Nano Research

, Volume 2, Issue 5, pp 349–364 | Cite as

Viruses and virus-like protein assemblies—Chemically programmable nanoscale building blocks

Open Access
Review Article

Abstract

Supramolecular proteins are generated using a limited set of twenty amino acids, but have distinctive functionalities which arise from the sequential arrangement of amino acids configured to exquisite three-dimensional structures. Viruses, virus-like particles, ferritins, enzyme complexes, cellular micro-compartments, and other supramolecular protein assemblies exemplify these systems, with their precise arrangements of tens to hundreds of molecules into highly organized scaffolds for nucleic acid packaging, metal storage, catalysis or sequestering reactions at the nanometer scale. These versatile protein systems, dubbed as bionanoparticles (BNPs), have attracted materials scientists to seek new opportunities with these pre-fabricated templates in a wide range of nanotechnology-related applications. Here, we focus on some of the key modification strategies that have been utilized, ranging from basic protein conjugation techniques to more novel strategies, to expand the functionalities of these multimeric protein assemblies. Ultimately, in combination with molecular cloning and sophisticated chemistries, these BNPs are being incorporated into many applications ranging from functional materials to novel biomedical drug designs.

Keywords

Bionanoparticles virus bioconjugation nanomaterials bioimaging drug delivery 

References

  1. [1]
    Niemeyer, C. M.; Adler, M. Nanomechanical devices based on DNA. Angew. Chem. Int. Ed. 2002, 41, 3779–3783.Google Scholar
  2. [2]
    Yan, H.; Park, S. H.; Finkelstein, G.; Reif, J. H.; LaBean, T. H. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 2003, 301, 1882–1884.PubMedADSGoogle Scholar
  3. [3]
    Jaeger, L.; Chworos, A. The architectonics of programmable RNA and DNA nanostructures. Curr. Opin. Struct. Biol. 2006, 16, 531–543.PubMedGoogle Scholar
  4. [4]
    Feldkamp, U.; Niemeyer, C. M. Rational design of DNA nanoarchitectures. Angew. Chem. Int. Ed. 2006, 45, 1856–1876.Google Scholar
  5. [5]
    Seeman, N. C.; Belcher, A. M. Emulating biology: Building nanostructures from the bottom up. Proc. Natl. Acad. Sci. USA 2002, 99, 6451–6455.PubMedADSGoogle Scholar
  6. [6]
    Dujardin, E.; Mann, S. Bio-inspired materials chemistry. Adv. Eng. Mater. 2002, 4, 461–474.Google Scholar
  7. [7]
    Seeman, N. C. At the crossroads of chemistry, biology, and materials: Structural DNA nanotechnology. Chem. Biol. 2003, 10, 1151–1159.PubMedGoogle Scholar
  8. [8]
    Yan, H.; LaBean, T. H.; Feng, L.; Reif, J. H. Directed nucleation assembly of DNA tile complexes for barcode-patterned lattices. Proc. Natl. Acad. Sci. USA 2003, 100, 8103–8108.PubMedADSGoogle Scholar
  9. [9]
    Winfree, E.; Liu, F.; Wenzler, L. A.; Seeman, N. C. Design and self-assembly of two-dimensional DNA crystals. Nature 1998, 394, 539–544.PubMedADSGoogle Scholar
  10. [10]
    Ding, B.; Seeman, N. C. Operation of a DNA robot arm inserted into a 2D DNA crystalline substrate. Science 2006, 314, 1583–1585.PubMedADSGoogle Scholar
  11. [11]
    Shih, W. M.; Quispe, J. D.; Joyce, G. F. A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 2004, 427, 618–621.PubMedADSGoogle Scholar
  12. [12]
    Goodman, R. P.; Schaap, I. A. T.; Tardin, C. F.; Erben, C. M.; Berry, R. M.; Schmidt, C. F.; Turberfield, A. J. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 2005, 310, 1661–1665.PubMedADSGoogle Scholar
  13. [13]
    Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440, 297–302.PubMedADSGoogle Scholar
  14. [14]
    Chworos, A.; Severcan, I.; Koyfman, A. Y.; Weinkam, P.; Oroudjev, E.; Hansma, H. G.; Jaeger, L. Building programmable jigsaw puzzles with RNA. Science 2004, 306, 2068–2072.PubMedADSGoogle Scholar
  15. [15]
    Douglas, T.; Young, M. Viruses: Making friends with old foes. Science 2006, 312, 873–875.PubMedADSGoogle Scholar
  16. [16]
    Kramer, R. M.; Li, C.; Carter, D. C.; Stone, M. O.; Naik, R. R. Engineered protein cages for nanomaterial synthesis. J. Am. Chem. Soc. 2004, 126, 13282–13286.PubMedGoogle Scholar
  17. [17]
    Meldrum, F. C.; Heywood, B. R.; Mann, S. Magnetoferritin: In vitro synthesis of a novel magnetic protein. Science 1992, 257, 522–523.PubMedADSGoogle Scholar
  18. [18]
    Flenniken, M. L.; Willits, D. A.; Brumfield, S.; Young, M. J.; Douglas, T. The small heat shock protein cage from Methanococcus jannaschii is a versatile nanoscale platform for genetic and chemical modification. Nano Lett. 2003, 3, 1573–1576.ADSGoogle Scholar
  19. [19]
    Seebeck, F. P.; Woycechowsky, K. J.; Zhuang, W.; Rabe, J. P.; Hilvert, D. A simple tagging system for protein encapsulation. J. Am. Chem. Soc. 2006, 128, 4516–4517.PubMedGoogle Scholar
  20. [20]
    Domingo, G. J.; Orru, S.; Perham, R. N. Multiple display of peptides and proteins on a macromolecular scaffold derived from a multienzyme complex. J. Mol. Biol. 2001, 305, 259–267.PubMedGoogle Scholar
  21. [21]
    Paavola, C. D.; Chan, S. L.; Li, Y.; Mazzarella, K. M.; McMillan, R. A.; Trent, J. D. A versatile platform for nanotechnology based on circular permutation of a chaperonin protein. Nanotechnology 2006, 17, 1171–1176.ADSGoogle Scholar
  22. [22]
    Campos, S. K.; Barry, M. A. Current advances and future challenges in adenoviral vector biology and targeting. Curr. Gene Ther. 2007, 7, 189–204.PubMedGoogle Scholar
  23. [23]
    Manchester, M.; Singh, P. Virus-based nanoparticles (VNPs): Platform technologies for diagnostic imaging. Adv. Drug Deliv. Rev. 2006, 58, 1505–1522.PubMedGoogle Scholar
  24. [24]
    Lee, L. A.; Wang, Q. Adaptations of nanoscale viruses and other protein cages for medical applications. Nanomedicine 2006, 2, 137–149.PubMedGoogle Scholar
  25. [25]
    Canizares, M. C.; Nicholson, L.; Lomonossoff, G. P. Use of viral vectors for vaccine production in plants. Immunol. Cell Biol. 2005, 83, 263–270.PubMedGoogle Scholar
  26. [26]
    Ramqvist, T.; Andreasson, K.; Dalanis, T. Vaccination, immune and gene therapy based on virus-like particles against viral infections and cancer. Expert Opin. Biol. Ther. 2007, 7, 997–1007.PubMedGoogle Scholar
  27. [27]
    Streatfield, S. J. Oral hepatitis B vaccine candidates produced and delivered in plant material. Immunol. Cell Biol. 2005, 83, 257–262.PubMedGoogle Scholar
  28. [28]
    Flynn, C. E.; Mao, C.; Hayhurst, A.; Williams, J. L.; Georgiou, G.; Iverson, B.; Belcher, A. M. Synthesis and organization of nanoscale II-III semiconductor materials using evolved peptide specificity and viral capsid assembly. J. Mater. Chem. 2003, 13, 2414–2421.Google Scholar
  29. [29]
    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. 2006, 3019–3021.Google Scholar
  30. [30]
    Niu, Z.; Bruckman, M. A.; Li, S.; Lee, L. A.; Lee, B.; Pingali, S. V.; Thiyagarajan, P.; Wang, Q. Assembly of tobacco mosaic virus into fibrous and macroscopic bundled arrays by aniline polymerization on its surface. Langmuir 2007, 23, 6719–6724.PubMedGoogle Scholar
  31. [31]
    Niu, Z.; Liu, J.; Lee, L. A.; Bruckman, M.; Zhao, D.; Koley, G.; Wang, Q. Biological templated synthesis of water-soluble conductive polymeric nanowires. Nano Lett. 2007, 7, 3729–3733.PubMedADSGoogle Scholar
  32. [32]
    Mao, C.; Flynn, C. E.; Hayhurst, A.; Sweeney, R.; Qi, J.; Georgiou, G.; Iverson, B.; Belcher, A. M. Viral assembly of oriented quantum dot nanowires. Proc. Natl. Acad. Sci. USA 2003, 100, 6946–6951.PubMedADSGoogle Scholar
  33. [33]
    Niu, Z.; Bruckman, M.; Harp, B.; Mello, C. M.; Wang, Q. Bacteriophage M13 as scaffold for preparing conductive polymeric composite fibers. Nano Res. 2008, 1, 235–241.Google Scholar
  34. [34]
    Rong, J.; Lee, L. A.; Li, K.; Harp, B.; Mello, C. M.; Niu, Z.; Wang, Q. Oriented cells growth on self-assembled bacteriophage M13 thin films. Chem. Commun. 2008, 5185–5187.Google Scholar
  35. [35]
    Aniagyei, S. E.; DuFort, C.; Kao, C. C.; Dragnea, B. Selfassembly approaches to nanomaterial encapsulation in viral protein cages. J. Mater. Chem. 2008, 18, 3763–3774.PubMedGoogle Scholar
  36. [36]
    Singh, P.; Gonzalez, M. J.; Manchester, M. Viruses and their uses in nanotechnology. Drug Dev. Res. 2006, 67, 23–41.Google Scholar
  37. [37]
    Steinmetz, N. F.; Evans, D. J. Utilisation of plant viruses in bionanotechnology. Org. Biomol. Chem. 2007, 5, 2891–2902.PubMedGoogle Scholar
  38. [38]
    Ueno, T. Functionalization of viral protein assemblies by self-assembly reactions. J. Mater. Chem. 2008, 18, 3741–3745.Google Scholar
  39. [39]
    Young, M.; Willits, D.; Uchida, M.; Douglas, T. Plant viruses as biotemplates for materials and their use in nanotechnology. Ann. Rev. Phytopathol. 2008, 46, 361–384.Google Scholar
  40. [40]
    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.PubMedGoogle Scholar
  41. [41]
    Wang, Q.; Kaltgrad, E.; Lin, T.; Johnson, J. E.; Finn, M. G. Natural supramolecular building blocks: Wild-type cowpea mosaic virus. Chem. Biol. 2002, 9, 805–811.PubMedGoogle Scholar
  42. [42]
    Wang, Q.; Lin, T.; Tang, L.; Johnson, J. E.; Finn, M. G. Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. 2002, 41, 459–462.Google Scholar
  43. [43]
    Wang, Q.; Raja, K. S.; Janda, K. D.; Lin, T.; Finn, M. G. Blue fluorescent antibodies as reporters of steric accessibility in virus conjugates. Bioconjugate Chem. 2003, 14, 38–43.Google Scholar
  44. [44]
    Raja, K. S.; Wang, Q.; Finn, M. G. Icosahedral virus particles as polyvalent carbohydrate display platforms. ChemBioChem 2003, 4, 1348–1351.PubMedGoogle Scholar
  45. [45]
    Gillitzer, E.; Willits, D.; Young, M.; Douglas, T. Chemical modification of a viral cage for multivalent presentation. Chem. Commun. 2002, 2390–2391.Google Scholar
  46. [46]
    Hooker, J. M.; Kovacs, E. W.; Francis, M. B. Interior surface modification of bacteriophage MS2. J. Am. Chem. Soc. 2004, 126, 3718–3719.PubMedGoogle Scholar
  47. [47]
    Schlick, T. L.; Ding, Z.; Kovacs, E. W.; Francis, M. B. Dualsurface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 2005, 127, 3718–3723.PubMedGoogle Scholar
  48. [48]
    Barnhill, H. N.; Claudel-Gillet, S.; Ziessel, R.; Charbonniere, L. J.; Wang, Q. Prototype protein assembly as scaffold for time-resolved fluoroimmuno assays. J. Am. Chem. Soc. 2007, 129, 7799–7806.PubMedGoogle Scholar
  49. [49]
    Lin, T.; Chen, Z.; Usha, R.; Stauffacher, C. V.; Dai, J. B.; Schmidt, T.; Johnson, J. E. The refined crystal structure of cowpea mosaic virus at 2.8 Å resolution. Virology 1999, 265, 20–34.PubMedGoogle Scholar
  50. [50]
    Chatterji, A.; Ochoa, W. F.; Paine, M.; Ratna, B. R.; Johnson, J. E.; Lin, T. New addresses on an addressable virus nanoblock: Uniquely reactive Lys residues on cowpea mosaic virus. Chem. Biol. 2004, 11, 855–863.PubMedGoogle Scholar
  51. [51]
    Barnhill, H. N.; Reuther, R.; Ferguson, P. L.; Dreher, T.; Wang, Q. Turnip yellow mosaic virus as a chemoaddressable bionanoparticle. Bioconjugate Chem. 2007, 18, 852–859.Google Scholar
  52. [52]
    Taylor, D.; Wang, Q.; Bothner, B.; Natarajan, P.; Finn, M. G.; Johnson, J. E. Correlation of chemical reactivity of Nudaurelia capensis omega virus with a pH-induced conformational change. Chem. Commun. 2003, 2770–2771.Google Scholar
  53. [53]
    Wong, K. K.; Colfen, H.; Whilton, N. T.; Douglas, T.; Mann, S. Synthesis and characterization of hydrophobic ferritin proteins. J. Inorg. Biochem. 1999, 76, 187–195.PubMedGoogle Scholar
  54. [54]
    Wong, K. K. W.; Whilton, N. T.; Douglas, T.; Mann, S.; Colfen, H. Hydrophobic proteins: Synthesis and characterization of organic-soluble alkylated ferritins. Chem. Commun. 1998, 1621–1622.Google Scholar
  55. [55]
    Steinmetz, N. F.; Lomonossoff, G. P.; Evans, D. J. Cowpea mosaic virus for material fabrication: Addressable carboxylate groups on a programmable nanoscaffold. Langmuir 2006, 22, 3488–3490.PubMedGoogle Scholar
  56. [56]
    Hermanson, G. T. Bioconjugate Techniques; Academic Press, Inc.: San Diego, CA, 1996.Google Scholar
  57. [57]
    Kovacs, E. W.; Hooker, J. M.; Romanini, D. W.; Holder, P. G.; Berry, K. E.; Francis, M. B. Dual-surface-modified bacteriophage MS2 as an ideal scaffold for a viral capsid-based drug delivery system. Bioconjugate Chem. 2007, 18, 1140–1147.Google Scholar
  58. [58]
    Hooker, J. M.; Datta, A.; Botta, M.; Raymond, K. N.; Francis, M. B. Magnetic resonance contrast agents from viral capsid shells: A comparison of exterior and interior cargo strategies. Nano Lett. 2007, 7, 2207–2210.PubMedADSGoogle Scholar
  59. [59]
    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.PubMedGoogle Scholar
  60. [60]
    Lin, T. Structural genesis of the chemical addressability of a viral nano-block. J. Mater. Chem. 2006, 16, 3673–3681.Google Scholar
  61. [61]
    Chatterji, A.; Ochoa, W. F.; Shamieh, L.; Salakian, S. P.; Wong, S. M.; Clinton, G.; Ghosh, P.; Lin, T.; Johnson, J. E. Chemical conjugation of heterologous proteins on the surface of cowpea mosaic virus. Bioconjugate Chem. 2004, 15, 807–813.Google Scholar
  62. [62]
    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.ADSGoogle Scholar
  63. [63]
    Flenniken, M. L.; Liepold, L. O.; Crowley, B. E.; Willits, D.; Young, M.; Douglas, T. Selective attachment and release of a chemotherapeutic agent from the interior of a protein cage architecture. Chem. Commun. 2005, 447–449.Google Scholar
  64. [64]
    Yi, H.; Rubloff, G. W.; Culver, J. N. TMV microarrays: Hybridization-based assembly of DNA-programmed viral nanotemplates. Langmuir 2007, 23, 2663–2667.PubMedGoogle Scholar
  65. [65]
    Yi, H. M.; 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.PubMedADSGoogle Scholar
  66. [66]
    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.PubMedGoogle Scholar
  67. [67]
    Kaltgrad, E.; Sen Gupta, S.; Punna, S.; Huang, C. Y.; Chang, A.; Wong, C. H.; Finn, M. G.; Blixt, O. Anticarbohydrate antibodies elicited by polyvalent display on a viral scaffold. ChemBioChem 2007, 8, 1455–1462.PubMedGoogle Scholar
  68. [68]
    Miermont, A.; Barnhill, H.; Strable, E.; Lu, X. W.; Wall, K. A.; Wang, Q.; Finn, M. G.; Huang, X. F. Cowpea mosaic virus capsid: A promising carrier for the development of carbohydrate based antitumor vaccines. Chem. Eur. J. 2008, 14, 4939–4947.Google Scholar
  69. [69]
    Kaltgrad, E.; O’Reilly, M. K.; Liao, L. A.; Han, S. F.; Paulson, J. C.; Finn, M. G. On-virus construction of polyvalent glycan ligands for cell-surface receptors. J. Am. Chem. Soc. 2008, 130, 4578–4579.PubMedGoogle Scholar
  70. [70]
    Gleiter, S.; Lilie, H. Cell-type specific targeting and gene expression using a variant of polyoma VP1 virus-like particles. Biol. Chem. 2003, 384, 247–255.PubMedGoogle Scholar
  71. [71]
    Rostovtsev, V. V.; Green, L. G.; Fokin, V. V.; Sharpless, K. B. A stepwise Huisgen cycloaddition process: Copper(I)-catalyzed regioselective “ligation” of azides and terminal alkynes. Angew. Chem. Int. Ed. 2002, 41, 2596–2599.Google Scholar
  72. [72]
    Antos, J. M.; Francis, M. B. Transition metal catalyzed methods for site-selective protein modification. Curr. Opin. Chem. Biol. 2006, 10, 253–262.PubMedGoogle Scholar
  73. [73]
    Tornoe, C. W.; Christensen, C.; Meldal, M. Peptidotriazoles on solid phase: [1,2,3]-triazoles by regiospecific copper(I)-catalyzed 1,3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 2002, 67, 3057–3064.PubMedGoogle Scholar
  74. [74]
    Lewis, W. G.; Magallon, F. G.; Fokin, V. V.; Finn, M. G. Discovery and characterization of catalysts for azidealkyne cycloaddition by fluorescence quenching. J. Am. Chem. Soc. 2004, 126, 9152–9153.PubMedGoogle Scholar
  75. [75]
    Sen Gupta, S.; Kuzelka, J.; Singh, P.; Lewis, W. G.; Manchester, M.; Finn, M. G. Accelerated bioorthogonal conjugation: A practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjugate Chem. 2005, 16, 1572–1579.Google Scholar
  76. [76]
    Wang, Q.; Chan, T. R.; Hilgraf, R.; Fokin, V. V.; Sharpless, K. B.; Finn, M. G. Bioconjugation by copper(I)-catalyzed azide-alkyne [3+2] cycloaddition. J. Am. Chem. Soc. 2003, 125, 3192–3193.PubMedGoogle Scholar
  77. [77]
    Zeng, Q.; Li, T.; Cash, B.; Li, S.; Xie, F.; Wang, Q. Chemoselective derivatization of a bionanoparticle by click reaction and ATRP reaction. Chem. Commun. 2007, 1453–1455.Google Scholar
  78. [78]
    Bruckman, M. A.; Kaur, G.; Lee, L. A.; Xie, F.; Sepulveda, J.; Breitenkamp, R.; Zhang, X.; Joralemon, M.; Russell, T. P.; Emrick, T.; Wang, Q. Surface modification of tobacco mosaic virus with “click” chemistry. ChemBioChem 2008, 9, 519–523.PubMedGoogle Scholar
  79. [79]
    Prasuhn, D. E.; Singh, P.; Strable, E.; Brown, S.; Manchester, M.; Finn, M. G. Plasma clearance of bacteriophage Qβ particles as a function of surface charge. J. Am. Chem. Soc. 2008, 130, 1328–1334.PubMedGoogle Scholar
  80. [80]
    Xie, F.; Sivakumar, K.; Zeng, Q.; Bruckman, M. A.; Hodges, B.; Wang, Q. A fluorogenic “click” reaction of azidoanthracene derivatives. Tetrahedron 2008, 64, 2906–2914.Google Scholar
  81. [81]
    Tilley, S. D.; Francis, M. B. Tyrosine-selective protein alkylation using π-allylpalladium complexes. J. Am. Chem. Soc. 2006, 128, 1080–1081.PubMedGoogle Scholar
  82. [82]
    Meunier, S.; Strable, E.; Finn, M. G. Crosslinking of and coupling to viral capsid proteins by tyrosine oxidation. Chem. Biol. 2004, 11, 319–326.PubMedGoogle Scholar
  83. [83]
    Sapsford, K. E.; Soto, C. M.; Blum, A. S.; Chatterji, A.; Lin, T.; Johnson, J. E.; Ligler, F. S.; Ratna, B. R. A cowpea mosaic virus nanoscaffold for multiplexed antibody conjugation: Application as an immunoassay tracer. Biosens. Bioelectron. 2006, 21, 1668–1673.PubMedGoogle Scholar
  84. [84]
    Soto, C. M.; Blum, A. S.; Vora, G. J.; Lebedev, N.; Meador, C. E.; Won, A. P.; Chatterji, A.; Johnson, J. E.; Ratna, B. R. Fluorescent signal amplification of carbocyanine dyes using engineered viral nanoparticles. J. Am. Chem. Soc. 2006, 128, 5184–5189.PubMedGoogle Scholar
  85. [85]
    Flenniken, M. L.; Willits, D. A.; Harmsen, A. L.; Liepold, L. O.; Harmsen, A. G.; Young, M. J.; Douglas, T. Melanoma and lymphocyte cell-specific targeting incorporated into a heat shock protein cage architecture. Chem. Biol. 2006, 13, 161–170.PubMedGoogle Scholar
  86. [86]
    Tan, W. S.; Lewis, C. L.; Horelik, N. E.; Pregibon, D. C.; Doyle, P. S.; Yi, H. Hierarchical assembly of viral nanotemplates with encoded microparticles via nucleic acid hybridization. Langmuir 2008, 24, 12483–12488.PubMedGoogle Scholar
  87. [87]
    Destito, G.; Yeh, R.; Rae, C. S.; Finn, M. G.; Manchester, M. Folic acid-mediated targeting of cowpea mosaic virus particles to tumor cells. Chem. Biol. 2007, 14, 1152–1162.PubMedGoogle Scholar
  88. [88]
    Douglas, T.; Young, M. Host-guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393, 152–155.ADSGoogle Scholar
  89. [89]
    Allen, M.; Willits, D.; Mosolf, J.; Young, M.; Douglas, T. Protein cage constrained synthesis of ferrimagnetic iron oxide nanoparticles. Adv. Mater. 2002, 14, 1562–1565.Google Scholar
  90. [90]
    Allen, M.; Willits, D.; Young, M.; Douglas, T. Constrained synthesis of cobalt oxide nanomaterials in the 12-subunit protein cage from Listeria innocua. Inorg. Chem. 2003, 42, 6300–6305.PubMedGoogle Scholar
  91. [91]
    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.Google Scholar
  92. [92]
    Wong, K. K. W.; Douglas, T.; Gider, S.; Awschalom, D. D.; Mann, S. Biomimetic synthesis and characterization of magnetic proteins (magnetoferritin). Chem. Mater. 1998, 10, 279–285.Google Scholar
  93. [93]
    Douglas, T.; Stark, V. T. Nanophase cobalt oxyhydroxide mineral synthesized within the protein cage of ferritin. Inorg. Chem. 2000, 39, 1828–1830.PubMedGoogle Scholar
  94. [94]
    Ensign, D.; Young, M.; Douglas, T. Photocatalytic synthesis of copper colloids from Cu(II) by the ferrihydrite core of ferritin. Inorg. Chem. 2004, 43, 3441–3446.PubMedGoogle Scholar
  95. [95]
    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.Google Scholar
  96. [96]
    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, 253–256.Google Scholar
  97. [97]
    Fonoberov, V. A.; Balandin, A. A. Phonon confinement effects in hybrid virus-inorganic nanotubes for nanoelectronic applications. Nano Lett. 2005, 5, 1920–1923.PubMedADSGoogle Scholar
  98. [98]
    Royston, E.; Lee, S. Y.; Culver, J. N.; Harris, M. T. Characterization of silica-coated tobacco mosaic virus. J Colloid Interface Sci. 2006, 298, 706–712.PubMedGoogle Scholar
  99. [99]
    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.ADSGoogle Scholar
  100. [100]
    Knez, M.; Kadri, A.; Wege, C.; Gosele, U.; Jeske, H.; Nielsch, K. Atomic layer deposition on biological macromolecules: Metal oxide coating of tobacco mosaic virus and ferritin. Nano Lett. 2006, 6, 1172–1177.PubMedADSGoogle Scholar
  101. [101]
    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.Google Scholar
  102. [102]
    Knez, M.; Sumser, M. P.; Bittner, A. M.; Wege, C.; Jeske, H.; Hoffmann, D. M. P.; Kuhnke, K.; Kern, K. Binding the tobacco mosaic virus to inorganic surfaces. Langmuir 2004, 20, 441–447.PubMedGoogle Scholar
  103. [103]
    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.ADSGoogle Scholar
  104. [104]
    Brown, S. Engineered iron oxide-adhesion mutants of the Escherichia coli phage receptor. Proc. Natl. Acad. Sci. USA. 1992, 89, 8651–8655.PubMedADSGoogle Scholar
  105. [105]
    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.PubMedADSGoogle Scholar
  106. [106]
    Lee, S. W.; Mao, C.; Flynn, C. E.; Belcher, A. M. Ordering of quantum dots using genetically engineered viruses. Science 2002, 296, 892–895.PubMedADSGoogle Scholar
  107. [107]
    Flynn, C. E.; Mao, C. B.; Hayhurst, A.; Williams, J. L.; Georgiou, G.; Iverson, B.; Belcher, A. M. Synthesis and organization of nanoscale II-IV semiconductor materials using evolved peptide specificity and viral capsid assembly. J. Mater. Chem. 2003, 13, 2414–2421.Google Scholar
  108. [108]
    Nam, K. T.; Peelle, B. R.; Lee, S. -W.; Belcher, A. M. Genetically driven assembly of nanorings based on the M13 virus. Nano Lett. 2004, 4, 23–27.ADSGoogle Scholar
  109. [109]
    Lee, S. W.; Belcher, A. M. Virus-based fabrication of micro- and nanofibers using electrospinning. Nano Lett. 2004, 4, 387–390.ADSGoogle Scholar
  110. [110]
    Lee, S. W.; Wood, B. M.; Belcher, A. M. Chiral smectic C structures of virus-based films. Langmuir 2003, 19, 1592–1598.Google Scholar
  111. [111]
    Lee, S. W.; Lee, S. K.; Belcher, A. M. Virus-based alignment of inorganic, organic, and biological nanosized materials. Adv. Mater. 2003, 15, 689–692.Google Scholar
  112. [112]
    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.Google Scholar
  113. [113]
    Souza, G. R.; Christianson, D. R.; Staquicini, F. I.; Ozawa, M. G.; Snyder, E. Y.; Sidman, R. L.; Houston Miller, J.; Arap, W.; R., P. Networks of gold nanoparticles and bacteriophage as biological sensors and celltargeting agents. Proc. Natl. Acad. Sci. USA 2006, 103, 1215–1220.PubMedADSGoogle Scholar
  114. [114]
    Huang, Y.; Chiang, C. Y.; Lee, S. K.; Gao, Y.; Hu, E. L.; De Yoreo, J.; Belcher, A. M. Programmable assembly of nanoarchitectures using genetically engineered viruses. Nano Lett. 2005, 5, 1429–1434.PubMedADSGoogle Scholar
  115. [115]
    Nam, K. T.; Kim, D. W.; Yoo, P. J.; Chiang, C. Y.; Meethong, N.; Hammond, P. T.; Chiang, Y. M.; Belcher, A. M. Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 2006, 312, 885–888.PubMedADSGoogle Scholar
  116. [116]
    Carette, N.; Engelkamp, H.; Akpa, E.; Pierre, S. J.; Cameron, N. R.; Christianen, P. C. M.; Maan, J. C.; Thies, J. C.; Weberskirch, R.; Rowan, A. E.; Nolte, R. J. M.; Michon, T.; Van Hest, J. C. M. A virus-based biocatalyst. Nat. Nanotechnol. 2007, 2, 226–229.PubMedADSGoogle Scholar
  117. [117]
    Comellas-Aragones, M.; Engelkamp, H.; Claessen, V. I.; Sommerdijk, N.; Rowan, A. E.; Christianen, P. C. M.; Maan, J. C.; Verduin, B. J. M.; Cornelissen, J.; Nolte, R. J. M. A virus-based single-enzyme nanoreactor. Nat. Nanotechnol. 2007, 2, 635–639.PubMedADSGoogle Scholar
  118. [118]
    Sun, J.; DuFort, C.; Daniel, M. C.; Murali, A.; Chen, C.; Gopinath, K.; Stein, B.; De, M.; Rotello, V. M.; Holzenburg, A.; Kao, C. C.; Dragnea, B. Core-controlled polymorphism in virus-like particles. Proc. Natl. Acad. Sci. USA. 2007, 104, 1354–1359.PubMedADSGoogle Scholar
  119. [119]
    Chen, C.; Daniel, M. -C.; Quinkert, Z. T.; De, M.; Stein, B.; Bowman, V. D.; Chipman, P. R.; Rotello, V. M.; Kao, C. C.; Dragnea, B. Nanoparticle-templated assembly of viral protein cages. Nano Lett. 2006, 6, 611–615.PubMedADSGoogle Scholar
  120. [120]
    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.PubMedADSGoogle Scholar
  121. [121]
    Huang, X.; Bronstein, L. M.; Retrum, J.; Dufort, C.; Tsvetkova, I.; Aniagyei, S.; Stein, B.; Stucky, G.; McKenna, B.; Remmes, N.; Baxter, D.; Kao, C. C.; Dragnea, B. Self-assembled virus-like particles with magnetic cores. Nano Lett. 2007, 7, 2407–2416.PubMedADSGoogle Scholar
  122. [122]
    Loo, L.; Guenther, R. H.; Basnayake, V. R.; Lommel, S. A.; Franzen, S. Controlled encapsidation of gold nanoparticles by a viral protein shell. J. Am. Chem. Soc. 2006, 128, 4502–4503.PubMedGoogle Scholar
  123. [123]
    Loo, L.; Guenther, R. H.; Lommel, S. A.; Franzen, S. Infusion of dye molecules into red clover necrotic mosaic virus. Chem. Commun. 2008, 88–90.Google Scholar
  124. [124]
    Fischlechner, M.; Reibetanz, U.; Zaulig, M.; Enderlein, D.; Romanova, J.; Leporatti, S.; Moya, S.; Donath, E. Fusion of enveloped virus nanoparticles with polyelectrolyte-supported lipid membranes for the design of bio/nonbio interfaces. Nano Lett. 2007, 7, 3540–3546.PubMedADSGoogle Scholar
  125. [125]
    Fischlechner, M.; Toellner, L.; Messner, P.; Grabherr, R.; Donath, E. Virus-engineered colloidal particles A surface display system. Angew. Chem. Int. Ed. 2006, 45, 784–789.Google Scholar
  126. [126]
    Li, T.; Niu, Z. W.; Emrick, T.; Russell, T. R.; Wang, Q. Core/shell biocomposites from the hierarchical assembly of bionanoparticles and polymer. Small 2008, 4, 1624–1629.PubMedGoogle Scholar
  127. [127]
    Lin, Y.; Su, Z.; Niu, Z.; Li, S.; Kaur, G.; Lee, L. A.; Wang, Q. Layer-by-layer assembly of viral capsid for cell adhesion. Acta Biomater. 2008, 4, 838–843.PubMedGoogle Scholar
  128. [128]
    Steinmetz, N. F.; Findlay, K. C.; Noel, T. R.; Parker, R.; Lomonossoff, G. R.; Evans, D. J. Layer-by-layer assembly of viral nanoparticles and polyelectrolytes: The film architecture is different for spheres versus rods. ChemBioChem 2008, 9, 1662–1670.PubMedGoogle Scholar
  129. [129]
    Yoo, P. J.; Nam, K. T.; Belchert, A. M.; Hammond, P. T. Solvent-assisted patterning of polyelectrolyte multilayers and selective deposition of virus assemblies. Nano Lett. 2008, 8, 1081–1089.PubMedADSGoogle Scholar

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© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Department of Chemistry & Biochemistry and NanocenterUniversity of South CarolinaColumbiaUSA

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