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 Chemistry

Volumn 22, Issue 1, 2011, Pages 58-66

  Zeng, Qingbing ^a,b   Saha, Sharmistha ^b   Lee, L Andrew ^b   Barnhill, Hannah ^b   Oxsher, Jerry ^b   Dreher, Theo ^c   Wang, Qian ^b  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CELL CULTURE; CELL ENGINEERING; CELLS; COPPER COMPOUNDS; CYCLOADDITION; DRUG DELIVERY; ETHYLENE; ETHYLENE GLYCOL; SURFACE CHEMISTRY; TISSUE ENGINEERING; VIRUSES;

3-DIPOLAR CYCLOADDITION; CELLS ADHESION; CHEMOSELECTIVE; DIPOLAR CYCLOADDITION REACTION; ITS APPLICATIONS; OLIGO(ETHYLENE GLYCOL); OLIGO(ETHYLENE GLYCOL) (OEGN); OLIGOETHYLENE GLYCOLS; PLANT VIRUS; TURNIP YELLOW MOSAIC VIRUS;

CELL ADHESION;

ALKYNE; ARGINYLGLYCYLASPARTIC ACID; AZIDE; COPPER ION; CYANAMIDE; GLASS; MACROGOL; TRIAZOLE DERIVATIVE;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL ADHESION; CELL GROWTH; CELL PROLIFERATION; CELL STRAIN 3T3; CELL STRUCTURE; CHEMICAL MODIFICATION; CONJUGATION; CYCLOADDITION; MOUSE; NONHUMAN; SURFACE PROPERTY; TURNIP YELLOW MOSAIC VIRUS; VIRUS PARTICLE;

BRASSICA RAPA SUBSP. PEKINENSIS; BRASSICA RAPA SUBSP. RAPA; TURNIP YELLOW MOSAIC VIRUS;

EID: 78751640028     PISSN: 10431802     EISSN: 15204812     Source Type: Journal    
DOI: 10.1021/bc100351n     Document Type: Article

References (66)

1. Niemeyer, C. M. (2001) Nanoparticles, proteins, and nucleic acids: biotechnology meets materials science Angew. Chem., Int. Ed. 40, 4128-4158
2. Vriezema, D. M., Comellas Aragonès, M., Elemans, J. A. A. W., Cornelissen, J. J. L. M., Rowan, A. E., and Nolte, R. J. M. (2005) Self-assembled nanoreactors Chem. Rev. 105, 1445-1490
3. Lee, L. A. and Wang, Q. (2006) Adaptations of nanoscale viruses and other protein cages for medical applications Nanomedicine 2, 137-49
4. Tu, R. S. and Tirrell, M. (2004) Bottom-up design of biomimetic assemblies Adv. Drug Delivery Rev. 56, 1537-63
5. Langer, R. and Tirrell, D. A. (2004) Designing materials for biology and medicine Nature 428, 487-492
6. Zhang, M., Desai, T., and Ferrari, M. (1998) Proteins and cells on PEG immobilized silicon surfaces Biomaterials 19, 953-960
7. Davis, D. H., Giannoulis, C. S., Johnson, R. W., and Desai, T. A. (2002) Immobilization of RGD to <111> silicon surfaces for enhanced cell adhesion and proliferation Biomaterials 23, 4019-4027
8. Duan, X., McLaughlin, C., Griffith, M., and Sheardown, H. (2007) Biofunctionalization of collagen for improved biological response: Scaffolds for corneal tissue engineering Biomaterials 28, 78-88
9. Wang, Q., Lin, T., Tang, L., Johnson, J. E., and Finn, M. G. (2002) Icosahedral virus particles as addressable nanoscale building blocks Angew. Chem., Int. Ed. 41, 459-462
10. Wang, Q., Kaltgrad, E., Lin, T., Johnson, J. E., and Finn, M. G. (2002) Natural supramolecular building blocks:: wild-type cowpea mosaic virus Chem. Biol. 9, 805-811
11. Wang, Q., Lin, T., Johnson, J. E., and Finn, M. G. (2002) Natural supramolecular building blocks:: cysteine-added mutants of cowpea mosaic virus Chem. Biol. 9, 813-819
12. Barnhill, H. N., Reuther, R., Ferguson, P. L., Dreher, T., and Wang, Q. (2007) Turnip yellow mosaic virus as a chemoaddressable bionanoparticle Bioconjugate Chem. 18, 852-859
13. Barnhill, H. N., Claudel-Gillet, S., Ziessel, R., Charbonnière, L. J., and Wang, Q. (2007) Prototype protein assembly as scaffold for time-resolved fluoroimmuno assays J. Am. Chem. Soc. 129, 7799-7806
14. Anderson, E. A., Isaacman, S., Peabody, D. S., Wang, E. Y., Canary, J. W., and Kirshenbaum, K. (2006) Viral nanoparticles donning a paramagnetic coat: conjugation of MRI contrast agents to the MS2 capsid Nano Lett. 6, 1160-1164
15. Gillitzer, E., Willits, D., Young, M., and Douglas, T. (2002) Chemical modification of a viral cage for multivalent presentation Chem. Commun. 2002, 2390-2391
16. Ren, Y., Wong, S. M., and Lim, L. Y. (2007) Folic acid-conjugated protein cages of a plant virus: A novel delivery platform for doxorubicin Bioconjugate Chem. 18, 836-843
17. Raja, K. S., Wang, Q., Gonzalez, M. J., Manchester, M., Johnson, J. E., and Finn, M. G. (2003) Hybrid virus-polymer materials. 1. Synthesis and properties of PEG-decorated cowpea mosaic virus Biomacromolecules 4, 472-476
18. Schlick, T. L., Ding, Z., Kovacs, E. W., and Francis, M. B. (2005) Dual-surface modification of the tobacco mosaic virus J. Am. Chem. Soc. 127, 3718-3723
19. ORiordan, C. R., Lachapelle, A., Delgado, C., Parkes, V., Wadsworth, S. C., Smith, A. E., and Francis, G. E. (1999) PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody in vitro and in vivo Hum. Gene Ther. 10, 1349-1358
20. Croyle, M. A., Yu, Q. C., and Wilson, J. M. (2000) Development of a rapid method for the PEGylation of adenoviruses with enhanced transduction and improved stability under harsh storage conditions Hum. Gene Ther. 11, 1713-1722
21. Raja, K. S., Wang, Q., and Finn, M. G. (2003) Icosahedral virus particles as polyvalent carbohydrate display platforms ChemBioChem 4, 1348-1351
22. Gupta, S. S., Raja, K. S., Kaltgrad, E., Strable, E., and Finn, M. G. (2005) Virus-glycopolymer conjugates by copper (i) catalysis of atom transfer radical polymerization and azide-alkyne cycloaddition Chem. Commun. 2005, 4315-4317
23. Strable, E., Johnson, J. E., and Finn, M. G. (2004) Natural nanochemical building blocks: icosahedral virus particles organized by attached oligonucleotides Nano Lett. 4, 1385-1389
24. Gupta, S. S., Kuzelka, J., Singh, P., Lewis, W. G., Manchester, M., and Finn, M. G. (2005) Accelerated bioorthogonal conjugation: a practical method for the ligation of diverse functional molecules to a polyvalent virus scaffold Bioconjugate Chem. 16, 1572-1579
25. Wang, Q., Chan, T. R., Hilgraf, R., Fokin, V. V., Sharpless, K. B., and Finn, M. G. (2003) Bioconjugation by copper (I)-catalyzed azide-alkyne [3 + 2] cycloaddition J. Am. Chem. Soc. 125, 3192-3193
26. Chatterji, A., Ochoa, W., Shamieh, L., Salakian, S. P., Wong, S. M., Clinton, G., Ghosh, P., Lin, T., and Johnson, J. E. (2004) Chemical conjugation of heterologous proteins on the surface of cowpea mosaic virus Bioconjugate Chem. 15, 807-813
27. Lewis, J. D., Destito, G., Zijlstra, A., Gonzalez, M. J., Quigley, J. P., Manchester, M., and Stuhlmann, H. (2006) Viral nanoparticles as tools for intravital vascular imaging Nat. Med. 12, 354-360
28. Allen, M., Bulte, J., Liepold, L., Basu, G., Zywicke, H. A., Frank, J. A., Young, M., and Douglas, T. (2005) Paramagnetic viral nanoparticles as potential high-relaxivity magnetic resonance contrast agents Magn. Reson. Med. 54, 807-812
29. Brown, W. L., Mastico, R. A., Wu, M., Heal, K. G., Adams, C. J., Murray, J. B., Simpson, J. C., Lord, J. M., Taylor-Robinson, A. W., and Stockley, P. G. (2000) RNA bacteriophage capsid-mediated drug delivery and epitope presentation Intervirology 45, 371-380
30. Pickett, G. G. and Peabody, D. S. (1993) Encapsidation of heterologous RNAs by bacteriophage MS2 coat protein Nucleic Acids Res. 21, 4621-4626
31. Hooker, J. M., Kovacs, E. W., and Francis, M. B. (2004) Interior surface modification of bacteriophage MS2 J. Am. Chem. Soc. 126, 3718-3719
32. Abbing, A., Blaschke, U. K., Grein, S., Kretschmar, M., Stark, C., Thies, M., Walter, J., Weigand, M., Woith, D. C., and Hess, J. (2004) Efficient intracellular delivery of a protein and a low molecular weight substance via recombinant polyomavirus-like particles J. Biol. Chem. 279, 27410-27421
33. Kang, S., Lander, G. C., Johnson, J. E., and Prevelige, P. E. (2008) Development of bacteriophage P22 as a platform for molecular display: genetic and chemical modifications of the procapsid exterior surface ChemBioChem 9, 514-518
34. Steinmetz, N. F., Bize, A., Findlay, K. C., Lomonossoff, G. P., Manchester, M., Evans, D. J., and Prangishvili, D. (2008) Site-specific and spatially controlled addressability of a new viral nanobuilding block: Sulfolobus islandicus rod-shaped virus 2 Adv. Funct. Mater. 18, 3478-3486
35. Kaur, G., Valarmathi, M. T., Potts, J. D., and Wang, Q. (2008) The promotion of osteoblastic differentiation of rat bone marrow stromal cells by a polyvalent plant mosaic virus Biomaterials 29, 4074-4081
36. Klug, A., Finch, J. T., and Franklin, R. E. (1957) Structure of turnip yellow mosaic virus Nature 179, 683-684
37. Canady, M. A., Larson, S. B., Day, J., and McPherson, A. (1996) Crystal structure of turnip yellow mosaic virus Nat. Struct. Mol. Biol. 3, 771-781
38. Reddy, V. S., Natarajan, P., Okerberg, B., Li, K., Damodaran, K. V., Morton, R. T., Brooks III, C. L., and Johnson, J. E. (2001) Virus particle explorer (VIPER), a website for virus capsid structures and their computational analyses J. Virol. 75, 11943-11947
39. van Roon, A., Bink, H., Plaisier, J. R., Pleij, C., Abrahams, J. P., and Pannu, N. S. (2004) Crystal structure of an empty capsid of turnip yellow mosaic virus J. Mol. Biol. 341, 1205-1214
40. Brenner, S. and Horne, R. W. (1959) A negative staining method for high resolution electron microscopy of viruses Biochim. Biophys. Acta 34, 103-110
41. Kaper, J. M. (1975) The chemical basis of virus structure, dissociation and reassembly, Frontiers of biology, pp 273 - 320, Vol 39, North-Holland/ American Elservier, Amsterdam, New York.
42. Leimkühler, M., Goldbeck, A., Lechner, M. D., Adrian, M., Michels, B., and Witz, J. (2001) The formation of empty shells upon pressure induced decapsidation of turnip yellow mosaic virus Arch. Virol. 146, 653-667
43. Katouzian-Safadi, M., Favre, A., and Haenni, A. L. (1980) Effect of freezing and thawing on the structure of turnip yellow mosaic virus Eur. J. Biochem. 112, 479-486
44. Kolb, H. C., Finn, M. G., and Sharpless, K. B. (2001) Click chemistry: diverse chemical function from a few good reactions Angew. Chem., Int. Ed. 40, 2004-2021
45. Hong, V., Presolski, S. I., Ma, C., and Finn, M. G. (2009) Analysis and optimization of copper-catalyzed azide-alkyne cycloaddition for bioconjugation Angew. Chem., Int. Ed. 48, 9879-9883
46. Rostovtsev, V. V., Green, L. G., Fokin, V. V., and Sharpless, K. B. (2002) A stepwise Huisgen cycloaddition process: copper (I)-catalyzed regioselective "ligation" of azides and terminal alkynes Angew. Chem., Int. Ed. 41, 2596-2599
47. Wu, P., Feldman, A. K., Nugent, A. K., Hawker, C. J., Scheel, A., Voit, B., Pyun, J., Fréchet, J., Sharpless, K. B., and Fokin, V. V. (2004) Efficiency and fidelity in a click-chemistry route to triazole dendrimers by the copper (I)-catalyzed ligation of azides and alkynes Angew. Chem., Int. Ed. 43, 3928-3932
48. Helms, B., Mynar, J. L., Hawker, C. J., and Frechet, J. (2004) Dendronized linear polymers via "click chemistry J. Am. Chem. Soc. 126, 15020-15021
49. Parrish, B., Breitenkamp, R. B., and Emrick, T. (2005) PEG-and peptide-grafted aliphatic polyesters by click chemistry J. Am. Chem. Soc. 127, 7404-7410
50. Link, A. J., Vink, M., and Tirrell, D. A. (2004) Presentation and detection of azide functionality in bacterial cell surface proteins J. Am. Chem. Soc. 126, 10598-10602
51. Bruckman, M. A., Kaur, G., Lee, L. A., Xie, F., Sepulveda, J., Breitenkamp, R., Zhang, X., Joralemon, M., Russell, T. P., Emrick, T., and Wang, Q. (2008) Surface modification of tobacco mosaic virus with "Click" chemistry ChemBioChem 9, 519-523
52. Steinmetz, N. F., Lomonossoff, G. P., and Evans, D. J. (2006) Cowpea mosaic virus for material fabrication: addressable carboxylate groups on a programmable nanoscaffold Langmuir 22, 3488-3490
53. Zeng, Q., Li, T., Cash, B., Li, S., Xie, F., and Wang, Q. (2007) Chemoselective derivatization of a bionanoparticle by click reaction and ATRP reaction Chem. Commun. 2007, 1453-1455
54. Sivakumar, K., Xie, F., Cash, B. M., Long, S., Barnhill, H. N., and Wang, Q. (2004) A fluorogenic 1,3-dipolar cycloaddition reaction of 3-azidocoumarins and acetylenes Org. Lett. 6, 4603-4606
55. Yamada, K., Yoshii, S., Kumagai, S., Fujiwara, I., Nishio, K., Okuda, M., Matsukawa, N., and Yamashita, I. (2006) High-density and highly surface selective adsorption of protein-nanoparticle complexes by controlling electrostatic interaction Jpn. J. Appl. Phys. 45, 4259-4264
56. Shu, X. Z., Ghosh, K., Liu, Y., Palumbo, F. S., Luo, Y., Clark, R. A., and Prestwich, G. D. (2004) Attachment and spreading of fibroblasts on an RGD peptide-modified injectable hyaluronan hydrogel J. Biomed. Mater. Res., Part A 68, 365-375
57. Desai, N. P. and Hubbell, J. A. (1991) Biological responses to polyethylene oxide modified polyethylene terephthalate surfaces J. Biomed. Mater. Res. 25, 829-843
58. Griffith, L. G. (2000) Polymeric biomaterials Acta Mater. 48, 263-277
59. Pierschbacher, M. D., Hayman, E. G., and Ruoslahti, E. (1985) The cell attachment determinant in fibronectin J. Cell. Biochem. 28, 115-126
60. Humphries, M. J. (1990) The molecular basis and specificity of integrin-ligand interactions J. Cell Sci. 97, 585-592
61. Benoit, D. and Anseth, K. S. (2005) The effect on osteoblast function of colocalized RGD and PHSRN epitopes on PEG surfaces Biomaterials 26, 5209-5220
62. Dee, K. C., Andersen, T. T., and Bizios, R. (1999) Osteoblast population migration characteristics on substrates modified with immobilized adhesive peptides Biomaterials 20, 221-227
63. Hern, D. L. and Hubbell, J. A. (1998) Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing J. Biomed. Mater. Res., Part A 39, 266-276
64. Burdick, J. A. and Anseth, K. S. (2002) Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering Biomaterials 23, 4315-4323
65. Rhee, S. and Grinnell, F. (2007) Fibroblast mechanics in 3D collagen matrices Adv. Drug Delivery Rev. 59, 1299-1305
66. Nilsson, K. and Mosbach, K. (1981) Immobilization of enzymes and affinity ligands to various hydroxyl group carrying supports using highly reactive sulfonyl chlorides Biochem. Biophys. Res. Commun. 102, 449-457