Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 634-641 , October 2010

Viral nanoparticles as platforms for next-generation therapeutics and imaging devices

  • Nicole F. Steinmetz, PhD

      Affiliations

    • Department of Molecular Biology and Center of Integrative Molecular Biology, The Scripps Research Institute, La Jolla, CA, USA
    • Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA
    • Corresponding Author InformationCorresponding author: Department of Molecular Biology and Center of Integrative Molecular Biology, The Scripps Research Institute, La Jolla, CA 92037, USA.

Received 28 January 2010 ,Accepted 7 April 2010.

References 

  1. Majoros IJ, Williams CR, Baker Jr. Current dendrimer applications in cancer diagnosis and therapy. Curr Top Med Chem. 2008;8:1165–1179
  2. Manchester M, Singh P. Virus-based nanoparticles (VNPs): platform technologies for diagnostic imaging. Adv Drug Deliv Rev. 2006;58:1505–1522
  3. Soussan E, Cassel S, Blanzat M, Rico-Lattes I. Drug delivery by soft matter: matrix and vesicular carriers. Angew Chem Int Ed Engl. 2009;48:274–288
  4. Xing Y, Rao J. Quantum dot bioconjugates for in vitro diagnostics and in vivo imaging. Cancer Biomark. 2008;4:307–319
  5. Portney NG, Ozkan M. Nano-oncology: drug delivery, imaging, and sensing. Anal Bioanal Chem. 2006;384:620–630
  6. Svenson S, Tomalia DA. Dendrimers in biomedical applications—reflections on a field. Adv Drug Deliv Rev. 2005;57:2106–2129
  7. Murphy EA, Majeti BK, Barnes LA, Makale M, Weis SM, Lutu-Fuga K, et al. Nanoparticle-mediated drug delivery to tumor vasculature suppresses metastasis. Proc Natl Acad Sci USA. 2008;105:9343–9348
  8. Flynn CE, Lee S-W, Peelle BR, Belcher AM. Viruses as vehicles for growth, organisation and assembly of materials. Acta Mater. 2003;51:5867–5880
  9. Young M, Willits D, Uchida M, Douglas T. Plant viruses as biotemplates for materials and their use in nanotechnology. Annu Rev Phytopathol. 2008;46:361–384
  10. Steinmetz NF, Evans DJ. Utilisation of plant viruses in bionanotechnology. Org Biomol Chem. 2007;5:2891–2902
  11. Campos SK, Barry MA. Current advances and future challenges in adenoviral vector biology and targeting. Curr Gene Ther. 2007;7:189–204
  12. Parker AL, Nicklin SA, Baker AH. Interactions of adenovirus vectors with blood: implications for intravascular gene therapy applications. Curr Opin Mol Ther. 2008;10:439–448
  13. Singh R, Kostarelos K. Designer adenoviruses for nanomedicine and nanodiagnostics. Trends Biotechnol. 2009;27:220–229
  14. Ben-Gary H, McKinney RL, Rosengart T, Lesser ML, Crystal RG. Systemic interleukin-6 responses following administration of adenovirus gene transfer vectors to humans by different routes. Mol Ther. 2002;6:287–297
  15. Cotter MJ, Muruve DA. The induction of inflammation by adenovirus vectors used for gene therapy. Front Biosci. 2005;10:1098–1105
  16. Engler H, Machemer T, Philopena J, Wen SF, Quijano E, Ramachandra M, et al. Acute hepatotoxicity of oncolytic adenoviruses in mouse models is associated with expression of wild-type E1a and induction of TNF-α. Virology. 2004;328:52–61
  17. Singh P, Prasuhn D, Yeh RM, Destito G, Rae CS, Osborn K, et al. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J Control Release. 2007;120:41–50
  18. Kaiser CR, Flenniken ML, Gillitzer E, Harmsen AL, Harmsen AG, Jutila MA, et al. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int J Nanomed. 2007;2:715–733
  19. Rae CS, Khor IW, Wang Q, Destito G, Gonzalez MJ, Singh P, et al. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology. 2005;343:224–235
  20. Molenaar TJ, Michon I, de Haas SA, van Berkel TJ, Kuiper J, Biessen EA. Uptake and processing of modified bacteriophage M13 in mice: implications for phage display. Virology. 2002;293:182–191
  21. Prasuhn Jr, 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
  22. Peiser L, Mukhopadhyay S, Gordon S. Scavenger receptors in innate immunity. Curr Opin Immunol. 2002;14:123–128
  23. Thurber GM, Schmidt MM, Wittrup KD. Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance. Adv Drug Deliv Rev. 2008;60:1421–1434
  24. Li SD, Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol Pharm. 2008;5:496–504
  25. Bruckman MA, Kaur G, Lee LA, Xie F, Sepulveda J, Breitenkamp R, et al. Surface modification of tobacco mosaic virus with "click" chemistry. Chembiochem. 2008;9:519–523
  26. 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
  27. Steinmetz NF, Mertens ME, Taurog RE, Johnson JE, Commandeur U, Fischer R, et al. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 2010;10:305–312
  28. 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
  29. 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
  30. Lewis JD, Destito G, Zijlstra A, Gonzalez MJ, Quigley JP, Manchester M, et al. Viral nanoparticles as tools for intravital vascular imaging. Nat Med. 2006;12:354–360
  31. 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;3:472–476
  32. Steinmetz NF, Lin T, Lomonossoff GP, Johnson JE. Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology. Curr Top Microbiol Immunol. 2009;327:23–58
  33. Dragnea B, Chen C, Kwak ES, Stein B, Kao CC. Gold nanoparticles as spectroscopic enhancers for in vitro studies on single viruses. J Am Chem Soc. 2003;125:6374–6375
  34. Portney NG, Singh K, Chaudhary S, Destito G, Schneemann A, Manchester M, et al. Organic and inorganic nanoparticle hybrids. Langmuir. 2005;21:2098–2103
  35. Souza GR, Christianson DR, Staquicini FI, Ozawa MG, Snyder EY, Sidman RL, et al. Networks of gold nanoparticles and bacteriophage as biological sensors and cell targeting agents. Proc Natl Acad Sci U S A. 2007;103:1215–1220
  36. Wu C, Barnhill H, Liang X, Wang Q, Jiang H. A new probe using hybrid virus-dye nanoparticles for near-infrared fluorescence tomography. Optics Commun. 2005;255:366–374
  37. Aime S, Cabella C, Colombatto S, Geninatti Crich S, Gianolio E, Maggioni F. Insights into the use of paramagnetic Gd(III) complexes in MR-molecular imaging investigations. J Magn Reson Imaging. 2002;16:394–406
  38. Immordino ML, Dosio F, Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomed. 2006;1:297–315
  39. Kobayashi H, Brechbiel MW. Nano-sized MRI contrast agents with dendrimer cores. Adv Drug Deliv Rev. 2005;57:2271–2286
  40. Liepold L, Anderson S, Willits D, Oltrogge L, Frank JA, Douglas T, et al. Viral capsids as MRI contrast agents. Magn Reson Med. 2007;58:871–879
  41. Anderson EA, Isaacman S, Peabody DS, Wang EY, Canary JW, Kirshenbaum K. Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett. 2006;6:1160–1164
  42. Allen M, Bulte JW, Liepold L, Basu G, Zywicke HA, Frank JA, et al. Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents. Magn Reson Med. 2005;54:807–812
  43. Prasuhn DE, 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
  44. Hooker JM, Datta A, Botta M, Raymond KN, Francis MB. Magnetic resonance contrast agents from viral capsid shells: a comparison of exterior and interior cargo strategies. Nano Lett. 2007;7:2207–2210
  45. Ruoslahti E. Specialization of tumor vasculature. Nat Rev Cancer. 2002;2:83–90
  46. Nanda A, St. Croix B. Tumor endothelial markers: new targets for cancer therapy. Curr Opin Oncol. 2004;16:44–49
  47. Arap W, Haedicke W, Bernasconi M, Kain R, Rajotte D, Krajewski S, et al. Targeting the prostate for destruction through a vascular address. Proc Natl Acad Sci U S A. 2002;99:1527–1531
  48. Hajitou A, Pasqualini R, Arap W. Vascular targeting: recent advances and therapeutic perspectives. Trends Cardiovasc Med. 2006;16:80–88
  49. Koudelka KJ, Destito G, Plummer EM, Trauger SA, Siuzdak G, Manchester M. Endothelial targeting of cowpea mosaic virus via surface vimentin. PLOS Pathogens. 2009;5:e1000417
  50. Wang N, Stamenovic D. Mechanics of vimentin intermediate filaments. J Muscle Res Cell Motil. 2002;23:535–540
  51. Evans RM. Vimentin: the conundrum of the intermediate filament gene family. Bioessays. 1998;20:79–86
  52. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM. Vimentin is secreted by activated macrophages. Nat Cell Biol. 2003;5:59–63
  53. van Beijnum JR, Dings RP, van der Linden E, Zwaans BM, Ramaekers FC, Mayo KH, et al. Gene expression of tumor angiogenesis dissected: specific targeting of colon cancer angiogenic vasculature. Blood. 2006;108:2339–2348
  54. Xu B, deWaal RM, Mor-Vaknin N, Hibbard C, Markovitz DM, Kahn ML. The endothelial cell-specific antibody PAL-E identifies a secreted form of vimentin in the blood vasculature. Mol Cell Biol. 2004;24:9198–9206
  55. Shriver LP, Koudelka KJ, Manchester M. Viral nanoparticles associate with regions of inflammation and blood brain barrier disruption during CNS infection. J Neuroimmunol. 2009;211:66–72
  56. Brown WL, Mastico RA, Wu M, Heal KG, Adams CJ, Murray JB, et al. RNA bacteriophage capsid-mediated drug delivery and epitope presentation. Intervirology. 2002;45:371–380
  57. Sen Gupta S, Kuzelka J, Singh P, Lewis WG, Manchester M, Finn MG. Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug Chem. 2005;16:1572–1579
  58. Ren Y, Wong SM, Lim LY. Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjug Chem. 2007;18:836–843
  59. Steinmetz NF, Hong V, Spoerke ED, Lu P, Breitenkamp K, Finn MG, et al. Buckyballs meet viral nanoparticles: candidates for biomedicine. J Am Chem Soc. 2009;131:17093–17095
  60. 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
  61. Yacoby I, Shamis M, Bar H, Shabat D, Benhar I. Targeting antibacterial agents by using drug-carrying filamentous bacteriophages. Antimicrob Agents Chemother. 2006;50:2087–2097
  62. Bar H, Yacoby I, Benhar I. Killing cancer cells by targeted drug-carrying phage nanomedicines. BMC Biotechnol. 2008;8:37
  63. Loo L, Guenther RH, Lommel SA, Franzen S. Infusion of dye molecules into Red clover necrotic mosaic virus. Chemical Commun. 2008;(1):88–90

 This study was funded by an American Heart Association Postdoctoral Fellowship and National Institutes of Health grant K99 EB009105.

PII: S1549-9634(10)00103-6

doi: 10.1016/j.nano.2010.04.005

Nanomedicine: Nanotechnology, Biology and Medicine
Volume 6, Issue 5 , Pages 634-641 , October 2010

Article Tools

* Image Usage & Resolution