A mutation in alpha helix 3 of CA renders human immunodeficiency virus type 1 cyclosporin A resistant and dependent: Rescue by a second-site substitution in a distal region of CA

Journal of Virology

Volumn 81, Issue 8, 2007, Pages 3749-3756

  Yang, Ruifeng ^a   Aiken, Christopher ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CAPSID PROTEIN; CYCLOPHILIN A; CYCLOSPORIN A; MUTANT PROTEIN; THREONINE;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; VIROGENESIS; VIRUS INFECTIVITY; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; CELL LINE; CYCLOSPORINE; DRUG RESISTANCE, VIRAL; HELA CELLS; HIV CORE PROTEIN P24; HIV-1; HUMANS; MUTATION; RNA INTERFERENCE; SUPPRESSION, GENETIC; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 34247135950     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02634-06     Document Type: Article

References (45)

1. Aberham, C., S. Weber, and W. Phares. 1996. Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J. Virol. 70:3536-3544.
2. Aiken, C. 1997. Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporine A. J. Virol. 71:5871-5877.
3. Aiken, C., and D. Trono. 1995. Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. J. Virol. 69:5048-5056.
4. Berthoux, L., S. Sebastian, E. Sokolskaja, and J. Luban. 2005. Cyclophilin A is required for TRIMSα-mediated resistance to HIV-1 in Old World monkey cells. Proc. Natl. Acad. Sci. USA 102:14849-14853.
5. Bosco, D. A., E. Z. Eisenmesser, S. Pochapsky, W. I. Sundquist, and D. Kern. 2002. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc. Natl. Acad. Sci. USA 99:5247-5252.
6. Braaten, D., C. Aberham, E. K. Franke, L. Yin, W. Phares, and J. Luban. 1996. Cyclosporin A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70:5170-5176.
7. Bukovsky, A. A., A. Weimann, M. A. Accola, and H. G. Gottlinger. 1997. Transfer of the HIV-1 cyclophilin-binding site to simian immunodeficiency virus from Macaca mulatta can confer both cyclosporin sensitivity and cyclosporin dependence. Proc. Natl. Acad. Sci. USA 94:10943-10948.
8. Butler, S. L., M. S. Hansen, and F. D. Bushman. 2001. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 7:631-634.
9. Campos-Olivas, R., and M. F. Summers. 1999. Backbone dynamics of the N-terminal domain of the HIV-1 capsid protein and comparison with the G94D mutant conferring cyclosporin resistance/dependence. Biochemistry 38:10262-10271.
10. Cavrois, M., C. De Noronha, and W. C. Greene. 2002. A sensitive and specific enzyme-based assay detecting HIV-1 virion fusion in primary T lymphocytes. Nat. Biotechnol. 20:1151-1154.
11. Chameau, P., M. Alizon, and F. Clavel. 1992. A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J. Virol. 66:2814-2820.
12. Chen, C., and H. Okayama. 1987. High-efficiency tranformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
13. Dismuke, D. J., and C. Aiken. 2006. Evidence for a functional link between uncoating of the human immunodeficiency virus type 1 core and nuclear import of the viral preintegration complex. J. Virol. 80:3712-3720.
14. Dorfman, T., A. Bukovsky, A. Ohagen, S. Hoglund, and H. G. Gottlinger. 1994. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68:8180-3187.
15. 2-terminal capsid domain: structure determinants for proper core assembly and subsequent steps of early replication. Virology 268:294-307.
16. Forshey, B. M., J. Shi, and C. Aiken. 2005. Structural requirements for recognition of the human immunodeficiency virus type 1 core during host restriction in owl monkey cells. J. Virol. 79:869-875.
17. Forshey, B. M., U. von Schwedler, W. I. Sundquist, and C. Aiken. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76:5667-5677.
18. Franke, E. K., H. E. H. Yuan, and J. Luban. 1994. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372:359-362.
19. Gamble, T. R., F. F. Vajdos, S. Yoo, D. K. Worthylake, M. Houseweart, W. I. Sundquist, and C. P. Hill. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-1294.
20. Gitti, R. K., B. M. Lee, J. Walker, M. F. Summers, S. Yoo, and W. I. Sundquist. 1996. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273:231-235.
21. Hatziioannou, T., D. Perez-Caballero, S. Cowan, and P. D. Bieniasz. 2005. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79:176-183.
22. He, J., Y. Chen, M. Farzan, H. Choe, A. Ohagen, S. Gartner, J. Busciglio, X. Yang, W. Hofmann, W. Newman, C. R. Mackay, J. Sodroski, and D. Gabuzda. 1997. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385:645-649.
23. Keckesova, Z., L. M. Ylinen, and G. J. Towers. 2006. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIMSα antiviral activity. J. Virol. 80:4683-4690.
24. Kotov, A., J. Zhou, P. Flicker, and C. Aiken. 1999. Association of Nef with the human immunodeficiency virus type 1 core. J. Virol. 73:8824-8830.
25. Li, S., C. P. Hill, W. I. Sundquist, and J. T. Finch. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407:409-413.
26. Luban, J. 1996. Absconding with the chaperone: essential cyclophilin-Gag interactions in HIV-1 virions. Cell 87:1157-1159.
27. Luban, J., K. L. Bossolt, E. K. Franke, G. V. Kalpana, and S. P. Goff. 1993. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73:1067-1078.
28. Mammano, F., A. Ohagen, S. Hoglund, and H. G. Gottlinger. 1994. Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J. Virol. 68:4927-4936.
29. Momany, C., L. C. Kovari, A. J. Prongay, W. Keller, R. K. Gitti, B. M. Lee, A. E. Gorbalenya, L. Tong, J. McClure, L. S. Ehrlich, M. F. Summers, C. Carter, and M. G. Rossmann. 1996. Crystal structure of dimeric HIV-1 capsid protein. Nat. Struct. Biol. 3:763-770.
30. Owens, C. M., B. Song, M. J. Perron, P. C. Yang, M. Stremlau, and J. Sodroski. 2004. Binding and susceptibility to postentry restriction factors in monkey cells are specified by distinct regions of the human immunodeficiency virus type 1 capsid. J. Virol. 78:5423-5437.
31. Reicin, A. S., A. Ohagen, L. Yin, S. Hoglund, and S. P. Goff. 1996. The role of Gag in human immunodeficiency virus type 1 virion morphogenesis and early steps of the viral life cycle. J. Virol. 70:8645-8652.
32. Sayah, D. M., and J. Luban. 2004. Selection for loss of Ref1 activity in human cells releases human immunodeficiency virus type 1 from cyclophilin A dependence during infection. J. Virol. 78:12066-12070.
33. Scholz, I., B. Arvidson, D. Huseby, and E. Barklis. 2005. Virus particle core defects caused by mutations in the human immunodeficiency virus capsid N-terminal domain. J. Virol. 79:1470-1479.
34. Sokolsloya, E., L. Berthoux, and J. Luban. 2006. Cyclophilin A and TRIM5α independently regulate human immunodeficiency virus type 1 infectivity in human cells. J. Virol. 80:2855-2862.
35. Sokolskaja, E., D. M. Sayah, and J. Luban. 2004. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J. Virol. 78:12800-12808.
36. Stremlau, M., B. Song, H. Javanbakht, M. Perron, and J. Sodroski. 2006. Cyclophilin A: an auxiliary but not necessary cofactor for TRIM5α restriction of HIV-1. Virology 351:112-120.
37. Tang, S., T. Murakami, B. E. Agresta, S. Campbell, E. O. Freed, and J. G. Levin. 2001. Human immunodeficiency virus type 1 N-terminal capsid mutants that exhibit aberrant core morphology and are blocked in initiation of reverse transcription in infected cells. J. Virol. 75:9357-9366.
38. Tang, S., T. Murakami, N. Cheng, A. C. Steven, E. O. Freed, and J. G. Levin. 2003. Human immunodeficiency virus type 1 N-terminal capsid mutants containing cores with abnormally high levels of capsid protein and virtually no reverse transcriptase. J. Virol. 77:12592-12602.
39. Thali, M., A. Bukovsky, E. Kondo, B. Rosenwirth, C. T. Walsh, J. Sodroski, and H. G. Gottlinger. 1994. Functional association of cyclophilin A with HIV-1 virions. Nature 372:363-365.
40. Towers, G. J., T. Hatziioannou, S. Cowan, S. P. Goff, J. Luban, and P. D. Bieniasz. 2003. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9:1138-1143.
41. von Schwedler, U. K., K. M. Stray, J. E. Garrus, and W. I. Sundquist. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
42. Wehrly, K., and B. Chesebro. 1997. p24 antigen capture assay for quantification of human immunodeficiency virus using readily available inexpensive reagents. Methods 12:288-293.
43. Wyma, D. J., J. Jiang, J. Shi, J. Zhou, J. E. Lineberger, M. D. Miller, and C. Aiken. 2004. Coupling of human immunodeficiency virus type 1 fusion to virion maturation: a novel role of the gp41 cytoplasmic tail. J. Virol. 78:3429-3435.
44. Yee, J. K., T. Friedmann, and J. C. Burns. 1994. Generation of high-titer pseudotyped retrovirus with very broad host range. Methods Cell Biol. 43:99-112.
45. Yin, L., D. Braaten, and J. Luban. 1998. Human immunodeficiency virus type 1 replication is modulated by host cyclophilin A expression levels. J. Virol. 72:6430-6436.