SCHEMA computational design of virus capsid chimeras: Calibrating how genome packaging, protection, and transduction correlate with calculated structural disruption

ACS Synthetic Biology

Volumn 2, Issue 12, 2013, Pages 724-733

  Ho, Michelle L ^a   Adler, Benjamin A ^a,b   Torre, Michael L ^a   Silberg, Jonathan J ^a,b   Suh, Junghae ^a  

^a Rice University   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

adeno associated virus; capsid; chimera; protein engineering; recombination; SCHEMA

Indexed keywords

CAPSID PROTEIN; HEPARIN;

ADENO ASSOCIATED VIRUS; ARTICLE; CHIMERA; HOMOLOGOUS RECOMBINATION; NANOBIOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; SEROTYPE; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY; ALGORITHM; BIOLOGY; CHEMISTRY; DEPENDOPARVOVIRUS; GENETIC RECOMBINATION; GENETICS; METABOLISM; PROCEDURES; PROTEIN ENGINEERING;

ALGORITHMS; CAPSID; CHIMERA; COMPUTATIONAL BIOLOGY; DEPENDOVIRUS; GENOME, VIRAL; HEPARIN; PROTEIN ENGINEERING; RECOMBINATION, GENETIC;

EID: 84890953395     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/sb400076r     Document Type: Article

References (53)

1. Negroni, M. and Buc, H. (2001) Mechanisms of retroviral recombination Annu. Rev. Genet. 35, 275-302
2. Martin, D. P., Biagini, P., Lefeuvre, P., Golden, M., Roumagnac, P., and Varsani, A. (2011) Recombination in eukaryotic single stranded DNA viruses Viruses 3, 1699-738
3. Gao, G., Alvira, M. R., Somanathan, S., Lu, Y., Vandenberghe, L. H., Rux, J. J., Calcedo, R., Sanmiguel, J., Abbas, Z., and Wilson, J. M. (2003) Adeno-associated viruses undergo substantial evolution in primates during natural infections Proc. Natl. Acad. Sci. U.S.A. 100, 6081-6
4. Lefeuvre, P., Lett, J.-M., Varsani, a, and Martin, D. P. (2009) Widely conserved recombination patterns among single-stranded DNA viruses J. Virol. 83, 2697-707
5. Lau, S. K. P., Woo, P. C. Y., Yip, C. C. Y., Li, K. S. M., Fu, C. T. Y., Huang, Y., Chan, K.-H., and Yuen, K.-Y. (2011) Co-existence of multiple strains of two novel porcine bocaviruses in the same pig, a previously undescribed phenomenon in members of the family Parvoviridae, and evidence for inter- and intra-host genetic diversity and recombination J. Gen. Virol. 92, 2047-59
6. Duffy, S., Shackelton, L. a, and Holmes, E. C. (2008) Rates of evolutionary change in viruses: Patterns and determinants Nat. Rev. Genet. 9, 267-76
7. Felsenstein, J. (1974) The evolutionary advantage of recombination Genetics 78, 737-56
8. Maheshri, N., Koerber, J. T., Kaspar, B. K., and Schaffer, D. V. (2006) Directed evolution of adeno-associated virus yields enhanced gene delivery vectors Nat. Biotechnol. 24, 198-204
9. Mateu, M. G. (2011) Virus engineering: Functionalization and stabilization Protein Eng., Des. Sel. 24, 53-63
10. Judd, J., Wei, F., Nguyen, P. Q., Tartaglia, L. J., Agbandje-McKenna, M., Silberg, J. J., and Suh, J. (2012) Random insertion of mCherry into VP3 domain of adeno-associated virus yields fluorescent capsids with no loss of infectivity Mol. Ther.-Nucleic acids 1, e54
11. Powell, S. K., Kaloss, M. a, Pinkstaff, a, McKee, R., Burimski, I., Pensiero, M., Otto, E., Stemmer, W. P., and Soong, N. W. (2000) Breeding of retroviruses by DNA shuffling for improved stability and processing yields Nat. Biotechnol. 18, 1279-82
12. Muzyczka, N. and Berns, K. I. (2001) Parvoviridae: The viruses and their replication, in Fields Virology (Knipe, D. M. and Howley, P. M., Eds.) 4 th ed., pp 2327-2360, Lippincott, Williams and Wilkins, New York.
13. Kotin, R. M. (1994) Prospects for the use of adeno-associated virus as a vector for human gene therapy Hum. Gene Ther. 5, 793-801
14. Daya, S. and Berns, K. I. (2008) Gene therapy using adeno-associated virus vectors Clin. Microbiol. Rev. 21, 583-93
15. Xie, Q., Bu, W., Bhatia, S., Hare, J., Somasundaram, T., Azzi, A., and Chapman, M. S. (2002) The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy Proc. Natl. Acad. Sci. U.S.A. 99, 10405-10
16. Padron, E., Bowman, V., Kaludov, N., Govindasamy, L., Levy, H., Nick, P., McKenna, R., Muzyczka, N., Chiorini, J. A., Baker, T. S., and Agbandje-McKenna, M. (2005) Structure of adeno-associated virus type 4 J. Virol. 79, 5047-58
17. Maguire, C. a, Gianni, D., Meijer, D. H., Shaket, L. a, Wakimoto, H., Rabkin, S. D., Gao, G., and Sena-Esteves, M. (2010) Directed evolution of adeno-associated virus for glioma cell transduction J. Neuro-Oncol. 96, 337-47
18. Yang, L., Jiang, J., Drouin, L. M., Agbandje-McKenna, M., Chen, C., Qiao, C., Pu, D., Hu, X., Wang, D.-Z., Li, J., and Xiao, X. (2009) A myocardium tropic adeno-associated virus (AAV) evolved by DNA shuffling and in vivo selection Proc. Natl. Acad. Sci. U.S.A. 106, 3946-51
19. Jang, J.-H., Koerber, J. T., Kim, J.-S., Asuri, P., Vazin, T., Bartel, M., Keung, A., Kwon, I., Park, K. I., and Schaffer, D. V. (2011) An evolved adeno-associated viral variant enhances gene delivery and gene targeting in neural stem cells Mol. Ther. 19, 667-75
20. Asuri, P., Bartel, M. a, Vazin, T., Jang, J.-H., Wong, T. B., and Schaffer, D. V. (2012) Directed evolution of adeno-associated virus for enhanced gene delivery and gene targeting in human pluripotent stem cells Mol. Ther. 20, 329-38
21. Bartel, M. a, Weinstein, J. R., and Schaffer, D. V. (2012) Directed evolution of novel adeno-associated viruses for therapeutic gene delivery Gene Ther. 19, 694-700
22. Carbone, M. N. and Arnold, F. H. (2007) Engineering by homologous recombination: Exploring sequence and function within a conserved fold Curr. Opin. Struct. Biol. 17, 454-9
23. Voigt, C. a, Martinez, C., Wang, Z.-G., Mayo, S. L., and Arnold, F. H. (2002) Protein building blocks preserved by recombination Nat. Struct. Biol. 9, 553-8
24. Meyer, M. M., Silberg, J. J., Voigt, C. A., Endelman, J. B., Mayo, S. L., Wang, Z., and Arnold, F. H. (2003) Library analysis of SCHEMA-guided protein recombination Protein Sci. 12, 1686-93
25. Landwehr, M., Carbone, M., Otey, C. R., Li, Y., and Arnold, F. H. (2007) Diversification of catalytic function in a synthetic family of chimeric cytochrome p450s Chem. Biol. 14, 269-78
26. Heinzelman, P., Snow, C. D., Wu, I., Nguyen, C., Villalobos, A., Govindarajan, S., Minshull, J., and Arnold, F. H. (2009) A family of thermostable fungal cellulases created by structure-guided recombination Proc. Natl. Acad. Sci. U.S.A. 106, 5610-5
27. Romero, P. a, Stone, E., Lamb, C., Chantranupong, L., Krause, A., Miklos, A., Hughes, R. a, Fechtel, B., Ellington, A. D., Arnold, F. H., and Georgiou, G. (2012) SCHEMA Designed Variants of Human Arginase I & II Reveal Sequence Elements Important to Stability and Catalysis ACS Synth. Biol. 1, 221-228
28. Meyer, M. M., Hochrein, L., and Arnold, F. H. (2006) Structure-guided SCHEMA recombination of distantly related beta-lactamases Protein Eng., Des. Sel. 19, 563-70
29. Govindasamy, L., Padron, E., McKenna, R., Muzyczka, N., Kaludov, N., Chiorini, J. a, and Agbandje-McKenna, M. (2006) Structurally mapping the diverse phenotype of adeno-associated virus serotype 4 J. Virol. 80, 11556-70
30. Otey, C. R., Landwehr, M., Endelman, J. B., Hiraga, K., Bloom, J. D., and Arnold, F. H. (2006) Structure-guided recombination creates an artificial family of cytochromes P450 PLoS Biol. 4, e112
31. Sonntag, F., Schmidt, K., and Kleinschmidt, J. A. (2010) A viral assembly factor promotes AAV2 capsid formation in the nucleolus Proc. Natl. Acad. Sci. U.S.A. 107, 10220-5
32. Ayuso, E., Mingozzi, F., and Bosch, F. (2010) Production, purification and characterization of adeno-associated vectors Curr. Gene Ther. 10, 423-36
33. Potter, M., Chesnut, K., Muzyczka, N., Flotte, T., and Zolotukhin, S. (2002) Streamlined large-scale production of recombinant adeno-associated virus (rAAV) vectors Methods Enzymol. 346, 413-30
34. Zolotukhin, S., Potter, M., Zolotukhin, I., Sakai, Y., Loiler, S., Fraites, T. J., Chiodo, V. a, Phillipsberg, T., Muzyczka, N., Hauswirth, W. W., Flotte, T. R., Byrne, B. J., and Snyder, R. O. (2002) Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors Methods (San Diego, Calif.) 28, 158-67
35. Zolotukhin, S., Byrne, B. J., Mason, E., Zolotukhin, I., Potter, M., Chesnut, K., Summerford, C., Samulski, R. J., and Muzyczka, N. (1999) Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield Gene Ther. 6, 973-85
36. Smith, R. H., Levy, J. R., and Kotin, R. M. (2009) A simplified baculovirus-AAV expression vector system coupled with one-step affinity purification yields high-titer rAAV stocks from insect cells Mol. Ther. 17, 1888-96
37. O'Donnell, J., Taylor, K. a, and Chapman, M. S. (2009) Adeno-associated virus-2 and its primary cellular receptor-Cryo-EM structure of a heparin complex Virology 385, 434-43
38. Opie, S. R., Warrington, K. H., Agbandje-McKenna, M., Zolotukhin, S., and Muzyczka, N. (2003) Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding J. Virol. 77, 6995-7006
39. Kaludov, N., Brown, K. E., Walters, R. W., Zabner, J., and Chiorini, J. A. (2001) Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity J. Virol. 75, 6884-93
40. Endelman, J. B., Silberg, J. J., Wang, Z.-G., and Arnold, F. H. (2004) Site-directed protein recombination as a shortest-path problem Protein Eng., Des. Sel. 17, 589-94
41. Li, Y., Drummond, D. A., Sawayama, A. M., Snow, C. D., Bloom, J. D., and Arnold, F. H. (2007) A diverse family of thermostable cytochrome P450s created by recombination of stabilizing fragments Nat. Biotechnol. 25, 1051-6
42. Otey, C. R., Silberg, J. J., Voigt, C. A., Endelman, J. B., Bandara, G., and Arnold, F. H. (2004) Functional Evolution and Structural Conservation in Chimeric Cytochromes P450: Calibrating a Structure-Guided Approach Biochemistry and Molecular Biophysics Option 11, 309-318
43. Drummond, D. A., Silberg, J. J., Meyer, M. M., Wilke, C. O., and Arnold, F. H. (2005) On the conservative nature of intragenic recombination Proc. Natl. Acad. Sci. U.S.A. 102, 5380-5
44. Naumer, M., Sonntag, F., Schmidt, K., Nieto, K., Panke, C., Davey, N. E., Popa-Wagner, R., and Kleinschmidt, J. a. (2012) Properties of the adeno-associated virus assembly-activating protein J. Virol. 86, 13038-48
45. Smith, M. a, Romero, P. a, Wu, T., Brustad, E. M., and Arnold, F. H. (2013) Chimeragenesis of distantly-related proteins by noncontiguous recombination Protein Sci. 22, 231-8
46. Doll, T. A. P. F., Raman, S., Dey, R., and Burkhard, P. (2013) Nanoscale assemblies and their biomedical applications J. R. Soc., Interface 10, 20120740
47. Liu, Z., Qiao, J., Niu, Z., and Wang, Q. (2012) Natural supramolecular building blocks: From virus coat proteins to viral nanoparticles Chem. Soc. Rev. 41, 6178-94
48. Steinmetz, N. F. (2010) Viral nanoparticles as platforms for next-generation therapeutics and imaging devices Nanomedicine: Nanotechnology, Biology, And Medicine 6, 634-41
49. Manchester, M. and Singh, P. (2006) Virus-based nanoparticles (VNPs): Platform technologies for diagnostic imaging Adv. Drug Delivery Rev. 58, 1505-22
50. Merzlyak, A. and Lee, S.-W. (2006) Phage as templates for hybrid materials and mediators for nanomaterial synthesis Curr. Opin. Chem. Biol. 10, 246-52
51. Gibson, D. G., Young, L., Chuang, R.-Y., Venter, J. C., Hutchison, C. A., and Smith, H. O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases Nat. Methods 6, 343-5
52. Xiao, X., Li, J., and Samulski, R. J. (1998) Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus J. Virol. 72, 2224-2232
53. Rabinowitz, J. E., Rolling, F., Li, C., Conrath, H., Xiao, W., Xiao, X., and Samulski, R. J. (2002) Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity J. Virol. 76, 791-801 Bioengineering