Controlling forces and pathways in self-assembly using viruses and DNA

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 3, Issue 3, 2011, Pages 282-297

  Keum, Jung Won ^a   Hathorne, Adam P ^a   Bermudez, Harry ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NANO SCALE; SELF-ASSEMBLE; TEMPORAL CONTROLS;

SELF ASSEMBLY; VIRUSES;

NUCLEIC ACIDS;

DNA; NANOMATERIAL;

BIOMEDICINE; DNA VIRUS; HYDROGEN BOND; PRIORITY JOURNAL; REVIEW; STATIC ELECTRICITY; VIRUS ASSEMBLY;

BIOMECHANICS; DNA; NANOSTRUCTURES; VIRUSES;

EID: 79953273551     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.129     Document Type: Review

References (167)

1. Whitesides G, Boncheva M. Beyond molecules: self-assembly of mesoscopic and macroscopic components. Proc Natl Acad Sci U S A 2002, 99:4769-4774.
2. Whitesides GM, Grzybowski B. Self-assembly at all scales. Science 2002, 295:2418-2421.
3. Grosberg AY, Khokhlov AR. Statistical Physics of Macromolecules. New York: AIP Press; 1994.
4. Sambriski EJ, Schwartz DC, de Pablo JJ. A mesoscale model of DNA and its renaturation. Biophys J 2009, 96:1675-1690.
5. He Y, Mao CD. Balancing flexibility and stress in DNA nanostructures. Chem Commun 2006, 968-969.
6. Zhang C, Su M, He Y, Zhao X, Fang P-A, Ribbe AE, Jiang W, Mao C. Conformational flexibility facilitates self-assembly of complex DNA nanostructures. Proc Natl Acad Sci U S A 2008, 105:10665-10669.
7. Park SY, Lytton-Jean AKR, Lee B, Weigand S, Schatz GC, Mirkin CA. DNA-programmable nanoparticle crystallization. Nature 2008, 451:553-556.
8. Nykypanchuk D, Maye MM, van der Lelie D, Gang O. DNA-guided crystallization of colloidal nanoparticles. Nature 2008, 451:549-552.
9. Liedl T, Hogberg B, Tytell J, Ingber DE, Shih WM. Self-assembly of three-dimensional prestressed tensegrity structures from DNA. Nature Nanotechnol 2010, 5:520-524.
10. Yurke B, Turberfield AJ, Mills AP, Simmel FC, Neumann JL. A DNA-fuelled molecular machine made of DNA. Nature 2000, 406:605-608.
11. Seeman NC. Nucleic acid junctions and lattices. J Theor Biol 1982, 99:237-247.
12. Boal DH. Mechanics of the Cell. Cambridge: Cambridge University Press; 2002.
13. Dietz H, Douglas SM, Shih WM. Folding DNA into twisted and curved nanoscale shapes. Science 2009, 325:725-730.
14. Douglas SM, Dietz H, Liedl T, Hoegberg B, Graf F, Shih WM. Self-assembly of DNA into nanoscale three-dimensional shapes. Nature 2009, 459:414-418.
15. Zheng J, Birktoft JJ, Chen Y, Wang T, Sha R, Constantinou PE, Ginell SL, Mao C, Seeman NC. From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 2009, 461:74-77.
16. Fu TJ, Seeman NC. DNA double-crossover molecules. Biochemistry 1993, 32:3211-3220.
17. Li XJ, Yang XP, Qi J, Seeman NC. Antiparallel DNA double crossover molecules as components for nanoconstruction. J Am Chem Soc 1996, 118:6131-6140.
18. Winfree E, Liu F, Wenzler L, Seeman N. Design and self-assembly of two-dimensional DNA crystals. Nature 1998, 394:539-544.
19. LaBean TH, Yan H, Kopatsch J, Liu FR, Winfree E, Reif JH, Seeman NC. Construction, analysis, ligation, and self-assembly of DNA triple crossover complexes. J Am Chem Soc 2000, 122:1848-1860.
20. Sa-Ardyen P, Vologodskii AV, Seeman NC. The flexibility of DNA double crossover molecules. Biophys J 2003, 84:3829-3837.
21. Israelachvili JN. Intermolecular and Surface Forces. San Diego: Academic Press; 1992.
22. Seeman NC. De novo design of sequences for nucleic acid structural engineering. J Biomol Struct Dyn 1990, 8:573-581.
23. Douglas SM, Marblestone AH, Teerapittayanon S, Vazquez A, Church GM, Shih WM. Rapid prototyping of 3D DNA-origami shapes with caDNAno. Nucleic Acids Res 2009, 37:5001-5006.
24. Phan AT, Mergny J-L. Human telomeric DNA: G-quadruplex, i-motif and Watson-Crick double helix. Nucleic Acids Res 2002, 30:4618-4625.
25. Silverstein KAT, Haymet ADJ, Dill KA. The strength of hydrogen bonds in liquid water and around nonpolar solutes. J Am Chem Soc 2000, 122:8037-8041.
26. Dill KA, Truskett TM, Vlachy V, Hribar-Lee B. Modeling water, the hydrophobic effect, and ion solvation. Annu Rev Biophys Biomol Struct 2005, 34:173-199.
27. Chandler D. Interfaces and the driving force of hydrophobic assembly. Nature 2005, 437:640-647.
28. Bermudez H, Brannan AK, Hammer DA, Bates FS, Discher DE. Molecular weight dependence of polymersome membrane structure, elasticity, and stability. Macromolecules 2002, 35:8203-8208.
29. Bermudez H, Aranda-Espinoza H, Hammer DA, Discher DE. Pore stability and dynamics in polymer membranes. Europhys Lett 2003, 64:550-556.
30. Bermudez H, Hammer DA, Discher DE. Effect of bilayer thickness on membrane bending rigidity. Langmuir 2004, 20:540-543.
31. Wong GCL, Pollack L. Electrostatics of strongly charged biological polymers: ion-mediated interactions and self-organization in nucleic acids and proteins. Annu Rev Phys Chem 2010, 61:171-189.
32. Diehl A, Carmona HA, Levin Y. Counterion correlations and attraction between like-charged macromolecules. Phys Rev E Stat Nonlin Soft Matter Phys 2001, 64:011804.
33. Owczarzy R, Moreira BG, You Y, Behlke MA, Walder JA. Predicting stability of DNA duplexes in solutions containing magnesium and monovalent cations. Biochemistry 2008, 47:5336-5353.
34. Strey HH, Podgornik R, Rau DC, Parsegian VA. DNA-DNA interactions. Curr Opin Struct Biol 1998, 8:309-313.
35. Andresen K, Qiu X, Pabit SA, Lamb JS, Park HY, Kwok LW, Pollack L. Mono- and trivalent ions around DNA: a small-angle scattering study of competition and interactions. Biophys J 2008, 95:287-295.
36. Arscott PG, Li AZ, Bloomfield VA. Condensation of DNA by trivalent cations. 1. Effects of DNA length and topology on the size and shape of condensed particles. Biopolymers 1990, 30:619-630.
37. Ou Z, Muthukumar M. Langevin dynamics of semiflexible polyelectrolytes: rod-toroid-globule-coil structures and counterion distribution. J Chem Phys 2005, 123:074905.
38. Rich A, Nordheim A, Wang AH. The chemistry and biology of left-handed Z-DNA. Annu Rev Biochem 1984, 53:791-846.
39. Forrey C, Muthukumar M. Langevin dynamics simulations of genome packing in bacteriophage. Biophys J 2006, 91:25-41.
40. Belyi VA, Muthukumar M. Electrostatic origin of the genome packing in viruses. Proc Natl Acad Sci U S A 2006, 103:17174-17178.
41. Cacace MG, Landau EM, Ramsden JJ. The Hofmeister series: salt and solvent effects on interfacial phenomena. Q Rev Biophys 1997, 30:241-277.
42. Collins KD, Washabaugh MW. The Hofmeister effect and the behaviour of water at interfaces. Q Rev Biophys 1985, 18:323-422.
43. Zhang Y, Cremer PS. Chemistry of Hofmeister anions and osmolytes. Annu Rev Phys Chem 2010, 61:63-83.
44. Hamaguchi K, Geiduschek EP. The effect of electrolytes on the stability of the deoxyribonucleate helix. J Am Chem Soc 1962, 84:1329.
45. Pegram LM, Wendorff T, Erdmann R, Shkel I, Bellissimo D, Felitsky DJ, Record MT, Jr. Why Hofmeister effects of many salts favor protein folding but not DNA helix formation. Proc Natl Acad Sci U S A 2010, 107:7716-7721.
46. Claessens CG, Stoddart JF. pi-pi interactions in self-assembly. J Phys Organ Chem 1997, 10:254-272.
47. Arnold GE, Day LA, Dunker AK. Tryptophan contributions to the unusual circular dichroism of fd bacteriophage. Biochemistry 1992, 31:7948-7956.
48. Meunier S, Strable E, Finn MG. Crosslinking of and coupling to viral capsid proteins by tyrosine oxidation. Chem Biol 2004, 11:319-326.
49. DiPrimio N, Asokan A, Govindasamy L, Agbandje-McKenna M, Samulski RJ. Surface loop dynamics in adeno-associated virus capsid assembly. J Virol 2008, 82:5178-5189.
50. Seela F, Grein T. 7-Deaza-2'-deoxyadenosine and 3-deaza-2'-deoxyadenosine replacing dA within d(A6)-tracts: differential bending at 3'- and 5'-junctions of d(A6).d(T6) and B-DNA. Nucleic Acids Res 1992, 20: 2297-2306.
51. Genereux JC, Barton JK. Mechanisms for DNA charge transport. Chem Rev 2010, 110:1642-1662.
52. Guest CR, Hochstrasser RA, Sowers LC, Millar DP. Dynamics of mismatched base pairs in DNA. Biochemistry 1991, 30:3271-3279.
53. Xu D, Evans KO, Nordlund TM. Melting and premelting transitions of an oligomer measured by DNA base fluorescence and absorption. Biochemistry 1994, 33:9592-9599.
54. Butler PJ. Self-assembly of tobacco mosaic virus: the role of an intermediate aggregate in generating both specificity and speed. Philos Trans R Soc Lond B Biol Sci 1999, 354:537-550.
55. Butler PJ. The current picture of the structure and assembly of tobacco mosaic virus. J Gen Virol 1984, 65(Pt 2):253-279.
56. McPherson A. Micelle formation and crystallization as paradigms for virus assembly. Bioessays 2005, 27:447-458.
57. Zlotnick A, Aldrich R, Johnson JM, Ceres P, Young MJ. Mechanism of capsid assembly for an icosahedral plant virus. Virology 2000, 277:450-456.
58. Caspar DL. Movement and self-control in protein assemblies. Quasi-equivalence revisited. Biophys J 1980, 32:103-138.
59. Johnson JE, Speir JA. Quasi-equivalent viruses: a paradigm for protein assemblies. J Mol Biol 1997, 269:665-675.
60. Bancroft JB. The self-assembly of spherical plant viruses. Adv Virus Res 1970, 16:99-134.
61. Hagan MF, Chandler D. Dynamic pathways for viral capsid assembly. Biophys J 2006, 91:42-54.
62. Yan H, Park SH, Finkelstein G, Reif JH, LaBean TH. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 2003, 301:1882-1884.
63. Liu Y, Yan H. Modular self-assembly of DNA lattices with tunable periodicity. Small 2005, 1:327-330.
64. Goodman RP, Schaap IAT, Tardin CF, Erben CM, Berry RM, Schmidt CF, Turberfield AJ. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 2005, 310:1661-1665.
65. He Y, Ye T, Su M, Zhang C, Ribbe AE, Jiang W, Mao C. Hierarchical self-assembly of DNA into symmetric supramolecular polyhedra. Nature 2008, 452:198-201.
66. Li Z, Wei B, Nangreave J, Lin C, Liu Y, Mi Y, Yan H. A replicable tetrahedral nanostructure self-assembled from a single DNA strand. J Am Chem Soc 2009, 131:13093-13098.
67. Rothemund PWK. Folding DNA to create nanoscale shapes and patterns. Nature 2006, 440:297-302.
68. Lavelle L, Michel J-P, Gingery M. The disassembly, reassembly and stability of CCMV protein capsids. J Virol Methods 2007, 146:311-316.
69. van der Schoot P, Bruinsma R. Electrostatics and the assembly of an RNA virus. Phys Rev E Stat Nonlin Soft Matter Phys 2005, 71:061928.
70. Bruinsma RF. Physics of RNA and viral assembly. Eur Phys J E Soft Matter 2006, 19:303-310.
71. Liu Y, Ke Y, Yan H. Self-assembly of symmetric finite-size DNA nanoarrays. J Am Chem Soc 2005, 127:17140-17141.
72. Park S, Pistol C, Ahn S, Reif J, Lebeck A, Dwyer C, LaBean T. Finite-size, fully addressable DNA tile lattices formed by hierarchical assembly procedures. Angew Chem Int Ed 2006, 45:735-739.
73. Ke Y, Sharma J, Liu M, Jahn K, Liu Y, Yan H. Scaffolded DNA origami of a DNA tetrahedron molecular container. Nano Lett 2009, 9:2445-2447.
74. Rice G, Tang L, Stedman K, Roberto F, Spuhler J, Gillitzer E, Johnson JE, Douglas T, Young M. The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life. Proc Natl Acad Sci U S A 2004, 101:7716-7720.
75. Chen JH, Seeman NC. Synthesis from DNA of a molecule with the connectivity of a cube. Nature 1991, 350:631-633.
76. Park SH, Yin P, Liu Y, Reif JH, LaBean TH, Yan H. Programmable DNA self-assemblies for nanoscale organization of ligands and proteins. Nano Lett 2005, 5:729-733.
77. Zhang C, He Y, Chen Y, Ribbe AE, Mao C. Aligning one-dimensional DNA duplexes into two-dimensional crystals. J Am Chem Soc 2007, 129:14134-14135.
78. Andersen ES, Dong M, Nielsen MM, Jahn K, Subramani R, Mamdouh W, Golas MM, Sander B, Stark H, Oliveira CLP, et al. Self-assembly of a nanoscale DNA box with a controllable lid. Nature 2009, 459:73-76.
79. Sacca B, Meyer R, Feldkamp U, Schroeder H, Niemeyer CM. High-throughput, real-time monitoring of the self-assembly of DNA nanostructures by FRET spectroscopy. Angew Chem Int Ed Engl 2008, 47:2135-2137.
80. Nangreave J, Yan H, Liu Y. Studies of thermal stability of multivalent DNA hybridization in a nanostructured system. Biophys J 2009, 97:563-571.
81. Leunissen ME, Dreyfus R, Cheong FC, Grier DG, Sha R, Seeman NC, Chaikin PM. Switchable self-protected attractions in DNA-functionalized colloids. Nat Mater 2009, 8:590-595.
82. Jaeger L, Chworos A. The architectonics of programmable RNA and DNA nanostructures. Curr Opin Struct Biol 2006, 16:531-543.
83. Chworos A, Severcan I, Koyfman AY, Weinkam P, Oroudjev E, Hansma HG, Jaeger L. Building programmable jigsaw puzzles with RNA. Science 2004, 306:2068-2072.
84. Zlotnick A, Johnson JM, Wingfield PW, Stahl SJ, Endres D. A theoretical model successfully identifies features of hepatitis B virus capsid assembly. Biochemistry 1999, 38:14644-14652.
85. Liu D, Wang M, Deng Z, Walulu R, Mao C. Tensegrity: construction of rigid DNA triangles with flexible four-arm DNA junctions. J Am Chem Soc 2004, 126:2324-2325.
86. Mathieu F, Liao S, Kopatscht J, Wang T, Mao C, Seeman N. Six-helix bundles designed from DNA. Nano Lett 2005, 5:661-665.
87. Ke Y, Liu Y, Zhang J, Yan H. A study of DNA tube formation mechanisms using 4-, 8-, and 12-helix DNA nanostructures. J Am Chem Soc 2006, 128:4414-4421.
88. Steven AC, Heymann JB, Cheng N, Trus BL, Conway JF. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr Opin Struct Biol 2005, 15:227-236.
89. Dokland T. Scaffolding proteins and their role in viral assembly. Cell Mol Life Sci 1999, 56:580-603.
90. Cann A. Principles of Molecular Virology. 4th ed. Amsterdam: Elsevier Academic Press; 2005.
91. 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.
92. Shih WM, Quispe JD, Joyce GF. A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 2004, 427:618-621.
93. Douglas T, Young M. Virus particles as templates for materials synthesis. Adv Mater 1999, 11:679.
94. Uchida M, Klem MT, Allen M, Suci P, Flenniken M, Gillitzer E, Varpness Z, Liepold LO, Young M, Douglas T. Biological containers: protein cages as multifunctional nanoplatforms. Adv Mater 2007, 19:1025-1042.
95. Strable E, Finn MG. Chemical modification of viruses and virus-like particles. Curr Top Microbiol Immunol 2009, 327:1-21.
96. Seeman NC. DNA nanotechnology: novel DNA constructions. Annu Rev Biophys Biomol Struct 1998, 27:225-248.
97. Feldkamp U, Niemeyer CM. Rational design of DNA nanoarchitectures. Angew Chem Int Ed 2006, 45:1856-1876.
98. Aldaye FA, Palmer AL, Sleiman HF. Assembling materials with DNA as the guide. Science 2008, 321:1795-1799.
99. Ivanenkov VV, Felici F, Menon AG. Uptake and intracellular fate of phage display vectors in mammalian cells. Biochim Biophys Acta Mol Cell Res 1999, 1448:450-462.
100. Ivanenkov VV, Felici F, Menon AG. Targeted delivery of multivalent phage display vectors into mammalian cells. Biochim Biophys Acta Mol Cell Res 1999, 1448:463-472.
101. Larocca D, Kassner PD, Witte A, Ladner RC, Pierce GF, Baird A. Gene transfer to mammalian cells using genetically targeted filamentous bacteriophage. FASEB J 1999, 13:727-734.
102. Frenkel D, Solomon B. Filamentous phage as vector-mediated antibody delivery to the brain. Proc Natl Acad Sci U S A 2002, 99:5675-5679.
103. Anderson EA, Isaacman S, Peabody DS, Wang EY, Canary JW, Kirshenbaum K. Viral nanoparticles donning a paramagnetic coat: Conjugation of MRI contrast agents to the MS2 capsid. Nano Lett 2006, 6:1160-1164.
104. 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.
105. 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 (Camb) 2007, 1269-1271.
106. 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.
107. Suci PA, Berglund DL, Liepold L, Brumfield S, Pitts B, Davison W, Oltrogge L, Hoyt KO, Codd S, Stewart PS, et al. High-density targeting of a viral multifunctional nanoplatform to a pathogenic, biofilm-forming bacterium. Chem Biol 2007, 14:387-398.
108. Brunel FM, Lewis JD, Destito G, Steinmetz NF, Manchester M, Stuhlmann H, Dawson PE. Hydrazone ligation strategy to assemble multifunctional viral nanoparticles for cell imaging and tumor targeting. Nano Lett 2010, 10:1093-1097.
109. Chhabra R, Sharma J, Liu Y, Rinker S, Yan H. DNA Self-assembly for nanomedicine. Adv Drug Deliv Rev 2010, 62:617-625.
110. Douglas T, Young M. Host-guest encapsulation of materials by assembled virus protein cages. Nature 1998, 393:152-155.
111. Chatterji A, Ochoa WF, Ueno T, Lin T, Johnson JE. A virus-based nanoblock with tunable electrostatic properties. Nano Lett 2005, 5:597-602.
112. Braun E, Eichen Y, Sivan U, Ben-Yoseph G. DNA-templated assembly and electrode attachment of a conducting silver wire. Nature 1998, 391:775-778.
113. 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.
114. Knez M, Bittner AM, 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.
115. Liu D, Park SH, Reif JH, LaBean TH. DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires. Proc Natl Acad Sci U S A 2004, 101:717-722.
116. Gu Q, Cheng CD, Haynie DT. Cobalt metallization of DNA: toward magnetic nanowires. Nanotechnology 2005, 16:1358-1363.
117. Nam KT, Kim D-W, Yoo PJ, Chiang C-Y, Meethong N, Hammond PT, Chiang Y-M, Belcher AM. Virus-enabled synthesis and assembly of nanowires for lithium ion battery electrodes. Science 2006, 312:885-888.
118. Gazit E. Use of biomolecular templates for the fabrication of metal nanowires. FEBS J 2007, 274:317-322.
119. Bermudez H, Hathorne AP. Incorporating stimulus-responsive character into filamentous virus assemblies. Faraday Discuss 2008, 139:327-335.
120. Wang Q, Lin T, Johnson JE, Finn MG. Natural supramolecular building blocks. Cysteine-added mutants of cowpea mosaic virus. Chem Biol 2002, 9:813-819.
121. Wang Q, Lin T, Tang L, Johnson JE, Finn MG. Icosahedral virus particles as addressable nanoscale building blocks. Angew Chem Int Ed Engl 2002, 41:459-462.
122. Steinmetz NF, Lomonossoff GP, Evans DJ. Decoration of cowpea mosaic virus with multiple, redox-active, organometallic complexes. Small 2006, 2:530-533.
123. 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, 4:472-476.
124. Raja KS, Wang Q, Finn MG. Icosahedral virus particles as polyvalent carbohydrate display platforms. Chembiochem 2003, 4:1348-1351.
125. Medintz IL, Sapsford KE, Konnert JH, Chatterji A, Lin T, Johnson JE, Mattoussi H. Decoration of discretely immobilized cowpea mosaic virus with luminescent quantum dots. Langmuir 2005, 21:5501-5510.
126. Portney NG, Singh K, Chaudhary S, Destito G, Schneemann A, Manchester M, Ozkan M. Organic and inorganic nanoparticle hybrids. Langmuir 2005, 21:2098-2103.
127. Wang Q, Kaltgrad E, Lin T, Johnson JE, Finn MG. Natural supramolecular building blocks. Wild-type cowpea mosaic virus. Chem Biol 2002, 9:805-811.
128. Wang Q, Chan TR, Hilgraf R, Fokin VV, Sharpless KB, Finn MG. Bioconjugation by copper(I)-catalyzed azide-alkyne [3+2] cycloaddition. J Am Chem Soc 2003, 125:3192-3193.
129. Strable E, Johnson JE, Finn MG. Natural nanochemical building blocks: icosahedral virus particles organized by attached oligonucleotides. Nano Lett 2004, 4:1385-1389.
130. Sen Gupta S, Kuzelka J, Singh P, Lewis WG, Manchester M, Finn MG. Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold. Bioconjug Chem 2005, 16:1572-1579.
131. Steinmetz NF, Manchester M. PEGylated viral nanoparticles for biomedicine: the impact of PEG chain length on VNP cell interactions in vitro and ex vivo. Biomacromolecules 2009, 10:784-792.
132. Steinmetz NF, Lomonossoff GP, Evans DJ. Cowpea mosaic virus for material fabrication: addressable carboxylate groups on a programmable nanoscaffold. Langmuir 2006, 22:3488-3490.
133. Gillitzer E, Willits D, Young M, Douglas T. Chemical modification of a viral cage for multivalent presentation. Chem Commun (Camb) 2002, 2390-2391.
134. Klem MT, Willits D, Young M, Douglas T. 2-D array formation of genetically engineered viral cages on Au surfaces and imaging by atomic force microscopy. J Am Chem Soc 2003, 125:10806-10807.
135. Schlick TL, Ding Z, Kovacs EW, Francis MB. Dual-surface modification of the tobacco mosaic virus. J Am Chem Soc 2005, 127:3718-3723.
136. 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.
137. Miller RA, Stephanopoulos N, McFarland JM, Rosko AS, Geissler PL, Francis MB. Impact of assembly state on the defect tolerance of TMV-based light harvesting arrays. J Am Chem Soc 2010, 132:6068-6074.
138. Bruckman MA, Kaur G, Lee LA, Xie F, Sepulveda J, Breitenkamp R, Zhang X, Joralemon M, Russell TP, Emrick T, et al. Surface modification of tobacco mosaic virus with "click" chemistry. Chembiochem 2008, 9:519-523.
139. Hooker JM, Kovacs EW, Francis MB. Interior surface modification of bacteriophage MS2. J Am Chem Soc 2004, 126:3718-3719.
140. Antos JM, Francis MB. Transition metal catalyzed methods for site-selective protein modification. Curr Opin Chem Biol 2006, 10:253-262.
141. Strable E, Prasuhn DEJ, Udit AK, Brown S, Link AJ, Ngo JT, Lander G, Quispe J, Potter CS, Carragher B, et al. Unnatural amino acid incorporation into virus-like particles. Bioconjug Chem 2008, 19:866-875.
142. Verma S, Eckstein F. Modified oligonucleotides: synthesis and strategy for users. Annu Rev Biochem 1998, 67:99-134.
143. Kay BK, Winter J, McCafferty J. Phage Display of Peptides and Proteins: a Laboratory Manual. San Diego: Academic Press; 1996.
144. Smith GP, Petrenko VA. Phage display. Chem Rev 1997, 97:391-410.
145. Rodi DJ, Makowski L. Phage-display technology - finding a needle in a vast molecular haystack. Curr Opin Biotechnol 1999, 10:87-93.
146. Kriplani U, Kay BK. Selecting peptides for use in nanoscale materials using phage-displayed combinatorial peptide libraries. Curr Opin Biotechnol 2005, 16:470-475.
147. Ellerby HM, Arap W, Ellerby LM, Kain R, Andrusiak R, Del Rio G, Krajewski S, Lombardo CR, Rao R, Ruoslahti E, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nature Med 1999, 5:1032-1038.
148. Kolonin MG, Saha PK, Chan L, Pasqualini R, Arap W. Reversal of obesity by targeted ablation of adipose tissue. Nature Med 2004, 10:625-632.
149. Sergeeva A, Kolonin MG, Molldrem JJ, Pasqualini R, Arap W. Display technologies: application for the discovery of drug and gene delivery agents. Adv Drug Deliv Rev 2006, 58:1622-1654.
150. Rothenfluh DA, Bermudez H, O'Neil CP, Hubbell JA. Biofunctional polymer nanoparticles for intra-articular targeting and retention in cartilage. Nat Mater 2008, 7:248-254.
151. 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.
152. 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.
153. Prasuhn DEJ, Singh P, Strable E, Brown S, Manchester M, Finn MG. Plasma clearance of bacteriophage Qbeta particles as a function of surface charge. J Am Chem Soc 2008, 130:1328-1334.
154. Ko S, Liu H, Chen Y, Mao C. DNA nanotubes as combinatorial vehicles for cellular delivery. Biomacromolecules 2008, 9:3039-3043.
155. Li H, LaBean TH, Kenan DJ. Single-chain antibodies against DNA aptamers for use as adapter molecules on DNA tile arrays in nanoscale materials organization. Organ Biomol Chem 2006, 4:3420-3426.
156. Chhabra R, Sharma J, Ke Y, Liu Y, Rinker S, Lindsay S, Yan H. Spatially addressable multiprotein nanoarrays templated by aptamer-tagged DNA nanoarchitectures. J Am Chem Soc 2007, 129:10304-10305.
157. Erben CM, Goodman RP, Turberfield AJ. Single-molecule protein encapsulation in a rigid DNA cage. Angew Chem Int Ed Engl 2006, 45:7414-7417.
158. Bhatia D, Mehtab S, Krishnan R, Indi SS, Basu A, Krishnan Y. Icosahedral DNA nanocapsules by modular assembly. Angew Chem Int Ed Engl 2009, 48:4134-4137.
159. Koyfman AY, Braun GB, Reich NO. Cell-targeted self-assembled DNA nanostructures. J Am Chem Soc 2009, 131:14237-14239.
160. Keum J-W, Bermudez H. Enhanced resistance of DNA nanostructures to enzymatic digestion. Chem Commun 2009, 7036-7038.
161. Lin D, Yurke B, Langrana N. Mechanical properties of a reversible, DNA-crosslinked polyacrylamide hydrogel. J Biomech Eng Trans ASME 2004, 126:104-110.
162. Um SH, Lee JB, Park N, Kwon SY, Umbach CC, Luo D. Enzyme-catalysed assembly of DNA hydrogel. Nat Mater 2006, 5:797-801.
163. Park N, Um SH, Funabashi H, Xu J, Luo D. A cell-free protein-producing gel. Nat Mater 2009, 8:432-437.
164. Keren K, Krueger M, Gilad R, Ben-Yoseph G, Sivan U, Braun E. Sequence-specific molecular lithography on single DNA molecules. Science 2002, 297:72-75.
165. Nam YS, Shin T, Park H, Magyar AP, Choi K, Fantner G, Nelson KA, Belcher AM. Virus-templated assembly of porphyrins into light-harvesting nanoantennae. J Am Chem Soc 2010, 132:1462.
166. Kershner RJ, Bozano LD, Micheel CM, Hung AM, Fornof AR, Cha JN, Rettner CT, Bersani M, Frommer J, Rothemund PWK, et al. Placement and orientation of individual DNA shapes on lithographically patterned surfaces. Nature Nanotechnol 2009, 4:557-561.
167. Crane HR. Problems and principles of biological growth. Sci Mon 1950, 70:376-389.