Virus-Based Nanoparticles as Versatile Nanomachines

Annual Review of Virology

Volumn 2, Issue , 2015, Pages 379-401

  Koudelka, Kristopher J ^a   Pitek, Andrzej S ^c   Manchester, Marianne ^b   Steinmetz, Nicole F ^c,d  

^a POINT LOMA NAZARENE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c Department of Biomedical Engineering ^*  (United States)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Drug delivery; Imaging; Nanotechnology; Vaccines; Viruses

Indexed keywords

CANCER VACCINE; CONTRAST MEDIUM; DYE; IMMUNOMODULATING AGENT; MOLECULAR SCAFFOLD; NANOCARRIER; NANOPARTICLE; UNCLASSIFIED DRUG; VACCINE; VIRUS BASED NANOPARTICLE; VIRUS VACCINE;

ADDICTION; CANCER IMMUNIZATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; HUMAN; IMMUNIZATION; IMMUNOTHERAPY; NANOENGINEERING; NANOIMAGING; NANOMEDICINE; NANOPHARMACEUTICS; NANOTECHNOLOGY; NEOPLASM; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS; VIRUS INFECTION; ANIMAL; CHEMISTRY; DEVICES; GENETICS; METABOLISM; PROCEDURES;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; NANOPARTICLES; NANOTECHNOLOGY; VIRUSES;

EID: 84969219605     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-100114-055141     Document Type: Review

References (190)

1. Desai N. 2012. Challenges in development of nanoparticle-based therapeutics. AAPS J. 14:282-95
2. Franca R, Zhang XF, Veres T, Yahia L, Sacher E. 2013. Core-shell nanoparticles as prodrugs: possible cytotoxicological and biomedical impacts of batch-to-batch inconsistencies. J. Colloid Interface Sci. 389:292-97
3. Guenther CM, Kuypers BE, Lam MT, Robinson TM, Zhao J, Suh J. 2014. Synthetic virology: engineering viruses for gene delivery. WIRES Nanomed. Nanobiotechnol. 6:548-58
4. Wirth T, Parker N, Ylä-Herttuala S. 2013. History of gene therapy. Gene 525:162-69
5. Ylä-Herttuala S. 2012. Endgame: Glybera finally recommended for approval as the first gene therapy drug in the European Union. Mol. Ther. 20:1831-32
6. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. 2004. UCSF Chimera - A visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-12
7. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. 2007. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2:751-60
8. Steinmetz NF. 2010. Viral nanoparticles as platforms for next-generation therapeutics and imaging devices. Nanomedicine 6:634-41
9. Wang Q, Lin T, Johnson JE, Finn MG. 2002. Natural supramolecular building blocks: cysteine-added mutants of Cowpea mosaic virus. Chem. Biol. 9:813-19
10. Peabody DS. 2003. A viral platform for chemical modification and multivalent display. J. Nanobiotechnol. 1:5
11. Miller RA, Presley AD, Francis MB. 2007. Self-assembling light-harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J. Am. Chem. Soc. 129:3104-9
12. Klem MT, Willits D, Young M, Douglas T. 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
13. Udit AK, Brown S, Baksh MM, Finn MG. 2008. Immobilization of bacteriophage Qβ on metalderivatized surfaces via polyvalent display of hexahistidine tags. J. Inorg. Biochem. 102:2142-46
14. Medintz IL, Sapsford KE, Konnert JH, Chatterji A, Lin T, et al. 2005. Decoration of discretely immobilized cowpea mosaic virus with luminescent quantum dots. Langmuir 21:5501-10
15. Chatterji A, Ochoa WF, Ueno T, Lin T, Johnson JE. 2005. A virus-based nanoblock with tunable electrostatic properties. Nano Lett. 5:597-602
16. Douglas T, Strable E, Willits D. 2002. Protein engineering of a viral cage for constrained material synthesis. Adv. Mater. 14:415-18
17. Plummer EM, Manchester M. 2010. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. WIRES Nanomed. Nanobiotechnol. 3:174-96
18. Yildiz I, Shukla S, Steinmetz NF. 2011. Applications of viral nanoparticles in medicine. Curr. Opin. Biotechnol. 22:901-8
19. Strable E, Prasuhn DE Jr, Udit AK, Brown S, Link AJ, et al. 2008. Unnatural amino acid incorporation into virus-like particles. Bioconjug. Chem. 19:866-75
20. Daniel MC, Tsvetkova IB, Quinkert ZT, Murali A, De M, et al. 2010. Role of surface charge density in nanoparticle-templated assembly of bromovirus protein cages. ACS Nano 4:3853-60
21. Dixit SK, Goicochea NL, Daniel MC, Murali A, Bronstein L, et al. 2006. Quantum dot encapsulation in viral capsids. Nano Lett. 6:1993-99
22. Huang X, Bronstein LM, Retrum J,DufortC,Tsvetkova I, et al. 2007. Self-assembled virus-like particles with magnetic cores. Nano Lett. 7:2407-16
23. Sun J,DuFortC,DanielMC, Murali A, Chen C, et al. 2007. Core-controlled polymorphism in virus-like particles. PNAS 104:1354-59
24. BrownWL, Mastico RA,WuM, Heal KG, Adams CJ, et al. 2002. RNA bacteriophage capsid-mediated drug delivery and epitope presentation. Intervirology 45:371-80
25. Wu M, Brown WL, Stockley PG. 1995. Cell-specific delivery of bacteriophage-encapsidated ricin A chain. Bioconjug. Chem. 6:587-95
26. Pokorski JK, Steinmetz NF. 2011. The art of engineering viral nanoparticles. Mol. Pharm. 8:29-43
27. Wen AM, Shukla S, Saxena P, Aljabali AA, Yildiz I, et al. 2012. Interior engineering of a viral nanoparticle and its tumor homing properties. Biomacromolecules 13:3990-4001
28. 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. 2007:1269-71
29. Yildiz I, Lee KL, Chen K, Shukla S, Steinmetz NF. 2013. Infusion of imaging and therapeuticmolecules into the plant virus-based carrier cowpea mosaic virus: cargo-loading and delivery. J. Control. Release 172:568-78
30. Young M,Willits D, Uchida M, Douglas T. 2008. Plant viruses as biotemplates for materials and their use in nanotechnology. Annu. Rev. Phytopathol. 46:361-84
31. Kovacs EW, Hooker JM, Romanini DW, Holder PG, Berry KE, Francis MB. 2007. Dual-surfacemodified bacteriophageMS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjug. Chem. 18:1140-47
32. Schlick TL, Ding Z, Kovacs EW, Francis MB. 2005. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 127:3718-23
33. Bruckman MA, Kaur G, Lee LA, Xie F, Sepulveda J, et al. 2008. Surface modification of tobacco mosaic virus with "click" chemistry. ChemBioChem 9:519-23
34. Hong V, Presolski SI, Ma C, Finn MG. 2009. Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation. Angew. Chem. Int. Ed. 48:9879-83
35. Steinmetz NF, Hong V, Spoerke ED, Lu P, Breitenkamp K, et al. 2009. Buckyballs meet viral nanoparticles: candidates for biomedicine. J. Am. Chem. Soc. 131:17093-95
36. Steinmetz NF, Mertens ME, Taurog RE, Johnson JE, Commandeur U, et al. 2010. Potato virus X as a novel platform for potential biomedical applications. Nano Lett. 10:305-12
37. Uchida M, Morris DS, Kang S, Jolley CC, Lucon J, et al. 2012. Site-directed coordination chemistry with P22 virus-like particles. Langmuir 28:1998-2006
38. Datta A, Hooker JM, Botta M, Francis MB, Aime S, Raymond KN. 2008. High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosizedMRI contrast agents. J. Am. Chem. Soc. 130:2546-52
39. Hooker JM, Datta A, Botta M, Raymond KN, Francis MB. 2007. Magnetic resonance contrast agents from viral capsid shells: A comparison of exterior and interior cargo strategies. Nano Lett. 7:2207-10
40. Hooker J, O'Neil J, Romanini D, Taylor S, Francis M. 2008. Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol. Imaging Biol. 10:182-91
41. Venter PA, Dirksen A, Thomas D, Manchester M, Dawson PE, Schneemann A. 2011. Multivalent display of proteins on viral nanoparticles using molecular recognition and chemical ligation strategies. Biomacromolecules 12:2293-301
42. Carrico ZM, FarkasME, Zhou Y, Hsiao SC,Marks JD, et al. 2012. N-Terminal labeling of filamentous phage to create cancer marker imaging agents. ACS Nano 6:6675-80
43. Gatto D, Ruedl C, Odermatt B, Bachmann MF. 2004. Rapid response of marginal zone B cells to viral particles. J. Immunol. 173:4308-16
44. Singh P, Prasuhn D, Yeh RM, Destito G, Rae CS, et al. 2007. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J. Control. Release 120:41-50
45. Srivastava AS, Kaido T, Carrier E. 2004. Immunological factors that affect the in vivo fate of T7 phage in the mouse. J. Virol. Methods 115:99-104
46. Kwon OJ, Kang E, Choi JW, Kim SW, Yun CO. 2013. Therapeutic targeting of chitosan-PEG-folatecomplexed oncolytic adenovirus for active and systemic cancer gene therapy. J. Control. Release 169:257-65
47. Pasut G, Veronese FM. 2009. PEG conjugates in clinical development or use as anticancer agents: An overview. Adv. Drug Deliv. Rev. 61:1177-88
48. Tesfay MZ, Kirk AC, Hadac EM, Griesmann GE, Federspiel MJ, et al. 2013. PEGylation of vesicular stomatitis virus extends virus persistence in blood circulation of passively immunized mice. J. Virol. 87:3752-59
49. Zeng Q, WenH,Wen Q, Chen X, Wang Y, et al. 2013. Cucumber mosaic virus as drug delivery vehicle for doxorubicin. Biomaterials 34:4632-42
50. Galaway FA, Stockley PG. 2013. MS2 viruslike particles: A robust, semisynthetic targeted drug delivery platform. Mol. Pharm. 10:59-68
51. Huang RK, Steinmetz NF, Fu CY, Manchester M, Johnson JE. 2011. Transferrin-mediated targeting of bacteriophage HK97 nanoparticles into tumor cells. Nanomedicine 6:55-68
52. Chariou PL, Lee KL, Wen AM, Gulati NM, Stewart PL, Steinmetz NF. 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
53. Pokorski JK, Hovlid ML, Finn MG. 2011. Cell targeting with hybrid Qβvirus-like particles displaying epidermal growth factor. ChemBioChem 12:2441-47
54. Hovlid ML, Steinmetz NF, Laufer B, Lau JL, Kuzelka J, et al. 2012. Guiding plant virus particles to integrin-displaying cells. Nanoscale 4:3698-705
55. 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
56. Wen AM, Wang Y, Jiang K, Hsu GC, Gao H, et al. 2015. Shaping bio-inspired nanotechnologies to target thrombosis for dual optical-magnetic resonance imaging. J. Mater. Chem. B 3:6037-45
57. Shukla S, Eber FJ, Nagarajan AS, DiFranco NA, Schmidt N, 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
58. Cao J, Guenther RH, Sit TL, Opperman CH, Lommel SA, Willoughby JA. 2014. Loading and release mechanism of Red clover necrotic mosaic virus derived plant viral nanoparticles for drug delivery of doxorubicin. Small 10:5126-36
59. Choi KM, Kim K, Kwon IC, Kim IS, Ahn HJ. 2012. Systemic delivery of siRNA by chimeric capsid protein: tumor targeting and RNAi activity in vivo. Mol. Pharm. 10:18-25
60. Azizgolshani O, Garmann RF, Cadena-Nava R, Knobler CM, Gelbart WM. 2013. Reconstituted plant viral capsids can release genes to mammalian cells. Virology 441:12-17
61. Aljabali AA, Shukla S, Lomonossoff GP, Steinmetz NF, Evans DJ. 2013. CPMV-DOX delivers. Mol. Pharm. 10:3-10
62. Ren Y,Wong SM, Lim LY. 2007. Folic acid-conjugated protein cages of a plant virus: A novel delivery platform for doxorubicin. Bioconjug. Chem. 18:836-43
63. Pokorski JK, Breitenkamp K, Liepold LO, Qazi S, Finn MG. 2011. Functional virus-based polymerprotein nanoparticles by atom transfer radical polymerization. J. Am. Chem. Soc. 133:9242-45
64. Hovlid ML, Lau JL, Breitenkamp K, Higginson CJ, Laufer B, et al. 2014. Encapsidated atom-transfer radical polymerization in Qβvirus-like nanoparticles. ACS Nano 8:8003-14
65. Rhee JK, Baksh M, Nycholat C, Paulson JC, Kitagishi H, Finn MG. 2012. Glycan-targeted virus-like nanoparticles for photodynamic therapy. Biomacromolecules 13:2333-38
66. Milĺan JG, Brasch M, Anaya-Plaza E, de la Escosura A, Velders AH, et al. 2014. Self-assembly triggered by self-assembly: optically active, paramagnetic micelles encapsulated in protein cage nanoparticles. J. Inorg. Biochem. 136:140-46
67. Everts M, Saini V, Leddon JL, Kok RJ, Stoff-Khalili M, et al. 2006. Covalently linked Au nanoparticles to a viral vector: potential for combined photothermal and gene cancer therapy. Nano Lett. 6:587-91
68. Greenwood B, Salisbury D,Hill AV. 2011. Vaccines and global health. Philos. Trans. R. Soc. B 366:2733-42
69. Levine MM, Robins-Browne R. 2009. Vaccines, global health and social equity. Immunol. Cell Biol. 87:274-78
70. McElrath MJ,Walker BD. 2012. Is an HIV vaccine possible? JAIDS 60(Suppl. 2):S41-43
71. Ottenhoff TH, Kaufmann SH. 2012. Vaccines against tuberculosis:Where are we and where do we need to go? PLOS Pathog. 8:e1002607
72. Thera MA, Plowe CV. 2012. Vaccines for malaria: How close are we? Annu. Rev. Med. 63:345-57
73. Chackerian B, Rangel M, Hunter Z, Peabody DS. 2006. Virus and virus-like particle-based immunogens for Alzheimer's disease induce antibody responses against amyloid-βwithout concomitant T cell responses. Vaccine 24:6321-31
74. Kushnir N, Streatfield SJ, Yusibov V. 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
75. Miermont A, Barnhill H, Strable E, Lu X,Wall KA, et al. 2008. Cowpea mosaic virus capsid: A promising carrier for the development of carbohydrate based antitumor vaccines. Chemistry 14:4939-47
76. Yin Z, Nguyen HG, Chowdhury S, Bentley P, Bruckman MA, et al. 2012. Tobacco mosaic virus as a new carrier for tumor associated carbohydrate antigens. Bioconjug. Chem. 23:1694-703
77. ParmianiG, Russo V, Maccalli C, ParoliniD, Rizzo N, Maio M. 2014. Peptide-based vaccines for cancer therapy. Hum. Vaccines Immunother. 10:3175-78
78. Geynisman D, Chien CR, Smieliauskas F, Shen C, Tina Shih YC. 2014. Economic evaluation of therapeutic cancer vaccines and immunotherapy: A systematic review. Hum. Vaccines Immunother. 10:3415-24
79. Tagliamonte M, Petrizzo A, Tornesello ML, Buonaguro FM, Buonaguro L. 2014. Antigen-specific vaccines for cancer treatment. Hum. Vaccines Immunother. 10:3332-46
80. Winter H, Fox BA, Ruttinger D. 2014. Future of cancer vaccines. Methods Mol. Biol. 1139:555-64
81. Garcea RL, Gissmann L. 2004. Virus-like particles as vaccines and vessels for the delivery of small molecules. Curr. Opin. Biotechnol. 15:513-17
82. Grgacic EV, Anderson DA. 2006. Virus-like particles: passport to immune recognition. Methods 40:60-65
83. Ludwig C, Wagner R. 2007. Virus-like particles-universal molecular toolboxes. Curr. Opin. Biotechnol. 18:537-45
84. Folb PI,Bernatowska E, Chen R, Clemens J,Dodoo AN, et al. 2004.Aglobal perspective on vaccine safety and public health: The Global Advisory Committee on Vaccine Safety. Am. J. Public Health 94:1926-31
85. Kelso JM. 2012. Safety of influenza vaccines. Curr. Opin. Allergy Clin. Immunol. 12:383-88
86. Tozzi AE, Asturias EJ, BalakrishnanMR, Halsey NA, Law B, Zuber PL. 2013. Assessment of causality of individual adverse events following immunization (AEFI): AWHOtool for global use. Vaccine 44:5041-46
87. Klinman DM, Takeno M, Ichino M, Gu M, Yamshchikov G, et al. 1997. DNA vaccines: safety and efficacy issues. Springer Semin. Immunopathol. 19:245-56
88. Aguilar JC, Rodriguez EG. 2007. Vaccine adjuvants revisited. Vaccine 25:3752-62
89. Awate S, Babiuk LA, Mutwiri G. 2013. Mechanisms of action of adjuvants. Front. Immunol. 4:114
90. Bramwell VW, Perrie Y. 2005. The rational design of vaccines. Drug Discov. Today 10:1527-34
91. Leleux J, Roy K. 2013. Micro and nanoparticle-based delivery systems for vaccine immunotherapy: An immunological and materials perspective. Adv. Healthc. Mater. 2:72-94
92. De Temmerman ML, Rejman J, Demeester J, Irvine DJ, Gander B, De Smedt SC. 2011. Particulate vaccines: on the quest for optimal delivery and immune response. Drug Discov. Today 16:569-82
93. Banchereau J, Steinman RM. 1998. Dendritic cells and the control of immunity. Nature 392:245-52
94. Neefjes J, Jongsma ML, Paul P, Bakke O. 2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11:823-36
95. Vyas JM, Van der Veen AG, Ploegh HL. 2008. The known unknowns of antigen processing and presentation. Nat. Rev. Immunol. 8:607-18
96. Pushko P, Pumpens P, Grens E. 2013. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology 56:141-65
97. Roldao A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM. 2010. Virus-like particles in vaccine development. Expert Rev. Vaccines 9:1149-76
98. Chan JK, Berek JS. 2007. Impact of the human papilloma vaccine on cervical cancer. J. Clin. Oncol. 25:2975-82
99. Sominskaya I, Skrastina D, Dislers A, Vasiljev D, Mihailova M, et al. 2010. Construction and immunological evaluation ofmultivalent hepatitis B virus (HBV) core virus-like particles carryingHBV andHCV epitopes. Clin. Vaccine Immunol. 17:1027-33
100. Cheong WS, Reiseger J, Turner SJ, Boyd R, Netter HJ. 2009. Chimeric virus-like particles for the delivery of an inserted conserved influenza A-specific CTL epitope. Antiviral Res. 81:113-22
101. Brennan FR, Gilleland LB, Staczek J, Bendig MM, Hamilton WD, Gilleland HE Jr. 1999. A chimaeric plant virus vaccine protects mice against a bacterial infection. Microbiology 145:2061-67
102. Brennan K, McSherry EA, Hudson L, Kay EW, Hill AD, 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
103. Koo M, Bendahmane M, Lettieri GA, Paoletti AD, Lane TE, 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
104. Nuzzaci M, Piazzolla G, Vitti A, Lapelosa M, Tortorella C, et al. 2007. Cucumber mosaic virus as a presentation system for a double hepatitis C virus-derived epitope. Arch. Virol. 152:915-28
105. Rennermalm A, Li YH, Bohaufs L, Jarstrand C, Brauner A, et al. 2001. Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat. Vaccine 19:3376-83
106. WuL, Jiang L, Zhou Z, Fan J, ZhangQ, et al. 2003. Expression of foot-and-mouth disease virus epitopes in tobacco by a tobacco mosaic virus-based vector. Vaccine 21:4390-98
107. Yusibov V, Mett V, Mett V, Davidson C, Musiychuk K, et al. 2005. Peptide-based candidate vaccine against respiratory syncytial virus. Vaccine 23:2261-65
108. Caldeira JdC, Medford A, Kines RC, Lino CA, Schiller JT, 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
109. Richert LE, Rynda-Apple A, Harmsen AL, Han S, Wiley JA, 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
110. Manayani DJ, Thomas D, Dryden KA, Reddy V, Siladi ME, et al. 2007. A viral nanoparticle with dual function as an anthrax antitoxin and vaccine. PLOS Pathog. 3:1422-31
111. Bhatia BD, Chug S, Narang P, Singh MN. 1988. Bacterial flora of newborns at birth and 72 hours of age. Indian Pediatr. 25:1058-65
112. Schiller JT, LowyDR. 2001. Papillomavirus-like particle vaccines. J. Natl. Cancer Inst. Monogr. 2000:50-54
113. SkrastinaD, Petrovskis I, Petraityte R, Sominskaya I, Ose V, 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
114. Schneemann A, Speir JA, Tan GS, Khayat R, Ekiert DC, 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
115. Rynda-Apple A, Patterson DP, Douglas T. 2014. Virus-like particles as antigenic nanomaterials for inducing protective immune responses in the lung. Nanomedicine 9:1857-68
116. Yaddanapudi K, Mitchell RA, Eaton JW. 2013. Cancer vaccines: looking to the future. Oncoimmunology 2:e23403
117. Ryan SO, Turner MS, Gariepy J, Finn OJ. 2010. Tumor antigen epitopes interpreted by the immune system as self or abnormal-self differentially affect cancer vaccine responses. Cancer Res. 70:5788-96
118. Rosenberg SA. 2000. The identification of cancer antigens: impact on the development of cancer vaccines. Cancer J. 6(Suppl. 2):S142-49
119. Shukla S, Wen AM, Commandeur U, Steinmetz NF. 2014. Presentation of HER2 epitopes using a filamentous plant virus-based vaccination platform. J. Mater. Chem. B 2:6249-58
120. Chackerian B. 2010. Virus-like particle based vaccines for Alzheimer disease. Hum. Vaccines 6:926-30
121. Jin H, Wang W, Zhao S, Yang W, Qian Y, 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
122. Feng G, Wang W, Qian Y, Jin H. 2013. Anti-Aβ antibodies induced by Aβ-HBc virus-like particles prevent Aβaggregation and protect PC12 cells against toxicity of Aβ1-40. J. Neurosci.Methods 218:48-54
123. Maurer P, Jennings GT, Willers J, Rohner F, Lindman Y, et al. 2005. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and phase I safety and immunogenicity. Eur. J. Immunol. 35:2031-40
124. Cornuz J, Zwahlen S, Jungi WF, Osterwalder J, Klingler K, et al. 2008. A vaccine against nicotine for smoking cessation: A randomized controlled trial. PLOS ONE 3:e2547
125. Robertson KL, Liu JL. 2012. Engineered viral nanoparticles for flow cytometry and fluorescence microscopy applications. WIRES Nanomed. Nanobiotechnol. 4:511-24
126. KoudelkaKJ, Manchester M. 2010. Chemically modified viruses: principles and applications. Curr. Opin. Chem. Biol. 14:810-17
127. Schoonen L, van Hest JC. 2014. Functionalization of protein-based nanocages for drug delivery applications. Nanoscale 6:7124-41
128. Ghosh D, Kohli AG, Moser F, Endy D, Belcher AM. 2012. Refactored M13 bacteriophage as a platform for tumor cell imaging and drug delivery. ACS Synth. Biol. 1:576-82
129. Shukla S, Dickmeis C, Nagarajan AS, Fischer R, Commandeur U, Steinmetz NF. 2014. Molecular farming of fluorescent virus-based nanoparticles for optical imaging in plants, human cells and mouse models. Biomater. Sci. 2:784-97
130. Koudelka KJ, Ippoliti S, Medina E, Shriver LP, Trauger SA, et al. 2013. Lysine addressability and mammalian cell interactions of bacteriophage λ procapsids. Biomacromolecules 14:4169-76
131. Chang JR, Song EH, Nakatani-Webster E, Monkkonen L, Ratner DM, Catalano CE. 2014. Phage lambda capsids as tunable display nanoparticles. Biomacromolecules 15:4410-19
132. Tsvetkova IB, Cheng F, Ma Z, Moore AW, Howard B, 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
133. Cheng F, Tsvetkova IB, Khuong YL, Moore AW, Arnold RJ, et al. 2012. The packaging of different cargo into enveloped viral nanoparticles. Mol. Pharm. 10:51-58
134. Jin HE, Farr R, Lee SW. 2014. Collagen mimetic peptide engineered M13 bacteriophage for collagen targeting and imaging in cancer. Biomaterials 33:9236-45
135. Grove J. 2014. Super-resolution microscopy: A virus' eye view of the cell. Viruses 6:1365-78
136. Obermeyer AC, Capehart SL, Jarman JB, Francis MB. 2014. Multivalent viral capsids with internal cargo for fibrin imaging. PLOS ONE 9:e100678
137. Jung B, Rao AL, Anvari B. 2011. Optical nano-constructs composed of genome-depleted brome mosaic virus dopedwith a near infrared chromophore for potential biomedical applications. ACSNano 5:1243-52
138. Jung B, Anvari B. 2013. Virus-mimicking optical nanomaterials: near infrared absorption and fluorescence characteristics and physical stability in biological environments. ACS Appl. Mater. Interfaces 5:7492-500
139. Leeuw TK, Reith RM, Simonette RA, Harden ME, Cherukuri P, et al. 2007. Single-walled carbon nanotubes in the intact organism: near-IR imaging and biocompatibility studies in Drosophila. Nano Lett. 7:2650-54
140. Yi H, Ghosh D, Ham MH, Qi J, Barone PW, 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
141. Ghosh D, Bagley AF, Na YJ, Birrer MJ, Bhatia SN, Belcher AM. 2014. Deep, noninvasive imaging and surgical guidance of submillimeter tumors using targetedM13-stabilized single-walled carbon nanotubes. PNAS 111:13948-53
142. Qazi S, Liepold LO, Abedin MJ, Johnson B, Prevelige P, et al. 2013. P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. Mol. Pharm. 10:11-17
143. Min J, Jung H, Shin HH, 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 14:2332-39
144. Qazi S, Uchida M, Usselman R, Shearer R, Edwards E, Douglas T. 2014. Manganese(III) porphyrins complexed with P22 virus-like particles as T1-enhanced contrast agents formagnetic resonance imaging. J. Biol. Inorg. Chem. 19:237-46
145. 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 1:1482-90
146. Bruckman MA, Jiang K, Simpson EJ, Randolph LN, Luyt LG, 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
147. Ghosh D, Lee Y, Thomas S, Kohli AG, Yun DS, et al. 2012. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat. Nanotechnol. 7:677-82
148. Huang X, Stein BD, Cheng H, Malyutin A, Tsvetkova IB, 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
149. Meldrum T, Seim KL, Bajaj VS, Palaniappan KK, Wu W, et al. 2010. A xenon-based molecular sensor assembled on an MS2 viral capsid scaffold. J. Am. Chem. Soc. 132:5936-37
150. 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. Int. Ed. 52:4849-53
151. Farkas ME, Aanei IL, Behrens CR, Tong GJ, Murphy ST, et al. 2013. PET imaging and biodistribution of chemically modified bacteriophage MS2. Mol. Pharm. 10:69-76
152. 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. 128:2538-39
153. Bruckman MA, VanMeter A, Steinmetz NF. 2015. Nanomanufacturing of tobacco mosaic virus-based spherical biomaterials using a continuous flow method. ACS Biomater. Sci. Eng. 1:13-18
154. Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T. 2012. Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8:10158-66
155. Carette N, Engelkamp H, Akpa E, Pierre SJ, Cameron NR, et al. 2007. A virus-based biocatalyst. Nat. Nanotechnol. 2:226-29
156. Guo P, Lee TJ. 2007. Viral nanomotors for packaging of dsDNA and dsRNA. Mol. Microbiol. 64:886-903
157. Schneemann A, YoungMJ. 2003. Viral assembly using heterologous expression systems and cell extracts. Adv. Protein Chem. 64:1-36
158. Gillitzer E, Suci P, YoungM,Douglas T. 2006. Controlled ligand display on a symmetrical protein-cage architecture through mixed assembly. Small 2:962-66
159. Douglas T, Young M. 1998. Host-guest encapsulation of materials by assembled virus protein cages. Nature 393:152-55
160. Ren Y,Wong SM, Lim LY. 2006. In vitro-reassembled plant virus-like particles for loading of polyacids. J. Gen. Virol. 87:2749-54
161. Phelps JP,DangN,Rasochova L. 2007. Inactivation and purification of cowpeamosaic virus-like particles displaying peptide antigens from Bacillus anthracis. J. Virol. Methods 141:146-53
162. Lytle CD, Sagripanti JL. 2005. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J. Virol. 79:14244-52
163. Bruckman MA, Randolph LN, Vanmeter A, Hern S, Shoffstall AJ, 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
164. Kaiser CR, Flenniken ML, Gillitzer E, Harmsen AL, Harmsen AG, et al. 2007. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int. J. Nanomed. 2:715-33
165. Ruggiero A, Villa CH, Bander E, Rey DA, BergkvistM, et al. 2010. Paradoxical glomerular filtration of carbon nanotubes. PNAS 107:12369-74
166. Singh R, Pantarotto D, Lacerda L, Pastorin G, Klumpp C, et al. 2006. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. PNAS 103:3357-62
167. Lee KL, Shukla S,Wu M, Ayat NR, El Sanadi CE, 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
168. Semmler-BehnkeM, KreylingWG, Lipka J, Fertsch S, Wenk A, et al. 2008. Biodistribution of 1.4-and 18-nm gold particles in rats. Small 4:2108-11
169. Tarn D, Ashley CE, Xue M, Carnes EC, Zink JI, Brinker CJ. 2013. Mesoporous silica nanoparticle nanocarriers: biofunctionality and biocompatibility. Acc. Chem. Res. 46:792-801
170. Jaganathan H, Godin B. 2012. Biocompatibility assessment of Si-based nano-and micro-particles. Adv. Drug Deliv. Rev. 64:1800-19
171. Liu Y, Zhao Y, Sun B, Chen C. 2013. Understanding the toxicity of carbon nanotubes. Acc. Chem. Res. 46:702-13
172. Shukla S, Wen AM, Ayat NR, Commandeur U, Gopalkrishnan R, et al. 2014. Biodistribution and clearance of a filamentous plant virus in healthy and tumor-bearing mice. Nanomedicine 9:221-35
173. Rae CS, Khor IW, Wang Q, Destito G, Gonzalez MJ, et al. 2005. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 343:224-35
174. Baiu DC, Brazel CS, Bao Y, Otto M. 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
175. Meng J, Yang M, Jia F,XuZ,KongH,XuH. 2011. Immune responses of BALB/cmice to subcutaneously injected multi-walled carbon nanotubes. Nanotoxicology 5:583-91
176. Raja KS, Wang Q, Gonzalez MJ, Manchester M, Johnson JE, Finn MG. 2003. Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus. Biomacromolecules 4:472-76
177. Semple SC, Harasym TO, Clow KA, Ansell SM, Klimuk SK, Hope MJ. 2005. Immunogenicity and rapid blood clearance of liposomes containing polyethylene glycol-lipid conjugates and nucleic acid. J. Pharmacol. Exp. Ther. 312:1020-26
178. Shimizu T, Ishida T, Kiwada H. 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
179. Harris JM, Chess RB. 2003. Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2:214-21
180. Roberts MJ, Bentley MD, Harris JM. 2002. Chemistry for peptide and protein PEGylation. Adv. Drug Deliv. Rev. 54:459-76
181. WattendorfU,MerkleHP. 2008. PEGylation as a tool for the biomedical engineering of surface modified microparticles. J. Pharm. Sci. 97:4655-69
182. Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. 2013. Minimal "self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 339:971-75
183. Agrawal A, Manchester M. 2012. Differential uptake of chemically modified cowpea mosaic virus nanoparticles in macrophage subpopulations present in inflammatory and tumor microenvironments. Biomacromolecules 13:3320-26
184. Plummer EM, Manchester M. 2013. Endocytic uptake pathways utilized by CPMV nanoparticles. Mol. Pharm. 10:26-32
185. Plummer EM, Thomas D, Destito G, Shriver LP, Manchester M. 2012. Interaction of cowpea mosaic virus nanoparticles with surface vimentin and inflammatory cells in atherosclerotic lesions. Nanomedicine 7:877-88
186. Shriver LP, Koudelka KJ, Manchester M. 2009. Viral nanoparticles associate with regions of inflammation and blood brain barrier disruption during CNS infection. J. Neuroimmunol. 211:66-72
187. Steinmetz NF, Cho CF, Ablack A, Lewis JD, Manchester M. 2011. Cowpea mosaic virus nanoparticles target surface vimentin on cancer cells. Nanomedicine 6:351-64
188. Steinmetz NF, Maurer J, Sheng H, Bensussan A, Maricic I, 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
189. Koudelka KJ, Destito G, Plummer EM, Trauger SA, Siuzdak G, Manchester M. 2009. Endothelial targeting of cowpea mosaic virus (CPMV) via surface vimentin. PLOS Pathog. 5:e1000417
190. DesaiMS, Lee SW. 2014. Protein-based functional nanomaterial design for bioengineering applications. WIRES Nanomed. Nanobiotechnol. 7:69-97