Virus-based nanomaterials as positron emission tomography and magnetic resonance contrast agents: From technology development to translational medicine

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 7, Issue 5, 2015, Pages 708-721

  Shukla, Sourabh ^a   Steinmetz, Nicole F ^a,b  

^a Case Western Reserve University   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGES; BIOCOMPATIBILITY; ELECTRONS; IRON OXIDES; MAGNETIC RESONANCE IMAGING; MEDICAL IMAGING; NANOPARTICLES; NUCLEIC ACIDS; POSITRONS; REAGENTS; RECOMBINANT PROTEINS; REGULATORY COMPLIANCE; SCAFFOLDS (BIOLOGY); STOCHASTIC SYSTEMS; SYNTHESIS (CHEMICAL);

ENABLING TECHNOLOGIES; MAGNETIC RESONANCE CONTRAST AGENTS; POSITRON EMISSION TOMOGRAPHY (PET); POSITRON-EMITTING RADIOISOTOPES; SYNTHETIC NANOPARTICLES; TECHNOLOGY DEVELOPMENT; TRANSLATIONAL MEDICINE; VIRAL NANOPARTICLES;

POSITRON EMISSION TOMOGRAPHY;

COAT PROTEIN; CONTRAST MEDIUM; GADOLINIUM; IRON OXIDE; NANOCAGE; NANOMATERIAL; NUCLEAR MAGNETIC RESONANCE IMAGING AGENT; POSITRON EMISSION TOMOGRAPHY AGENT; PROTEIN VP1; PROTEIN VP4; SUPERPARAMAGNETIC IRON OXIDE; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS; ADENOVIRIDAE; ARTICLE; BACTERIOPHAGE; BIOCOMPATIBILITY; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTRAST ENHANCEMENT; ENTEROBACTERIA PHAGE M13; ENTEROBACTERIA PHAGE P22; ESCHERICHIA COLI; HETEROLOGOUS EXPRESSION; LENTIVIRINAE; MICRO-COMPUTED TOMOGRAPHY; MOLECULAR IMAGING; NANOTECHNOLOGY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PLANT VIRUS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; ROTAVIRUS; SIMIAN VIRUS 40; STATIC ELECTRICITY; VIRUS; VIRUS CAPSID; CHEMISTRY; HUMAN; MEDICAL TECHNOLOGY; PROCEDURES; TRANSLATIONAL RESEARCH;

BIOMEDICAL TECHNOLOGY; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; NANOSTRUCTURES; POSITRON-EMISSION TOMOGRAPHY; TRANSLATIONAL MEDICAL RESEARCH; VIRUSES;

EID: 84937818183     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.1335     Document Type: Article

References (96)

1. Plummer EM, Manchester M. Viral nanoparticles and virus-like particles: platforms for contemporary vaccine design. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2010, 3:174-196.
2. Desai MS, Lee S-W. Protein-based functional nanomaterial design for bioengineering applications. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2015, 7::69-97.
3. Ma Y, Nolte RJ, Cornelissen JJ. Virus-based nanocarriers for drug delivery. Adv Drug Deliv Rev 2012, 64:811-825.
4. Guenther CM, Kuypers BE, Lam MT, Robinson TM, Zhao J, Suh J. Synthetic virology: engineering viruses for gene delivery. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2014, 6:548-558.
5. Robertson KL, Liu JL. Engineered viral nanoparticles for flow cytometry and fluorescence microscopy applications. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2012, 4:511-524.
6. Malik N, Wiwattanapatapee R, Klopsch R, Lorenz K, Frey H, Weener JW, Meijer EW, Paulus W, Duncan R. Dendrimers: relationship between structure and biocompatibility in vitro, and preliminary studies on the biodistribution of 125I-labelled polyamidoamine dendrimers in vivo. J Control Release 2000, 65:133-148.
7. Cheng Y, Zhao L, Li Y, Xu T. Design of biocompatible dendrimers for cancer diagnosis and therapy: current status and future perspectives. Chem Soc Rev 2011, 40:2673-2703.
8. Semmler-Behnke M, Kreyling WG, Lipka J, Fertsch S, Wenk A, Takenaka S, Schmid G, Brandau W. Biodistribution of 1.4- and 18-nm gold particles in rats. Small 2008, 4:2108-2111.
9. Borden M, Sirsi S. Ultrasound imaging: better contrast with vesicles. Nat Nanotechnol 2014, 9:248-249.
10. Hovlid ML, Steinmetz NF, Laufer B, Lau JL, Kuzelka J, Wang Q, Hyypia T, Nemerow GR, Kessler H, Manchester M, et al. Guiding plant virus particles to integrin-displaying cells. Nanoscale 2012, 4:3698-3705.
11. Shukla S, Dickmeis C, Nagarajan AS, Fischer R, Commandeur U, Steinmetz NF. Molecular farming of fluorescent virus-based nanoparticles for optical imaging in plants, human cells and mouse models. Biomater Sci 2014, 2:784-797.
12. Jokerst JV, Lobovkina T, Zare RN, Gambhir SS. Nanoparticle PEGylation for imaging and therapy. Nanomedicine (Lond) 2011, 6:715-728.
13. Veronese FM, Pasut G. PEGylation, successful approach to drug delivery. Drug Discov Today 2005, 10:1451-1458.
14. 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.
15. Harris JM, Chess RB. Effect of PEGylation on pharmaceuticals. Nat Rev Drug Discov 2003, 2:214-221.
16. Roberts MJ, Bentley MD, Harris JM. Chemistry for peptide and protein PEGylation. Adv Drug Deliv Rev 2002, 54:459-476.
17. Wattendorf U, Merkle HP. PEGylation as a tool for the biomedical engineering of surface modified microparticles. J Pharm Sci 2008, 97:4655-4669.
18. Mukherjee S, Pfeifer CM, Johnson JM, Liu J, Zlotnick A. Redirecting the coat protein of a spherical virus to assemble into tubular nanostructures. J Am Chem Soc 2006, 128:2538-2539.
19. Fraenkel-Conrat H, Williams RC. Reconstitution of active tobacco mosaic virus from its inactive protein and nucleic acid components. Proc Natl Acad Sci USA 1955, 41:690-698.
20. Atabekov J, Nikitin N, Arkhipenko M, Chirkov S, Karpova O. Thermal transition of native tobacco mosaic virus and RNA-free viral proteins into spherical nanoparticles. J Gen Virol 2011, 92:453-456.
21. Bruckman MA, Hern S, Jiang K, Flask CA, Yu X, Steinmetz NF. Tobacco mosaic virus rods and spheres as supramolecular high-relaxivity MRI contrast agents. J Mater Chem B Mater Biol Med 2013, 1:1482-1490.
22. Sun J, DuFort C, Daniel MC, Murali A, Chen C, Gopinath K, Stein B, De M, Rotello VM, Holzenburg A, et al. Core-controlled polymorphism in virus-like particles. Proc Natl Acad Sci USA 2007, 104:1354-1359.
23. Biomacromolecules 2012, 13:3990-4001.
24. Lee KL, Hubbard LC, Hern S, Yildiz I, Gratzl M, Steinmetz NF. Shape matters: the diffusion rates of TMV rods and CPMV icosahedrons in a spheroid model of extracellular matrix are distinct. Biomater Sci 2013, 1:581-588.
25. Wen AM, Steinmetz NF. The aspect ratio of nanoparticle assemblies and the spatial arrangement of ligands can be optimized to enhance the targeting of cancer cells. Adv Healthc Mater 2014, 3:1739-1744.
26. Wen AM, Rambhia PH, French RH, Steinmetz NF. Design rules for nanomedical engineering: from physical virology to the applications of virus-based materials in medicine. J Biol Phys 2013, 39:301-325.
27. Bruckman MA, Randolph LN, VanMeter A, Hern S, Shoffstall AJ, Taurog RE, Steinmetz NF. Biodistribution, pharmacokinetics, and blood compatibility of native and PEGylated tobacco mosaic virus nano-rods and -spheres in mice. Virology 2014, 449:163-173.
28. Shukla S, Ablack AL, Wen AM, Lee KL, Lewis JD, Steinmetz NF. Increased tumor homing and tissue penetration of the filamentous plant viral nanoparticle potato virus X. Mol Pharm 2013, 10:33-42.
29. Bruckman MA, Jiang K, Simpson EJ, Randolph LN, Luyt LG, Yu X, Steinmetz NF. Dual-modal magnetic resonance and fluorescence imaging of atherosclerotic plaques in vivo using VCAM-1 targeted tobacco mosaic virus. Nano Lett 2014, 14:1551-1558.
30. Cai S, Vijayan K, Cheng D, Lima EM, Discher DE. Micelles of different morphologies-advantages of worm-like filomicelles of PEO-PCL in paclitaxel delivery. Pharm Res 2007, 24:2099-2109.
31. Chauhan VP, Popovic Z, Chen O, Cui J, Fukumura D, Bawendi MG, Jain RK. Fluorescent nanorods and nanospheres for real-time in vivo probing of nanoparticle shape-dependent tumor penetration. Angew Chem Int Ed Engl 2011, 50:11417-11420.
32. Christian DA, Cai S, Garbuzenko OB, Harada T, Zajac AL, Minko T, Discher DE. Flexible filaments for in vivo imaging and delivery: persistent circulation of filomicelles opens the dosage window for sustained tumor shrinkage. Mol Pharm 2009, 6:1343-1352.
33. Decuzzi P, Godin B, Tanaka T, Lee S-Y, Chiappini C, Liu X, Ferrari M. Size and shape effects in the biodistribution of intravascularly injected particles. J Control Release 2010, 141:320-327.
34. Geng Y, Dalhaimer P, Cai S, Tsai R, Tewari M, Minko T, Discher DE. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol 2007, 2:249-255.
35. Gentile F, Chiappini C, Fine D, Bhavane RC, Peluccio MS, Cheng MM-C, Liu X, Ferrari M, Decuzzi P. The effect of shape on the margination dynamics of non-neutrally buoyant particles in two-dimensional shear flows. J Biomech 2008, 41:2312-2318.
36. Lee S-Y, Ferrari M, Decuzzi P. Shaping nano-/micro-particles for enhanced vascular interaction in laminar flows. Nanotechnology 2009, 20:495101.
37. Hooker JM, O'Neil JP, Romanini DW, Taylor SE, Francis MB. Genome-free viral capsids as carriers for positron emission tomography radiolabels. Mol Imaging Biol 2008, 10:182-191.
38. Farkas ME, Aanei IL, Behrens CR, Tong GJ, Murphy ST, O'Neil JP, Francis MB. PET Imaging and biodistribution of chemically modified bacteriophage MS2. Mol Pharm 2013, 10:69-76.
39. Li Z, Jin Q, Huang C, Dasa S, Chen L, Yap L-P, Liu S, Cai H, Park R, Conti PS. Trackable and targeted phage as positron emission tomography (PET) agent for cancer imaging. Theranostics 2011, 1:371-380.
40. Flexman JA, Cross DJ, Lewellen BL, Miyoshi S, Kim Y, Minoshima S. Magnetically targeted viral envelopes: a PET investigation of initial biodistribution. IEEE Trans Nanobioscience 2008, 7:223-232.
41. Miyoshi S, Flexman JA, Cross DJ, Maravilla KR, Kim Y, Anzai Y, Oshima J, Minoshima S. Transfection of neuroprogenitor cells with iron nanoparticles for magnetic resonance imaging tracking: cell viability, differentiation, and intracellular localization. Mol Imaging Biol 2005, 7:286-295.
42. Brader P, Kelly K, Gang S, Shah JP, Wong RJ, Hricak H, Blasberg RG, Fong Y, Gil Z. Imaging of lumph node micrometastases using an oncolytic herpes virus and [F] FEAU PET. PLoS One 2009, 4:e4789.
43. Brader P, Wong RJ, Horowitz G, Gil Z. Combination of pet imaging with viral vectors for identification of cancer metastases. Adv Drug Deliv Rev 2012, 64:749-755.
44. Caravan P. Strategies for increasing the sensitivity of gadolinium based MRI contrast agents. Chem Soc Rev 2006, 35:512-523.
45. Caravan P, Farrar CT, Frullano L, Uppal R. Influence of molecular parameters and increasing magnetic field strength on relaxivity of gadolinium- and manganese-based T 1contrast agents. Contrast Media Mol Imaging 2009, 4:89-100.
46. Villaraza AJ, Bumb A, Brechbiel MW. Macromolecules, dendrimers, and nanomaterials in magnetic resonance imaging: the interplay between size, function, and pharmacokinetics. Chem Rev 2010, 110:2921-2959.
47. Ho D, Sun X, Sun S. Monodisperse magnetic nanoparticles for theranostic applications. Acc Chem Res 2011, 44:875-882.
48. Huang J, Zhong X, Wang L, Yang L, Mao H. Improving the magnetic resonance imaging contrast and detection methods with engineered magnetic nanoparticles. Theranostics 2012, 2:86-102.
49. Sosnovik DE, Nahrendorf M, Weissleder R. Magnetic nanoparticles for MR imaging: agents, techniques and cardiovascular applications. Basic Res Cardiol 2008, 103:122-130.
50. Colombo M, Carregal-Romero S, Casula MF, Gutiérrez L, Morales MP, Böhm IB, Heverhagen JT, Prosperi D, Parak WJ. Biological applications of magnetic nanoparticles. Chem Soc Rev 2012, 41:4306-4334.
51. Huang X, Stein BD, Cheng H, Malyutin A, Tsvetkova IB, Baxter DV, Remmes NB, Verchot J, Kao C, Bronstein LM, et al. Magnetic virus-like nanoparticles in N. benthamiana plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 2011, 5:4037-4045.
52. Chen W, Cao Y, Liu M, Zhao Q, Huang J, Zhang H, Deng Z, Dai J, Williams DF, Zhang Z. Rotavirus capsid surface protein VP4-coated Fe(3)O(4) nanoparticles as a theranostic platform for cellular imaging and drug delivery. Biomaterials 2012, 33:7895-7902.
53. Enomoto T, Kawano M, Fukuda H, Sawada W, Inoue T, Haw KC, Kita Y, Sakamoto S, Yamaguchi Y, Imai T, et al. Viral protein-coating of magnetic nanoparticles using simian virus 40 VP1. J Biotechnol 2013, 167:8-15.
54. Ghosh D, Lee Y, Thomas S, Kohli AG, Yun DS, Belcher AM, Kelly KA. M13-templated magnetic nanoparticles for targeted in vivo imaging of prostate cancer. Nat Nanotechnol 2012, 7:677-682.
55. Bruckman MA, Yu X, Steinmetz NF. Engineering Gd-loaded nanoparticles to enhance MRI sensitivity via T(1) shortening. Nanotechnology 2013, 24:462001.
56. 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.
57. Allen M, Bulte JW, Liepold L, Basu G, Zywicke HA, Frank JA, Young M, Douglas T. Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents. Magn Reson Med 2005, 54:807-812.
58. Basu G, Allen M, Willits D, Young M, Douglas T. Metal binding to cowpea chlorotic mottle virus using terbium(III) fluorescence. J Biol Inorg Chem 2003, 8:721-725.
59. Liepold L, Anderson S, Willits D, Oltrogge L, Frank JA, Douglas T, Young M. Viral capsids as MRI contrast agents. Magn Reson Med 2007, 58:871-879.
60. Garimella PD, Datta A, Romanini DW, Raymond KN, Francis MB. Multivalent, high-relaxivity MRI contrast agents using rigid cysteine-reactive gadolinium complexes. J Am Chem Soc 2011, 133:14704-14709.
61. Datta A, Hooker JM, Botta M, Francis MB, Aime S, Raymond KN. High relaxivity gadolinium hydroxypyridonate-viral capsid conjugates: nanosized MRI contrast agents 1. J Am Chem Soc 2008, 130:2546-2552.
62. 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.
63. Qazi S, Liepold LO, Abedin MJ, Johnson B, Prevelige P, Frank JA, Douglas T. P22 viral capsids as nanocomposite high-relaxivity MRI contrast agents. Mol Pharm 2013, 10:11-17.
64. Pokorski JK, Breitenkamp K, Liepold LO, Qazi S, Finn MG. Functional virus-based polymer-protein nanoparticles by atom transfer radical polymerization. J Am Chem Soc 2011, 133:9242-9245.
65. Doshi N, Prabhakarpandian B, Rea-Ramsey A, Pant K, Sundaram S, Mitragotri S. Flow and adhesion of drug carriers in blood vessels depend on their shape: a study using model synthetic microvascular networks. J Control Release 2010, 146:196-200.
66. Tan J, Shah S, Thomas A, Ou-Yang HD, Liu Y. The influence of size, shape and vessel geometry on nanoparticle distribution. Microfluid Nanofluidics 2013, 14:77-87.
67. Botta M, Tei L. Relaxivity enhancement in macromolecular and nanosized GdIII-based MRI contrast agents. Eur J Inorg Chem 2012, 2012:1945-1960.
68. van Zijl PC, Yadav NN. Chemical exchange saturation transfer (CEST): what is in a name and what isn't? Magn Reson Med 2011, 65:927-948.
69. Stevens TK, Palaniappan KK, Ramirez RM, Francis MB, Wemmer DE, Pines A. HyperCEST detection of a 129Xe-based contrast agent composed of cryptophane-A molecular cages on a bacteriophage scaffold. Magn Reson Med 2013, 69:1245-1252.
70. Meldrum T, Seim KL, Bajaj VS, Palaniappan KK, Wu W, Francis MB, Wemmer DE, Pines A. A xenon-based molecular sensor assembled on an MS2 viral capsid scaffold. J Am Chem Soc 2010, 132:5936-5937.
71. Palaniappan KK, Ramirez RM, Bajaj VS, Wemmer DE, Pines A, Francis MB. Molecular imaging of cancer cells using a bacteriophage-based 129Xe NMR biosensor. Angew Chem Int Ed Engl 2013, 52:4849-4853.
72. Carrico ZM, Farkas ME, Zhou Y, Hsiao SC, Marks JD, Chokhawala H, Clark DS, Francis MB. N-Terminal labeling of filamentous phage to create cancer marker imaging agents. ACS Nano 2012, 6:6675-6680.
73. Singh P, Prasuhn D, Yeh RM, Destito G, Rae CS, Osborn K, Finn MG, Manchester M. Bio-distribution, toxicity and pathology of cowpea mosaic virus nanoparticles in vivo. J Control Release 2007, 120:41-50.
74. Luckanagul JA, Lee LA, You S, Yang X, Wang Q. Plant virus incorporated hydrogels as scaffolds for tissue engineering possess low immunogenicity in vivo. J Biomed Mater Res A 2014, doi: 10.1002/jbm.a.35227.
75. Shukla S, Wen AM, Ayat NR, Commandeur U, Gopalkrishnan R, Broome AM, Lozada KW, Keri RA, Steinmetz NF. Biodistribution and clearance of a filamentous plant virus in healthy and tumor-bearing mice. Nanomedicine (Lond) 2014, 9:221-235.
76. Rae CS, Khor IW, Wang Q, Destito G, Gonzalez MJ, Singh P, Thomas DM, Estrada MN, Powell E, Finn MG, et al. Systemic trafficking of plant virus nanoparticles in mice via the oral route. Virology 2005, 343:224-235.
77. Tarn D, Ashley CE, Xue M, Carnes EC, Zink JI, Brinker CJ. Mesoporous silica nanoparticle nanocarriers: biofunctionality and biocompatibility. Acc Chem Res 2013, 46:792-801.
78. Jaganathan H, Godin B. Biocompatibility assessment of Si-based nano- and micro-particles. Adv Drug Deliv Rev 2012, 64:1800-1819.
79. Liu Y, Zhao Y, Sun B, Chen C. Understanding the toxicity of carbon nanotubes. Accounts of chemical research. Acc Chem Res 2013, 46:702-713.
80. Grobner T. Gadolinium - a specific trigger for the development of nephrogenic fibrosing dermopathy and nephrogenic systemic fibrosis? Nephrol Dial Transplant 2005, 21:1104-1108.
81. Baiu DC, Brazel CS, Bao Y, Otto M. Interactions of iron oxide nanoparticles with the immune system: challenges and opportunities for their use in nano-oncology. Curr Pharm Des 2013, 19:6606-6621.
82. Kaiser CR, Flenniken ML, Gillitzer E, Harmsen AL, Harmsen AG, Jutila MA, Douglas T, Young MJ. Biodistribution studies of protein cage nanoparticles demonstrate broad tissue distribution and rapid clearance in vivo. Int J Nanomed 2007, 2:715-733.
83. Meng J, Yang M, Jia F, Xu Z, Kong H, Xu H. Immune responses of BALB/c mice to subcutaneously injected multi-walled carbon nanotubes. Nanotoxicology 2011, 5:583-591.
84. Semple SC, Harasym TO, Clow KA, Ansell SM, Klimuk SK, Hope MJ. Immunogenicity and rapid blood clearance of liposomes containing polyethylene glycol-lipid conjugates and nucleic acid. J Pharmacol Exp Ther 2005, 312:1020-1026.
85. Shimizu T, Ishida T, Kiwada H. Transport of PEGylated liposomes from the splenic marginal zone to the follicle in the induction phase of the accelerated blood clearance phenomenon. Immunobiology 2013, 218:725-732.
86. Balique F, Colson P, Barry AO, Nappez C, Ferretti A, Moussawi KA, Ngounga T, Lepidi H, Ghigo E, Mege J-L, et al. Tobacco mosaic virus in the lungs of mice following intra-tracheal inoculation. PLoS One 2013, 8:e54993.
87. Liu R, Vaishnav RA, Roberts AM, Friedland RP. Humans have antibodies against a plant virus: evidence from tobacco mosaic virus. PLoS One 2013, 8:e60621.
88. Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. Minimal "Self" peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 2013, 339:971-975.
89. Gillitzer E, Suci P, Young M, Douglas T. Controlled ligand display on a symmetrical protein-cage architecture through mixed assembly. Small 2006, 2:962-966.
90. Miller RA, Presley AD, Francis MB. Self-assembling light-harvesting systems from synthetically modified tobacco mosaic virus coat proteins. J Am Chem Soc 2007, 129:3104-3109.
91. Douglas T, Young M. Host-guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393:152-155.
92. Ren Y, Wong SM, Lim LY. In vitro-reassembled plant virus-like particles for loading of polyacids. J Gen Virol 2006, 87:2749-2754.
93. Ochoa WF, Chatterji A, Lin T, Johnson JE. Generation and structural analysis of reactive empty particles derived from an icosahedral virus. Chem Biol 2006, 13:771-778.
94. Phelps JP, Dang N, Rasochova L. Inactivation and purification of cowpea mosaic virus-like particles displaying peptide antigens from Bacillus anthracis. J Virol Methods 2007, 141:146-153.
95. Lytle CD, Sagripanti JL. Predicted inactivation of viruses of relevance to biodefense by solar radiation. J Virol 2005, 79:14244-14252.
96. Schneemann A, Young MJ. Viral assembly using heterologous expression systems and cell extracts. Adv Protein Chem 2003, 64:1-36.