar]
  150. Palaniappan KK, Ramirez RM, Bajaj VS, Wemmer DE, Pines A, Francis MB. 150.  2013. Molecular imaging of cancer cells using a bacteriophage-based 129Xe NMR biosensor. Angew. Chem. Int. Ed. 52:4849–53 [Google Scholar]
  151. Farkas ME, Aanei IL, Behrens CR, Tong GJ, Murphy ST. 151.  et al. 2013. PET imaging and biodistribution of chemically modified bacteriophage MS2. Mol. Pharm. 10:69–76 [Google Scholar]
  152. Mukherjee S, Pfeifer CM, Johnson JM, Liu J, Zlotnick A. 152.  2006. Redirecting the coat protein of a spherical virus to assemble into tubular nanostructures. J. Am. Chem. Soc. 128:2538–39 [Google Scholar]
  153. Bruckman MA, VanMeter A, Steinmetz NF. 153.  2015. Nanomanufacturing of tobacco mosaic virus-based spherical biomaterials using a continuous flow method. ACS Biomater. Sci. Eng. 1:13–18 [Google Scholar]
  154. Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T. 154.  2012. Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8:10158–66 [Google Scholar]
  155. Carette N, Engelkamp H, Akpa E, Pierre SJ, Cameron NR. 155.  et al. 2007. A virus-based biocatalyst. Nat. Nanotechnol. 2:226–29 [Google Scholar]
  156. Guo P, Lee TJ. 156.  2007. Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol. 64:886–903 [Google Scholar]
  157. Schneemann A, Young MJ. 157.  2003. Viral assembly using heterologous expression systems and cell extracts. Adv. Protein Chem. 64:1–36 [Google Scholar]
  158. Gillitzer E, Suci P, Young M, Douglas T. 158.  2006. Controlled ligand display on a symmetrical protein-cage architecture through mixed assembly. Small 2:962–66 [Google Scholar]
  159. Douglas T, Young M. 159.  1998. Host-guest encapsulation of materials by assembled virus protein cages. Nature 393:152–55 [Google Scholar]
  160. Ren Y, Wong SM, Lim LY. 160.  2006. In vitro-reassembled plant virus-like particles for loading of polyacids. J. Gen. Virol. 87:2749–54 [Google Scholar]
  161. Phelps JP, Dang N, Rasochova L. 161.  2007. Inactivation and purification of cowpea mosaic virus-like particles displaying peptide antigens from Bacillus anthracis. J. Virol. Methods 141:146–53 [Google Scholar]
  162. Lytle CD, Sagripanti JL. 162.  2005. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J. Virol. 79:14244–52 [Google Scholar]
  163. Bruckman MA, Randolph LN, Vanmeter A, Hern S, Shoffstall AJ. 163.  et al. 2014. Biodistribution, pharmacokinetics, and blood compatibility of native and PEGylated tobacco mosaic virus nano-rods and -spheres in mice. Virology 449:163–73 [Google Scholar]
  164. Kaiser CR, Flenniken ML, Gillitzer E, Harmsen AL, Harmsen AG. 164.  et al. 2007. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int. J. Nanomed. 2:715–33 [Google Scholar]
  165. Ruggiero A, Villa CH, Bander E, Rey DA, Bergkvist M. 165.  et al. 2010. Paradoxical glomerular filtration of carbon nanotubes. PNAS 107:12369–74 [Google Scholar]
  166. Singh R, Pantarotto D, Lacerda L, Pastorin G, Klumpp C. 166.  et al. 2006. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. PNAS 103:3357–62 [Google Scholar]
  167. Lee KL, Shukla S, Wu M, Ayat NR, El Sanadi CE. 167.  et al. 2015. Stealth filaments: Polymer chain length and conformation affect the in vivo fate of PEGylated potato virus X. Acta Biomater. 19:166–79 [Google Scholar]
  168. Semmler-Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A. 168.  et al. 2008. Biodistribution of 1.4- and 18-nm gold particles in rats. Small 4:2108–11 [Google Scholar]
  169. Tarn D, Ashley CE, Xue M, Carnes EC, Zink JI, Brinker CJ. 169.  2013. Mesoporous silica nanoparticle nanocarriers: biofunctionality and biocompatibility. Acc. Chem. Res. 46:792–801 [Google Scholar]
  170. Jaganathan H, Godin B. 170.  2012. Biocompatibility assessment of Si-based nano- and micro-particles. Adv. Drug Deliv. Rev. 64:1800–19 [Google Scholar]
  171. Liu Y, Zhao Y, Sun B, Chen C. 171.  2013. Understanding the toxicity of carbon nanotubes. Acc. Chem. Res. 46:702–13 [Google Scholar]
  172. Shukla S, Wen AM, Ayat NR, Commandeur U, Gopalkrishnan R. 172.  et al. 2014. Biodistribution and clearance of a filamentous plant virus in healthy and tumor-bearing mice. Nanomedicine 9:221–35 [Google Scholar]
  173. Rae CS, Khor IW, Wang Q, Destito G, Gonzalez MJ. 173.  et al. 2005. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 343:224–35 [Google Scholar]
  174. Baiu DC, Brazel CS, Bao Y, Otto M. 174.  2013. Interactions of iron oxide nanoparticles with the immune system: challenges and opportunities for their use in nano-oncology. Curr. Pharm. Des. 19:6606–21 [Google Scholar]
  175. Meng J, Yang M, Jia F, Xu Z, Kong H, Xu H. 175.  2011. Immune responses of BALB/c mice to subcutaneously injected multi-walled carbon nanotubes. Nanotoxicology 5:583–91 [Google Scholar]
  176. Raja KS, Wang Q, Gonzalez MJ, Manchester M, Johnson JE, Finn MG. 176.  2003. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules 4:472–76 [Google Scholar]
  177. Semple SC, Harasym TO, Clow KA, Ansell SM, Klimuk SK, Hope MJ. 177.  2005. Immunogenicity and rapid blood clearance of liposomes containing polyethylene glycol-lipid conjugates and nucleic acid. J. Pharmacol. Exp. Ther. 312:1020–26 [Google Scholar]
  178. Shimizu T, Ishida T, Kiwada H. 178.  2013. Transport of PEGylated liposomes from the splenic marginal zone to the follicle in the induction phase of the accelerated blood clearance phenomenon. Immunobiology 218:725–32 [Google Scholar]
  179. Harris JM, Chess RB. 179.  2003. Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2:214–21 [Google Scholar]
  180. Roberts MJ, Bentley MD, Harris JM. 180.  2002. Chemistry for peptide and protein PEGylation. Adv. Drug Deliv. Rev. 54:459–76 [Google Scholar]
  181. Wattendorf U, Merkle HP. 181.  2008. PEGylation as a tool for the biomedical engineering of surface modified microparticles. J. Pharm. Sci. 97:4655–69 [Google Scholar]
  182. Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. 182.  2013. Minimal “self” peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 339:971–75 [Google Scholar]
  183. Agrawal A, Manchester M. 183.  2012. Differential uptake of chemically modified cowpea mosaic virus nanoparticles in macrophage subpopulations present in inflammatory and tumor microenvironments. Biomacromolecules 13:3320–26 [Google Scholar]
  184. Plummer EM, Manchester M. 184.  2013. Endocytic uptake pathways utilized by CPMV nanoparticles. Mol. Pharm. 10:26–32 [Google Scholar]
  185. Plummer EM, Thomas D, Destito G, Shriver LP, Manchester M. 185.  2012. Interaction of cowpea mosaic virus nanoparticles with surface vimentin and inflammatory cells in atherosclerotic lesions. Nanomedicine 7:877–88 [Google Scholar]
  186. Shriver LP, Koudelka KJ, Manchester M. 186.  2009. Viral nanoparticles associate with regions of inflammation and blood brain barrier disruption during CNS infection. J. Neuroimmunol. 211:66–72 [Google Scholar]
  187. Steinmetz NF, Cho CF, Ablack A, Lewis JD, Manchester M. 187.  2011. Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells. Nanomedicine 6:351–64 [Google Scholar]
  188. Steinmetz NF, Maurer J, Sheng H, Bensussan A, Maricic I. 188.  et al. 2011. Two domains of vimentin are expressed on the surface of lymph node, bone and brain metastatic prostate cancer lines along with the putative stem cell marker proteins CD44 and CD133. Cancers 3:2870–85 [Google Scholar]
  189. Koudelka KJ, Destito G, Plummer EM, Trauger SA, Siuzdak G, Manchester M. 189.  2009. Endothelial targeting of cowpea mosaic virus (CPMV) via surface vimentin. PLOS Pathog. 5:e1000417 [Google Scholar]
  190. Desai MS, Lee SW. 190.  2014. Protein-based functional nanomaterial design for bioengineering applications. WIRES Nanomed. Nanobiotechnol. 7:69–97 [Google Scholar]
/content/journals/10.1146/annurev-virology-100114-055141
Loading
/content/journals/10.1146/annurev-virology-100114-055141
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error