Plant virus directed fabrication of nanoscale materials and devices

Virology

Volumn 479-480, Issue , 2015, Pages 200-212

  Culver, James N ^a   Brown, Adam D ^a,b   Zang, Faheng ^b   Gnerlich, Markus ^b   Gerasopoulos, Konstantinos ^b   Ghodssi, Reza ^b  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Bio materials; Nanotechnology; Virus assembly; Virus particles; Virus like particles

Indexed keywords

BIOMATERIAL; NANOMATERIAL;

BIOTECHNOLOGY; GENETICS; METABOLISM; PLANT; PLANT VIRUS; PROCEDURES; VIROLOGY;

BIOCOMPATIBLE MATERIALS; BIOTECHNOLOGY; NANOSTRUCTURES; PLANT VIRUSES; PLANTS;

EID: 84933061901     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2015.03.008     Document Type: Review

References (142)

1. Alonso J.M., Gorzny M.L., Bittner A.M. The physics of tobacco mosaic virus and virus-based devices in biotechnology. Trends Biotechnol. 2013, 31:530-538.
2. Alonso J.M., Ondarcuhu T., Bittner A.M. Integration of plant viruses in electron beam lithography nanostructures. Nanotechnology 2013, 24.
3. Balci S., Bittner A.M., Hahn K., Scheu C., Knez M., Kadri A., Wege C., Jeske H., Kern K. Copper nanowires within the central channel of tobacco mosaic virus particles. Electrochim. Acta 2006, 51:6251-6257.
4. Balci S., Leinberger D.M., Knez M., Bittner A.M., Boes F., Kadri A., Wege C., Jeske H., Kern K. Printing and aligning mesoscale patterns of Tobacco mosaic virus on surfaces. Adv. Mater. 2008, 20:2195.
5. Barick K.C., Bahadur D. Self-assembly of colloidal nanoscale particles: fabrication, properties and applications. J. Nanosci. Nanotechnol. 2010, 10:668-689.
6. Basnayake V.R., Sit T.L., Lommel S.A. The Red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology 2009, 384:169-178.
7. Bittner A.M. Electroless deposition approaching the molecular scale. Advanced Nanoscale Ulsi Interconnects: Fundamentals and Applications 2009, 221-235.
8. Blum A.S., Soto C.M., Wilson C.D., Brower T.L., Pollack S.K., Schull T.L., Chatterji A., Lin T.W., Johnson J.E., Amsinck C., Franzon P., Shashidhar R., Ratna B.R. An engineered virus as a scaffold for three-dimensional self-assembly on the nanoscale. Small 2005, 1:702-706.
9. Blum A.S., Soto C.M., Wilson C.D., Cole J.D., Kim M., Gnade B., Chatterji A., Ochoa W.F., Lin T.W., Johnson J.E., Ratna B.R. Cowpea mosaic virus as a scaffold for 3-D patterning of gold nanoparticles. Nano Lett. 2004, 4:867-870.
10. Boukamp B.A., Lesh G.C., Huggins R.A. All-solid lithium electrodes with mixed-conductor matrix. J. Electrochem. Soc. 1981, 128:725-729.
11. Brown A.D., Naves L., Wang X., Ghodssi R., Culver J.N. Carboxylate-directed in vivo assembly of virus-like nanorods and tubes for the display of functional peptides and residues. Biomacromolecules 2013, 14:3123-3129.
12. Browne W.R., Feringa B.L. Making molecular machines work. Nat. Nanotechnol. 2006, 1:25-35.
13. Bruckman M.A., Jiang K., Simpson E.J., Randolph L.N., Luyt L.G., Yu X., Steinmetz N.F. 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.
14. Bruckman M.A., Soto C.M., McDowell H., Liu J.L., Ratna B.R., Korpany K.V., Zahr O.K., Blum A.S. Role of hexahistidine in directed nanoassemblies of tobacco mosaic virus coat protein. ACS Nano 2011, 5:1606-1616.
15. Brumfield S., Willits D., Tang L., Johnson J.E., Douglas T., Young M. Heterologous expression of the modified coat protein of Cowpea chlorotic mottle bromovirus results in the assembly of protein cages with altered architectures and function. J. Gen. Virol. 2004, 85:1049-1053.
16. Butler P.J.G. Self-assembly of tobacco mosaic virus: the role of an intermediate aggregate in generating both specificity and speed. Philos. Trans. R. Soc. B 1999, 354:537-550.
17. Cao J., Guenther R.H., Sit T.L., Opperman C.H., Lommel S.A., Willoughby J.A. Loading and release mechanism of red clover necrotic mosaic virus derived plant viral nanoparticles for drug delivery of doxorubicin. Small 2014.
18. Chan C.K., Peng H.L., Liu G., McIlwrath K., Zhang X.F., Huggins R.A., Cui Y. High-performance lithium battery anodes using silicon nanowires. Nat. Nanotechnol. 2008, 3:31-35.
19. Chapman S., Kavanagh T., Baulcombe D. Potato virus-X as a vector for gene-expression in plants. Plant J. 1992, 2:549-557.
20. Chen X.L., Gerasopoulos K., Guo J.C., Brown A., Ghodssi R., Culver J.N., Wang C.S. High rate performance of virus enabled 3D n-type Si anodes for lithium-ion batteries. Electrochim. Acta 2011, 56:5210-5213.
21. Chen X.L., Gerasopoulos K., Guo J.C., Brown A., Wang C.S., Ghodssi R., Culver J.N. Virus-enabled silicon anode for lithium-ion batteries. ACS Nano 2010, 4:5366-5372.
22. Chen X.L., Gerasopoulos K., Guo J.C., Brown A., Wang C.S., Ghodssi R., Culver J.N. A patterned 3D silicon anode fabricated by electrodeposition on a virus-structured current collector. Adv. Funct. Mater. 2011, 21:380-387.
23. Chen X.L., Guo J.C., Gerasopoulos K., Langrock A., Brown A., Ghodssi R., Culver J.N., Wang C.S. 3D tin anodes prepared by electrodeposition on a virus scaffold. J. Power Sources 2012, 211:129-132.
24. Chiang C.Y., Epstein J., Brown A., Munday J.N., Culver J.N., Ehrman S. Biological templates for antireflective current collectors for photoelectrochemical cell applications. Nano Lett. 2012, 12:6005-6011.
25. Comellas-Aragones M., Engelkamp H., Claessen V.I., Sommerdijk N.A., Rowan A.E., Christianen P.C., Maan J.C., Verduin B.J., Cornelissen J.J., Nolte R.J. A virus-based single-enzyme nanoreactor. Nat. Nanotechnol. 2007, 2:635-639.
26. Correia J.J., Shire S., Yphantis D.A., Schuster T.M. Sedimentation equilibrium measurements of the intermediate-size tobacco mosaic virus protein polymers. Biochemistry 1985, 24:3292-3297.
27. Cruz S.S., Chapman S., Roberts A.G., Roberts I.M., Prior D.A.M., Oparka K.J. Assembly and movement of a plant virus carrying a green fluorescent protein overcoat. Proc. Natl. Acad. Sci. USA 1996, 93:6286-6290.
28. Dawson W.O., Beck D.L., Knorr D.A., Grantham G.L. cDNA cloning of the complete genome of tobacco mosaic virus and production of infectious transcripts. Proc. Natl. Acad. Sci. USA 1986, 83:1832-1836.
29. Dedeo M.T., Duderstadt K.E., Berger J.M., Francis M.B. Nanoscale protein assemblies from a circular permutant of the tobacco mosaic virus. Nano Lett. 2010, 10:181-186.
30. Dedeo M.T., Finley D.T., Francis M.B. Viral capsids as self-assembling templates for new materials. Prog. Mol. Biol. Transl. Sci. 2011, 103:353-392.
31. Douglas T., Strable E., Willits D., Aitouchen A., Libera M., Young M. Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater. 2002, 14:415-418.
32. Douglas T., Young M. Host guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393:152-155.
33. Douglas T., Young M. Virus particles as templates for materials synthesis. Adv. Mater. 1999, 11:679-681.
34. Dujardin E., Peet C., Stubbs G., Culver J.N., Mann S. Organization of metallic nanoparticles using tobacco mosaic virus templates. Nano Lett. 2003, 3:413-417.
35. Durham A., Finch J., Klug A. States of aggregation of tobacco mosaic virus. Nat. New Biol. 1971, 229:37-42.
36. Eber F.J., Eiben S., Jeske H., Wege C. RNA-controlled assembly of tobacco mosaic virus-derived complex structures: from nanoboomerangs to tetrapods. Nanoscale 2015, 7:344-355.
37. Eggen R., Verver J., Wellink J., De Jong A., Goldbach R., van Kammen A. Improvements of the infectivity of in vitro transcripts from cloned cowpea mosaic virus cDNA: impact of terminal nucleotide sequences. Virology 1989, 173:447-455.
38. Endo M., Fujitsuka M., Majima T. Porphyrin light-harvesting arrays constructed in the recombinant tobacco mosaic virus scaffold. Chem.-Eur. J. 2007, 13:8660-8666.
39. Evans D.J. The bionanoscience of plant viruses: templates and synthons for new materials. J. Mater. Chem. 2008, 18:3746-3754.
40. Fan X.Z., Pomerantseva E., Gnerlich M., Brown A., Gerasopoulos K., McCarthy M., Culver J., Ghodssi R. Tobacco mosaic virus: a biological building block for micro/nano/bio systems. J. Vac. Sci. Technol. A 2013, 31.
41. Flynn C.E., Lee S.W., Peelle B.R., Belcher A.M. Viruses as vehicles for growth, organization and assembly of materials. Acta Mater. 2003, 51:5867-5880.
42. Fowler C.E., Shenton W., Stubbs G., Mann S. Tobacco mosaic virus liquid crystals as templates for the interior design of silica mesophases and nanoparticles. Adv. Mater. 2001, 13:1266-1269.
43. Franzen S., Lommel S.A. Targeting cancer with 'smart bombs': equipping plant virus nanoparticles for a 'seek and destroy' mission. Nanomedicine-UK 2009, 4:575-588.
44. Frolova O.Y., Petrunia I.V., Komarova T.V., Kosorukov V.S., Sheval E.V., Gleba Y.Y., Dorokhov Y.L. Trastuzumab-binding peptide display by Tobacco mosaic virus. Virology 2010, 407:7-13.
45. Gerasopoulos K., McCarthy M., Banerjee P., Fan X., Culver J.N., Ghodssi R. Biofabrication methods for the patterned assembly and synthesis of viral nanotemplates. Nanotechnology 2010, 21.
46. Gerasopoulos K., McCarthy M., Royston E., Culver J.N., Ghodssi R. Nanostructured nickel electrodes using the Tobacco mosaic virus for microbattery applications. J. Micromech. Microeng. 2008, 18.
47. Gerasopoulos K., Pomerantseva E., McCarthy M., Brown A., Wang C.S., Culver J., Ghodssi R. Hierarchical three-dimensional microbattery electrodes combining bottom-up self-assembly and top-down micromachining. ACS Nano 2012, 6:6422-6432.
48. Ghosh A., Guo J.C., Brown A.D., Royston E., Wang C.S., Kofinas P., Culver J.N. Virus-assembled flexible electrode-electrolyte interfaces for enhanced polymer-based battery applications. J. Nanomater. 2012, 795892.
49. Holder P.G., Finley D.T., Stephanopoulos N., Walton R., Clark D.S., Francis M.B. Dramatic thermal stability of virus-polymer conjugates in hydrophobic solvents. Langmuir 2010, 26:17383-17388.
50. Honarbakhsh S., Guenther R.H., Willoughby J.A., Lommel S.A., Pourdeyhimi B. Polymeric systems incorporating plant viral nanoparticles for tailored release of therapeutics. Adv. Healthc. Mater. 2013, 2:1001-1007.
51. Hou C.X., Luo Q., Liu J.L., Miao L., Zhang C.Q., Gao Y.Z., Zhang X.Y., Xu J.Y., Dong Z.Y., Liu J.Q. Construction of GPx active centers on natural protein nanodisk/nanotube: a new way to develop artificial nanoenzyme. ACS Nano 2012, 6:8692-8701.
52. Hwang D.J., Roberts I.M., Wilson T.M. Expression of tobacco mosaic virus coat protein and assembly of pseudovirus particles in Escherichia coli. Proc. Natl. Acad. Sci. USA 1994, 91:9067-9071.
53. Jaworski J.W., Raorane D., Huh J.H., Majumdar A., Lee S.W. Evolutionary screening of biomimetic coatings for selective detection of explosives. Langmuir 2008, 24:4938-4943.
54. Jung S., Yi H. An integrated approach for enhanced protein conjugation and capture with viral nanotemplates and hydrogel microparticle platforms via rapid bioorthogonal reactions. Langmuir 2014, 30:7762-7770.
55. Kaur G., Valarmathi M.T., Potts J.D., Jabbari E., Sabo-Attwood T., Wang Q. Regulation of osteogenic differentiation of rat bone marrow stromal cells on 2D nanorod substrates. Biomaterials 2010, 31:1732-1741.
56. Kaur G., Wang C., Sun J.A., Wang Q.A. The synergistic effects of multivalent ligand display and nanotopography on osteogenic differentiation of rat bone marrow stem cells. Biomaterials 2010, 31:5813-5824.
57. Kendall A., Bian W., Maris A., Azzo C., Groom J., Williams D., Shi J., Stewart P.L., Wall J.S., Stubbs G. A common structure for the potexviruses. Virology 2013, 436:173-178.
58. Klem M.T., Young M., Douglas T. Biomimetic magnetic nanoparticles. Mater. Today 2005, 8:28-37.
59. Klug A. The tobacco mosaic virus particle: structure and assembly. Philos. Trans. R. Soc. B 1999, 354:531-535.
60. Knez M., Bittner A.M., Boes F., Wege C., Jeske H., Maiss E., Kern K. Biotemplate synthesis of 3-nm nickel and cobalt nanowires. Nano Lett. 2003, 3:1079-1082.
61. Knez M., Sumser M., Bittner A.M., Wege C., Jeske H., Martin T.P., Kern K. Spatially selective nucleation of metal clusters on the tobacco mosaic virus. Adv. Funct. Mater. 2004, 14:116-124.
62. Kobayashi M., Seki M., Tabata H., Watanabe Y., Yamashita I. Fabrication of aligned magnetic nanoparticles using tobamoviruses. Nano Lett. 2010, 10:773-776.
63. Korten T., Mansson A., Diez S. Towards the application of cytoskeletal motor proteins in molecular detection and diagnostic devices. Curr. Opin. Biotechnol. 2010, 21:477-488.
64. Kostiainen M.A., Hiekkataipale P., Laiho A., Lemieux V., Seitsonen J., Ruokolainen J., Ceci P. Electrostatic assembly of binary nanoparticle superlattices using protein cages. Nat. Nanotechnol. 2013, 8:52. -+.
65. Kumar A., Reddy V.S., Yusibov V., Chipman P.R., Hata Y., Fita I., Fukuyama K., Rossmann M.G., LoeschFries L.S., Baker T.S., Johnson J.E. The structure of alfalfa mosaic virus capsid protein assembled as a T=1 icosahedral particle at 4.0-angstrom resolution. J. Virol. 1997, 71:7911-7916.
66. Lee K.L., Uhde-Holzem K., Fischer R., Commandeur U., Steinmetz N.F. Genetic engineering and chemical conjugation of potato virus X. Virus Hybrids as Nanomaterials: Methods and Protocols 2014, 1108:3-21.
67. Lee S.Y., Choi J., Royston E., Janes D.B., Culver J.N., Harris M.T. Deposition of platinum clusters on surface-modified Tobacco mosaic virus. J. Nanosci. Nanotechnol. 2006, 6:974-981.
68. Lee S.Y., Royston E., Culver J.N., Harris M.T. Improved metal cluster deposition on a genetically engineered tobacco mosaic virus template. Nanotechnology 2005, 16:S435-S441.
69. Li F., Wang Q.B. Fabrication of nanoarchitectures templated by virus-based nanoparticles: strategies and applications. Small 2014, 10:230-245.
70. Lim J.S., Kim S.M., Lee S.Y., Stach E.A., Culver J.N., Harris M.T. Biotemplated aqueous-phase palladium crystallization in the absence of external reducing agents. Nano Lett. 2010, 10:3863-3867.
71. Lin T.W., Chen Z.G., Usha R., Stauffacher C.V., Dai J.B., Schmidt T., Johnson J.E. The refined crystal structure of cowpea mosaic virus at 2.8 angstrom resolution. Virology 1999, 265:20-34.
72. Liu L., Lomonossoff G.P. Agroinfection as a rapid method for propagating Cowpea mosaic virus-based constructs. J. Virol. Methods 2002, 105:343-348.
73. Liu Y., Kim E., Ghodssi R., Rubloff G.W., Culver J.N., Bentley W.E., Payne G.F. Biofabrication to build the biology-device interface. Biofabrication 2010, 2.
74. Liu Z., Qiao J., Niu Z., Wang Q. Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles. Chem. Soc. Rev. 2012, 41:6178-6194.
75. Lomonossoff G.P., Evans D.J. Applications of plant viruses in bionanotechnology. Curr. Top. Microbiol. Immunol. 2014, 375:61-87.
76. Loo L., Guenther R.H., Lommel S.A., Franzen S. Encapsidation of nanoparticles by red clover necrotic mosaic virus. J. Am. Chem. Soc. 2007, 129:11111-11117.
77. Loo L., Guenther R.H., Lommel S.A., Franzen S. Infusion of dye molecules into Red clover necrotic mosaic virus. Chem. Commun. (Camb.) 2008, 88-90.
78. Lu B., Stubbs G., Culver J.N. Carboxylate interactions involved in the disassembly of tobacco mosaic tobamovirus. Virology 1996, 225:11-20.
79. Lu B., Taraporewala Z.F., Stubbs G., Culver J.N. Intersubunit interactions allowing a carboxylate mutant coat protein to inhibit tobamovirus disassembly. Virology 1998, 244:13-19.
80. Manocchi A.K., Seifert S., Lee B., Yi H. In situ small-angle X-ray scattering analysis of palladium nanoparticle growth on tobacco mosaic virus nanotemplates. Langmuir 2011, 27:7052-7058.
81. Martin S.L., Guenther R.H., Sit T.L., Swartz P.D., Meilleur F., Lommel S.A., Rose R.B. Crystallization and preliminary X-ray diffraction analysis of red clover necrotic mosaic virus. Acta Crystallogr. Sect. F Struct. Biol. Crys.t Commun. 2010, 66:1458-1462.
82. McCarthy M., Gerasopoulos K., Enright R., Culver J.N., Ghodssi R., Wang E.N. Biotemplated hierarchical surfaces and the role of dual length scales on the repellency of impacting droplets. Appl. Phys. Lett. 2012, 100.
83. 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.
84. Miller R.A., Stephanopoulos N., McFarland J.M., Rosko A.S., Geissler P.L., Francis M.B. Impact of assembly state on the defect tolerance of TMV-based light harvesting arrays. J. Am. Chem. Soc. 2010, 132:6068-6074.
85. Minten I.J., Claessen V.I., Blank K., Rowan A.E., Nolte R.J.M., Cornelissen J.J.L.M. Catalytic capsids: the art of confinement. Chem. Sci. 2011, 2:358-362.
86. Moen E.L., Godley L.A., Zhang W., Dolan M.E. Pharmacogenomics of chemotherapeutic susceptibility and toxicity. Genome Med. 2012, 4:90.
87. Montague N.P., Thuenemann E.C., Saxena P., Saunders K., Lenzi P., Lomonossoff G.P. Recent advances of cowpea mosaic virus-based particle technology. Hum. Vaccin. 2011, 7:383-390.
88. Mueller A., Eber F.J., Azucena C., Petershans A., Bittner A.M., Gliemann H., Jeske H., Wege C. Inducible site-selective bottom-up assembly of virus-derived nanotube arrays on RNA-equipped wafers. ACS Nano 2011, 5:4512-4520.
89. Namba K., Pattanayek R., Stubbs G. Visualization of protein-nucleic acid interactions in a virus - refined structure of intact tobacco mosaic virus at 2.9 A resolution by X-ray fiber diffraction. J. Mol. Biol. 1989, 208:307-325.
90. Ng B.C., Chan S.T., Lin J., Tolbert S.H. Using polymer conformation to control architecture in semiconducting polymer/viral capsid assemblies. ACS Nano 2011, 5:7730-7738.
91. Niu Z., Bruckman M., Kotakadi V.S., He J., Emrick T., Russell T.P., Yang L., Wang Q. Study and characterization of tobacco mosaic virus head-to-tail assembly assisted by aniline polymerization. Chem. Commun. (Camb.) 2006, 3019-3021.
92. Niu Z., Liu J., Lee L.A., Bruckman M.A., Zhao D., Koley G., Wang Q. Biological templated synthesis of water-soluble conductive polymeric nanowires. Nano Lett. 2007, 7:3729-3733.
93. Niu Z.W., Bruckman M.A., Li S.Q., Lee L.A., Lee B., Pingali S.V., Thiyagarajan P., Wang Q. Assembly of tobacco mosaic virus into fibrous and macroscopic bundled arrays mediated by surface aniline polymerization. Langmuir 2007, 23:6719-6724.
94. Pogue G.P., Lindbo J.A., Garger S.J., Fitzmaurice W.P. Making an ally from an enemy: plant virology and the new agriculture. Annu. Rev. Phytopathol. 2002, 40:45-74.
95. Pokorski J.K., Steinmetz N.F. The art of engineering viral nanoparticles. Mol. Pharm. 2011, 8:29-43.
96. Pomerantseva E., Gerasopoulos K., Chen X.Y., Rubloff G., Ghodssi R. Electrochemical performance of the nanostructured biotemplated V2O5 cathode for lithium-ion batteries. J. Power Sources 2012, 206:282-287.
97. Rahman M.M., Ölçeroğlu E., McCarthy M. Scalable nanomanufacturing of virus-templated coatings for enhanced boiling. Adv. Mater. Interfaces 2014, 1:1300107-1300113.
98. Rong J.H., Niu Z.W., Lee L.A., Wang Q. Self-assembly of viral particles. Curr. Opin. Colloid Interface Sci. 2011, 16:441-450.
99. Rong J.H., Oberbeck F., Wang X.N., Li X.D., Oxsher J., Niu Z.W., Wang Q. Tobacco mosaic virus templated synthesis of one dimensional inorganic-polymer hybrid fibres. J. Mater. Chem. 2009, 19:2841-2845.
100. Rothemund P.W. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440:297-302.
101. Royston E., Ghosh A., Kofinas P., Harris M.T., Culver J.N. Self-assembly of virus-structured high surface area nanomaterials and their application as battery electrodes. Langmuir 2008, 24:906-912.
102. Royston E.S., Brown A.D., Harris M.T., Culver J.N. Preparation of silica stabilized Tobacco mosaic virus templates for the production of metal and layered nanoparticles. J. Colloid Interface Sci. 2009, 332:402-407.
103. Sainsbury F., Canizares M.C., Lomonossoff G.P. Cowpea mosaic virus: the plant virus-based biotechnology workhorse. Annu. Rev. Phytopathol. 2010, 48:437-455.
104. Sainsbury F., Lomonossoff G.P. Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol. 2008, 148:1212-1218.
105. Sanchez-Sanchez L., Cadena-Nava R.D., Palomares L.A., Ruiz-Garcia J., Koay M.S., Cornelissen J.J., Vazquez-Duhalt R. Chemotherapy pro-drug activation by biocatalytic virus-like nanoparticles containing cytochrome P450. Enzyme Microb. Technol. 2014, 60:24-31.
106. Saunders K., Lomonossoff G.P. Exploiting plant virus-derived components to achieve in planta expression and for templates for synthetic biology applications. New Phytol. 2013, 200:16-26.
107. Saunders K., Sainsbury F., Lomonossoff G.P. Efficient generation of cowpea mosaic virus empty virus-like particles by the proteolytic processing of precursors in insect cells and plants. Virology 2009, 393:329-337.
108. Schlick T.L., Ding Z.B., Kovacs E.W., Francis M.B. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 2005, 127:3718-3723.
109. Shenton W., Douglas T., Young M., Stubbs G., Mann S. Inorganic-organic nanotube composites from template mineralization of tobacco mosaic virus. Adv. Mater. 1999, 11:253.
110. 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.
111. Sirotkin S., Mermet A., Bergoin M., Ward V., Van Etten J.L. Viruses as nanoparticles: structure versus collective dynamics. Phys. Rev. E 2014, 90.
112. Sitasuwan P., Lee L.A., Bo P., Davis E.N., Lin Y., Wang Q. A plant virus substrate induces early upregulation of BMP2 for rapid bone formation. Integr. Biol.-UK 2012, 4:651-660.
113. Sitasuwan P., Lee L.A., Li K., Nguyen H.G., Wang Q. RGD-conjugated rod-like viral nanoparticles on 2D scaffold improve bone differentiation of mesenchymal stem cells. Front. Chem. 2014, 2:31.
114. Speir J.A., Munshi S., Wang G., Baker T.S., Johnson J.E. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 1995, 3:63-78.
115. Speir J.A., Munshi S., Wang G.J., Baker T.S., Johnson J.E. Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryoelectron microscopy. Structure 1995, 3:63-78.
116. Steckert J.J., Schuster T.M. Sequence specificity of trinucleoside diphosphate binding to polymerized tobacco mosaic virus protein. Nature 1982, 299:32-36.
117. Steinmetz N.F., Calder G., Lomonossoff G.P., Evans D.J. Plant viral capsids as nanobuilding blocks: construction of arrays on solid supports. Langmuir 2006, 22:10032-10037.
118. Steinmetz N.F., Lin T., Lomonossoff G.P., Johnson J.E. Structure-based engineering of an icosahedral virus for nanomedicine and nanotechnology. Curr. Top. Microbiol. 2009, 327:23-58.
119. Stephanopoulos N., Francis M.B. Choosing an effective protein bioconjugation strategy. Nat. Chem. Biol. 2011, 7:876-884.
120. Stock D., Namba K., Lee L.K. Nanorotors and self-assembling macromolecular machines: the torque ring of the bacterial flagellar motor. Curr. Opin. Biotechnol. 2012, 23:545-554.
121. Strable E., Finn M.G. Chemical modification of viruses and virus-like particles. Curr. Top. Microbiol. 2009, 327:1-21.
122. Suci P.A., Klem M.T., Arce F.T., Douglas T., Young M. Assembly of multilayer films incorporating a viral protein cage architecture. Langmuir 2006, 22:8891-8896.
123. Tama F., Brooks C.L. The mechanism and pathway of pH induced swelling in cowpea chlorotic mottle virus. J. Mol. Biol. 2002, 318:733-747.
124. Tilsner J., Linnik O., Louveaux M., Roberts I.M., Chapman S.N., Oparka K.J. Replication and trafficking of a plant virus are coupled at the entrances of plasmodesmata. J. Cell Biol. 2013, 201:981-995.
125. Turpen T.H. Tobacco mosaic virus and the virescence of biotechnology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1999, 354:665-673.
126. Wang Q., Lin T.W., Tang L., Johnson J.E., Finn M.G. Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. 2002, 41:459-462.
127. Wen A.M., Rambhia P.H., French R.H., Steinmetz N.F. Design rules for nanomedical engineering: from physical virology to the applications of virus-based materials in medicine. J. Biol. Phys. 2013, 39:301-325.
128. Werner S., Marillonnet S., Hause G., Klimyuk V., Gleba Y. Immunoabsorbent nanoparticles based on a tobamovirus displaying protein A. Proc. Natl. Acad. Sci. USA 2006, 103:17678-17683.
129. Whaley S.R., English D.S., Hu E.L., Barbara P.F., Belcher A.M. Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 2000, 405:665-668.
130. Wilson T.M. Cotranslational disassembly of tobacco mosaic virus in vitro. Virology 1984, 137:255-265.
131. Xiong Z.G., Lommel S.A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 1991, 182:388-392.
132. Yang C.X., Meldon J.H., Lee B., Yi H. Investigation on the catalytic reduction kinetics of hexavalent chromium by viral-templated palladium nanocatalysts. Catal. Today 2014, 233:108-116.
133. Yi H., Nisar S., Lee S.Y., Powers M.A., Bentley W.E., Payne G.F., Ghodssi R., Rubloff G.W., Harris M.T., Culver J.N. Patterned assembly of genetically modified viral nanotemplates via nucleic acid hybridization. Nano Lett. 2005, 5:1931-1936.
134. Yi H., Rubloff G.W., Culver J.N. TMV microarrays: hybridization-based assembly of DNA-programmed viral nanotemplates. Langmuir 2007, 23:2663-2667.
135. Yildiz I., Shukla S., Steinmetz N.F. Applications of viral nanoparticles in medicine. Curr. Opin. Biotechnol. 2011, 22:901-908.
136. 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.
137. Zan X.J., Sitasuwan P., Powell J., Dreher T.W., Wang Q. Polyvalent display of RGD motifs on turnip yellow mosaic virus for enhanced stem cell adhesion and spreading. Acta Biomater. 2012, 8:2978-2985.
138. Zang F., Gerasopoulos K., Fan X.Z., Brown A.D., Culver J.N., Ghodssi R. An electrochemical sensor for selective TNT sensing based on Tobacco mosaic virus-like particle binding agents. Chem. Commun. (Camb.) 2014, 50:12977-12980.
139. Zeng Q.B., Saha S., Lee L.A., Barnhill H., Oxsher J., Dreher T., Wang Q.A. Chemoselective modification of turnip yellow mosaic virus by Cu(I) catalyzed azide-alkyne 1,3-Dipolar cycloaddition reaction and its application in cell binding. Bioconjugate Chem. 2011, 22:58-66.
140. Zhang Z.C., Xu B., Wang X. Engineering nanointerfaces for nanocatalysis. Chem. Soc. Rev. 2014, 43:7870-7886.
141. Zhou J.C., Soto C.M., Chen M.S., Bruckman M.A., Moore M.H., Barry E., Ratna B.R., Pehrsson P.E., Spies B.R., Confer T.S. Biotemplating rod-like viruses for the synthesis of copper nanorods and nanowires. J. Nanobiotechnol. 2012, 10:18.
142. Zhou K., Li F., Dai G.L., Meng C., Wang Q.B. Disulfide bond: dramatically enhanced assembly capability and structural stability of tobacco mosaic virus nanorods. Biomacromolecules 2013, 14:2593-2600.