Applications of viral nanoparticles in medicine

Current Opinion in Biotechnology

Volumn 22, Issue 6, 2011, Pages 901-908

  Yildiz, Ibrahim ^a   Shukla, Sourabh ^a   Steinmetz, Nicole F ^a  

^a Case Western Reserve University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMEDICAL APPLICATIONS; ENGINEERING PRINCIPLES; NATURALLY OCCURRING; PARTICLE SURFACE; PEPTIDE LIGAND; SYNTHETIC MATERIALS; VIRAL NANOPARTICLES; VIRUS-LIKE PARTICLES;

MEDICAL APPLICATIONS; VIRUSES;

NANOPARTICLES;

BACULOVIRUS VECTOR; BIOMATERIAL; CHIMERIC PROTEIN; CHLORAMPHENICOL; COAT PROTEIN; CYTOTOXIC AGENT; DOXORUBICIN; FLUORINE 18; FLUOROBENZALDEHYDE F 18; FULLERENE; GADOLINIUM; HERPESVIRUS VECTOR; HYGROMYCIN; LENTIVIRUS VECTOR; MACROGOL; NANOMATERIAL; NANOPARTICLE; PACLITAXEL; PARVOVIRUS VECTOR; PORPHYRIN DERIVATIVE; RADIOPHARMACEUTICAL AGENT; RUTHENIUM; UNCLASSIFIED DRUG; VIRAL NANOPARTICLE; VIROSOME; VIRUS LIKE PARTICLE VACCINE;

BACTERIAL INFECTION; BACTERIOPHAGE; BACULOVIRUS EXPRESSION SYSTEM; CANCER INHIBITION; CHEMICAL ENGINEERING; DRUG TARGETING; GENETIC ENGINEERING; HUMAN; LEUKEMIA; MOSAIC VIRUS; NANOBIOTECHNOLOGY; NANOENCAPSULATION; NANOENGINEERING; NANOIMAGING; NANOMEDICINE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSICAL CHEMISTRY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SIMIAN VIRUS 40; TOBACCO MOSAIC VIRUS; VIRAL GENE DELIVERY SYSTEM; VIRUS LIKE AGENT;

DIAGNOSTIC IMAGING; GENETIC ENGINEERING; GENETIC VECTORS; MOLECULAR IMAGING; NANOMEDICINE; NANOPARTICLES; VIRION;

EID: 82755187264     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2011.04.020     Document Type: Review

References (77)

1. Resch-Genger U., Grabolle M., Cavaliere-Jaricot S., Nitschke R., Nann T. Quantum dots versus organic dyes as fluorescent labels. Nat Methods 2008, 5:763-775.
2. McNerny D.Q., Leroueil P.R., Baker J.R. Understanding specific and nonspecific toxicities: a requirement for the development of dendrimer-based pharmaceuticals. Wires Nanomed Nanobiol 2010, 2:249-259.
3. Jesorka A., Orwar O. Liposomes: technologies and analytical applications. Annu Rev Anal Chem 2008, 1:801-832.
4. Giljohann D.A., Seferos D.S., Daniel W.L., Massich M.D., Patel P.C., Mirkin C.A. Gold nanoparticles for biology and medicine. Angew Chem Int Ed 2010, 49:3280-3294.
5. Fortin J.P., Wilhelm C., Servais J., Menager C., Bacri J.C., Gazeau F. Size-sorted anionic iron oxide nanomagnets as colloidal mediators for magnetic hyperthermia. J Am Chem Soc 2007, 129:2628-2635.
6. Qiao R.R., Yang C.H., Gao M.Y. Superparamagnetic iron oxide nanoparticles: from preparations to in vivo MRI applications. J Mater Chem 2009, 19:6274-6293.
7. Khemtong C., Kessinger C.W., Gao J.M. Polymeric nanomedicine for cancer MR imaging and drug delivery. Chem Commun 2009, 24:3497-3510.
8. Wagner V., Dullaart A., Bock A.K., Zweck A. The emerging nanomedicine landscape. Nat Biotechnol 2006, 24:1211-1217.
9. Lu J.M., Wang X.W., Marin-Muller C., Wang H., Lin P.H., Yao Q.Z., Chen C.Y. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Rev Mol Diagn 2009, 9:325-341.
10. Peek L.J., Middaugh C.R., Berkland C. Nanotechnology in vaccine delivery. Adv Drug Deliv Rev 2008, 60:915-928.
11. Farrell D., Alper J., Ptak K., Panaro N.J., Grodzinski P., Barker A.D. Recent advances from the National Cancer Institute alliance for nanotechnology in cancer. ACS Nano 2010, 4:589-594.
12. Singh P., Prasuhn D., Yeh R.M., Destito G., Rae C.S., Osborn K., Finn M.G., Manchester M. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J Control Release 2007, 120:41-50.
13. Kaiser C.R., Flenniken M.L., Gillitzer E., Harmsen A.L., Harmsen A.G., Jutila M.A., Douglas T., Young M.J. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int J Nanomed 2007, 2:715-733.
14. Doan D.N., Lee K.C., Laurinmaki P., Butcher S., Wong S.M., Dokland T. Three-dimensional reconstruction of hibiscus chlorotic ringspot virus. J Struct Biol 2003, 144:253-261.
15. Sherman M.B., Guenther R.H., Tama F., Sit T.L., Brooks C.L., Mikhailov A.M., Orlova E.V., Baker T.S., Lommel S.A. Removal of divalent cations induces structural transitions in red clover necrotic mosaic virus, revealing a potential mechanism for RNA release. J Virol 2006, 80:10395-10406.
16. Agirrezabala X., Velázquez-Muriel J.A., Gómez-Puertas P., Scheres S.H.W., Carazo J.M., Carrascosa J.L. Quasi-atomic model of bacteriophage T7 procapsid shell: insights into the structure and evolution of a basic fold. Structure 2007, 15:461-472.
17. Kendall A., McDonald M., Bian W., Bowles T., Baumgarten S.C., Shi J., Stewart P.L., Bullitt E., Gore D., Irving T.C., et al. Structure of flexible filamentous plant viruses. J Virol 2008, 82:9546-9554.
18. Sachse C., Chen J.Z., Coureux P.-D., Stroupe M.E., Fändrich M., Grigorieff N. High-resolution electron microscopy of helical specimens: a fresh look at tobacco mosaic virus. J Mol Biol 2007, 371:812-835.
19. Pokorski J.K., Steinmetz N.F. The art of engineering viral nanoparticles. Mol Pharm 2010.
20. Schneemann A., Young M.J. Viral assembly using heterologous expression systems and cell extracts. Adv Protein Chem 2003, 64.
21. Garnier A., Cote J., Nadeau I., Kamen A., Massie B. Scale-up of the adenovirus expression system for the production of recombinant protein in human 293S cells. Cytotechnology 1994, 15:145-155.
22. Mueller A., Kadri A., Jeske H., Wege C. In vitro assembly of Tobacco mosaic virus coat protein variants derived from fission yeast expression clones or plants. J Virol Methods 2010, 166:77-85.
23. Miller R.A., Presley A.D., Francis M.B. Self-assembling light-harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J Am Chem Soc 2007, 129:3104-3109.
24. Wang Q., Lin T., Johnson J.E., Finn M.G. Natural supramolecular building blocks. Cysteine-added mutants of cowpea mosaic virus. Chem Biol 2002, 9:813-819.
25. Park J.S., Cho M.K., Lee E.J., Ahn K.Y., Lee K.E., Jung J.H., Cho Y., Han S.S., Kim Y.K., Lee J. A highly sensitive and selective diagnostic assay based on virus nanoparticles. Nat Nanotechnol 2009, 4:259-264.
26. Lee J.-H., Kim J.S., Park J.-S., Lee W., Lee K.E., Han S.-S., Lee K.B., Lee J. A three-dimensional and sensitive bioassay based on nanostructured quartz combined with viral nanoparticles. Adv Funct Mater 2010, 20:2004-2009.
27. Ren Y., Wong S.M., Lim L.Y. Folic acid-conjugated protein cages of a plant virus: a novel delivery platform for doxorubicin. Bioconjug Chem 2007, 18:836-843.
28. Sikkema F.D., Comellas-Aragones M., Fokkink R.G., Verduin B.J.M., Cornelissen J.J.L.M., Nolte R.J.M. Monodisperse polymer-virus hybrid nanoparticles. Org Biomol Chem 2007, 5:54-57.
29. Daniel M.C., Tsvetkova I.B., Quinkert Z.T., Murali A., De M., Rotello V.M., Kao C.C., Dragnea B. Role of surface charge density in nanoparticle-templated assembly of bromovirus protein cages. ACS Nano 2010, 4:3853-3860.
30. Ren Y.P., Wong S.M., Lim L.Y. In vitro-reassembled plant virus-like particles for loading of polyacids. J Gen Virol 2006, 87:2749-2754.
31. Hu Y.F., Zandi R., Anavitarte A., Knobler C.M., Gelbart W.M. Packaging of a polymer by a viral capsid: the interplay between polymer length and capsid size. Biophys J 2008, 94:1428-1436.
32. Dixit S.K., Goicochea N.L., Daniel M.C., Murali A., Bronstein L., De M., Stein B., Rotello V.M., Kao C.C., Dragnea B. Quantum dot encapsulation in viral capsids. Nano Lett 2006, 6:1993-1999.
33. Mcaleer W.J., Buynak E.B., Maigetter R.Z., Wampler D.E., Miller W.J., Hilleman M.R. Human hepatitis-B vaccine from recombinant yeast. Nature 1984, 307:178-180.
34. Villa L.L., Costa R.L.R., Petta C.A., Andrade R.P., Ault K.A., Giuliano A.R., Wheeler C.M., Koutsky L.A., Malm C., Lehtinen M., et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. Lancet Oncol 2005, 6:271-278.
35. Martin S.J., Vyakarnam A., Cheingsongpopov R., Callow D., Jones K.L., Senior J.M., Adams S.E., Kingsman A.J., Matear P., Gotch F.M., et al. Immunization of human Hiv-seronegative volunteers with recombinant P17/P24-Ty virus-like particles elicits Hiv-1 P24-specific cellular and humoral immune-responses. AIDS 1993, 7:1315-1323.
36. Pejawar-Gaddy S., Rajawat Y., Hilioti Z., Xue J., Gaddy D.F., Finn O.J., Viscidi R.P., Bossis I. Generation of a tumor vaccine candidate based on conjugation of a MUC1 peptide to polyionic papillomavirus virus-like particles. Cancer Immunol Immun 2010, 59:1685-1696.
37. Edelstein M.L., Abedi M.R., Wixon J., Edelstein R.M. Gene therapy clinical trials worldwide 1989-2004 - an overview. J Gene Med 2004, 6:597-602.
38. Srivastava A.S., Kaido T., Carrier E. Immunological factors that affect the in vivo fate of T7 phage in the mouse. J Virol Methods 2004, 115:99-104.
39. Gatto D., Ruedl C., Odermatt B., Bachmann M.F. Rapid response of marginal zone B cells to viral particles. J Immunol 2004, 173:4308-4316.
40. Plummer E.M., Manchester M. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wires Nanomed Nanobi 2011, 3:174-196.
41. Raja K.S., Wang Q., Gonzalez M.J., Manchester M., Johnson J.E., Finn M.G. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules 2003, 4:472-476.
42. Steinmetz N.F., 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.
43. Lewis J.D., Destito G., Zijlstra A., Gonzalez M.J., Quigley J.P., Manchester M., Stuhlmann H. Viral nanoparticles as tools for intravital vascular imaging. Nat Med 2006, 12:354-360.
44. Ruoslahti E., Bhatia S.N., Sailor M.J. Targeting of drugs and nanoparticles to tumors. J Cell Biol 2010, 188:759-768.
45. Sugahara K.N., Teesalu T., Karmali P.P., Kotamraju V.R., Agemy L., Girard O.M., Hanahan D., Mattrey R.F., Ruoslahti E. Tissue-penetrating delivery of compounds and nanoparticles into tumors. Cancer Cell 2009, 16:510-520.
46. Ruoslahti E. Vascular zip codes in angiogenesis and metastasis. Biochem Soc Trans 2004, 32:397-402.
47. Arap W., Haedicke W., Bernasconi M., Kain R., Rajotte D., Krajewski S., Ellerby H.M., Bredesen D.E., Pasqualini R., Ruoslahti E. Targeting the prostate for destruction through a vascular address. Proc Natl Acad Sci USA 2002, 99:1527-1531.
48. Loo L., Guenther R.H., Lommel S.A., Franzen S. Infusion of dye molecules into Red clover necrotic mosaic virus. Chem Commun 2008, 1:88-90.
49. Acosta-Ramirez E., Perez-Flores R., Majeau N., Pastelin-Palacios R., Gil-Cruz C., Ramirez-Saldana M., Manjarrez-Orduno N., Cervantes-Barragan L., Santos-Argumedo L., Flores-Romo L., et al. Translating innate response into long-lasting antibody response by the intrinsic antigen-adjuvant properties of papaya mosaic virus. Immunology 2008, 124:186-197.
50. Brown W.L., Mastico R.A., Wu M., Heal K.G., Adams C.J., Murray J.B., Simpson J.C., Lord J.M., Taylor-Robinson A.W., Stockley P.G. RNA bacteriophage capsid-mediated drug delivery and epitope presentation. Intervirology 2002, 45:371-380.
51. Huang R.K., Steinmetz N.F., Fu C.Y., Manchester M., Johnson J.E. Transferrin-mediated targeting of bacteriophage HK97 nanoparticles into tumor cells. Nanomedicine (Lond) 2011, 6:55-68.
52. Brunel F.M., Lewis J.D., Destito G., Steinmetz N.F., Manchester M., Stuhlmann H., Dawson P.E. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett 2010, 10:1093-1097.
53. Steinmetz NF, Ablack A, Hickey JL, Ablack J, Manocha B, Mymryk JS, L.G. L, Lewis JD: Intravital imaging of human prostate cancer using viral nanoparticles targeted to gastrin-releasing peptide receptors. Small 2011, doi:10.1002/smll.201000435.
54. 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.
55. Steinmetz N.F., Hong V., Spoerke E.D., Lu P., Breitenkamp K., Finn M.G., Manchester M. Buckyballs meet viral nanoparticles: candidates for biomedicine. J Am Chem Soc 2009, 131:17093-17095.
56. Suci P.A., 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.
57. Stephanopoulos N., Tong G.J., Hsiao S.C., Francis M.B. Dual-surface modified virus capsids for targeted delivery of photodynamic agents to cancer cells. ACS Nano 2010, 4:6014-6020.
58. Waehler R., Russell S.J., Curiel D.T. Engineering targeted viral vectors for gene therapy. Nat Rev Genet 2007, 8:573-587.
59. Tenenbaum L., Lehtonen E., Monahan P.E. Evaluation of risks related to the use of adeno-associated virus-based vectors. Curr Gene Ther 2003, 3:545-565.
60. Wu T.L., Ertl H.C.J. Immune barriers to successful gene therapy. Trends Mol Med 2009, 15:32-39.
61. Wei B., Wei Y.X., Zhang K., Wang J., Xu R.H., Zhan S., Lin G.G., Wang W., Liu M., Wang J.N., et al. Development of an antisense RNA delivery system using conjugates of the MS2 bacteriophage capsids and HIV-1 TAT cell penetrating peptide. Biomed Pharmacother 2009, 63:313-318.
62. Hajitou A., Trepel M., Lilley C.E., Soghomonyan S., Alauddin M.M., Marini F.C., Restel B.H., Ozawa M.G., Moya C.A., Rangel R., et al. A hybrid vector for ligand-directed tumor targeting and molecular imaging. Cell 2006, 125:385-398.
63. Trepel M., Stoneham C.A., Eleftherohorinou H., Mazarakis N.D., Pasqualini R., Arap W., Hajitou A. A heterotypic bystander effect for tumor cell killing after adeno-associated virus/phage-mediated, vascular-targeted suicide gene transfer. Mol Cancer Ther 2009, 8:2383-2391.
64. Singh R., Al-Jamal K.T., Lacerda L., Kostarelos K. Nanoengineering artificial lipid envelopes around adenovirus by self-assembly. ACS Nano 2008, 2:1040-1050.
65. Lai C.Y., Wiethoff C.M., Kickhoefer V.A., Rome L.H., Nemerow G.R. Vault nanoparticles containing an adenovirus-derived membrane lytic protein facilitate toxin and gene transfer. ACS Nano 2009, 3:691-699.
66. Koudelka K.J., Destito G., Plummer E.M., Trauger S.A., Siuzdak G., Manchester M. Endothelial targeting of cowpea mosaic virus (CPMV) via surface vimentin. PLoS Pathog 2009, 5.
67. Leong H.S., Steinmetz N.F., Ablack A., Destito G., Zijlstra A., Stuhlmann H., Manchester M., Lewis J.D. Intravital imaging of embryonic and tumor neovasculature using viral nanoparticles. Nat Protoc 2010, 5:1406-1417.
68. Steinmetz N.F., Cho C.-F., Ablack A., Lewis J.D., Manchester M. Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells. Nanomedicine 2011, 6:351-364.
69. Li F., Zhang Z.P., Peng J., Cui Z.Q., Pang D.W., Li K., Wei H.P., Zhou Y.F., Wen J.K., Zhang X.E. Imaging viral behavior in mammalian cells with self-assembled capsid-quantum-dot hybrid particles. Small 2009, 5:718-726.
70. Jung B., Rao A.L.N., Anvari B. Optical Nano-Constructs Composed of Genome-Depleted Brome Mosaic Virus Doped with a Near Infrared Chromophore for Potential Biomedical Applications. Acs Nano 2011, 5:1243-1252.
71. Datta A., Hooker J.M., Botta M., Francis M.B., Aime S., Raymond K.N. High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosized MRI contrast agents. J Am Chem Soc 2008, 130:2546-2552.
72. Allen M., Bulte J.W.M., Liepold L., Basu G., Zywicke H.A., Frank J.A., Young M., Douglas T. Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents. Magn Reson Med 2005, 54:807-812.
73. Anderson E.A., Isaacman S., Peabody D.S., Wang E.Y., Canary J.W., Kirshenbaum K. Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid. Nano Lett 2006, 6:1160-1164.
74. Prasuhn D.E., Yeh R.M., Obenaus A., Manchester M., Finn M.G. 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.
75. Meldrum T., Seim K.L., Bajaj V.S., Palaniappan K.K., Wu W., Francis M.B., Wemmer D.E., Pines A. A xenon-based molecular sensor assembled on an MS2 viral capsid scaffold. J Am Chem Soc 2010, 132:5936-5937.
76. Hooker J.M., O'Neil J.P., Romanini D.W., Taylor S.E., Francis M.B. Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol Imaging Biol 2008, 10:182-191.
77. Flexman J.A., Cross D.J., Lewellen B.L., Miyoshi S., Kim Y., Minoshima S. Magnetically targeted viral envelopes: a PET investigation of initial biodistribution. IEEE Trans Nanobiosci 2008, 7:223-232.