Cyclophilin A renders human immunodeficiency virus type 1 sensitive to old world monkey but not human TRIM5α antiviral activity

Journal of Virology

Volumn 80, Issue 10, 2006, Pages 4683-4690

  Keckesova, Zuzana ^a   Ylinen, Laura M J ^a   Towers, Greg J ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; PROLINE; PROTEIN; SMALL INTERFERING RNA; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG;

ADAPTATION; ANTIVIRAL ACTIVITY; ARTICLE; CERCOPITHECIDAE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INNATE IMMUNITY; ISOMERIZATION; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRION; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS REPLICATION;

ANIMALS; ANTI-HIV AGENTS; CARRIER PROTEINS; CATS; CELL LINE; CERCOPITHECIDAE; CYCLOPHILIN A; CYCLOSPORINE; DRUG RESISTANCE, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; LEUKEMIA VIRUS, MURINE; SIMIAN IMMUNODEFICIENCY VIRUS;

AOTUS TRIVIRGATUS; CERCOPITHECIDAE; CERCOPITHECUS AETHIOPS; FELIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; MIRIDAE; SIMIAE;

EID: 33646457944     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.10.4683-4690.2006     Document Type: Article

References (52)

1. Avela, K., M. Lipsanen-Nyman, N. Idanheimo, E. Seemanova, S. Rosengren, T. P. Makela, J. Perheentupa, A. D. Chapelle, and A. E. Lehesjoki. 2000. Gene encoding a new RING-B-box-coiled-coil protein is mutated in mulibrey nanism. Nat. Genet. 25:298-301.
2. Berthoux, L., S. Sebastian, E. Sokolskaja, and J. Luban. 2005. Cyclophilin A is required for TRIM5α-mediated resistance to HIV-1 in Old World monkey cells. Proc. Natl. Acad. Sci. USA 102:14849-14853.
3. Berthoux, L., S. Sebastian, E. Sokolskaja, and J. Luban. 2004. Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J. Virol. 78:11739-11750.
4. Besnier, C., Y. Takeuchi, and G. Towers. 2002. Restriction of lentivirus in monkeys. Proc. Natl. Acad. Sci. USA 99:11920-11925.
5. Bock, M., K. Bishop, G. Towers, and J. P. Stoye. 2000. Use of a transient assay for studying the genetic determinants of Fv1 restriction. J. Virol. 74:7422-7430.
6. 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.
7. Bosco, D. A., and D. Kern. 2004. Catalysis and binding of cyclophilin A with different HIV-1 capsid constructs. Biochemistry 43:6110-6119.
8. Braaten, D., C. Aberham, E. K. Franke, L. Yin, W. Phares, and J. Luban. 1996. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70:5170-5176.
9. CPZGAB but not group O HIV-1 or other primate immunodeficiency viruses. J. Virol. 70:4220-4227.
10. Brazin, K. N., R. J. Mallis, D. B. Fulton, and A. H. Andreotti. 2002. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc. Natl. Acad. Sci. USA 99:1899-1904.
11. Chatterji, U., M. D. Bobardt, R. Stanfield, R. G. Ptak, L. A. Pallansch, P. A. Ward, M. J. Jones, C. A. Stoddart, P. Scalfaro, J. M. Dumont, K. Besseghir, B. Rosenwirth, and P. A. Gallay. 2005. Naturally occurring capsid substitutions render HIV-1 cyclophilin A independent in human cells and TRIM-cyclophilin-resistant in Owl monkey cells. J. Biol. Chem. 280:40293-40300.
12. Coaker, G., A. Falick, and B. Staskawicz. 2005. Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548-550.
13. + T cells via a proline-directed conformational switch in Itk. Immunity 21:189-201.
14. Damaso, C. R., and N. Moussatche. 1998. Inhibition of vaccinia virus replication by cyclosporin A analogues correlates with their affinity for cellular cyclophilins. J. Gen. Virol. 79:339-346.
15. Franke, E. K., H. E. Yuan, and J. Luban. 1994. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372:359-362.
16. Gao, F., E. Bailes, D. L. Robertson, Y. Chen, C. Rodenburg, S. F. Michael, L. B. Cummins, L. O. Arthur, M. Peeters, G. M. Shaw, and B. H. Hahn. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes. Nature 397:436-441.
17. Geiss, G. K., M. Salvatore, T. M. Tumpey, V. S. Carter, X. Wang, C. F. Basler, J. K. Taubenberger, R. E. Bumgarner, P. Palese, M. G. Katze, and A. Garcia-Sastre. 2002. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc. Natl. Acad. Sci. USA 99:10736-10741.
18. Hatziioannou, T., S. Cowan, S. P. Goff, P. D. Bieniasz, and G. J. Towers. 2003. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 22:1-10.
19. Hatziioannou, T., S. Cowan, U. K. Von Schwedler, W. I. Sundquist, and P. D. Bieniasz. 2004. Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J. Virol. 78:6005-6012.
20. 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.
21. Hatziioannou, T., D. Perez-Caballero, A. Yang, S. Cowan, and P. D. Bieniasz. 2004. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. USA 101:10774-10779.
22. Heitman, J., and B. R. Cullen. 2005. Cyclophilin B escorts the hepatitis C virus RNA polymerase: a viral aehilles heel? Mol. Cell 19:145-146.
23. Hofmann, W., D. Schubert, J. LaBonte, L. Munson, S. Gibson, J. Scammell, P. Ferrigno, and J. Sodroski. 1999. Species-specific, postentry barriers to primate immunodeficiency virus infection. J. Virol. 73:10020-10028.
24. Ikeda, Y., L. Ylinen, M. Kahar-Bador, and G. J. Towers. 2004. The influence of gag on HIV-1 species specific tropism. J. Virol. 78:11816-11822.
25. Keckesova, Z., L. M. Ylinen, and G. J. Towers. 2004. The human and African green monkey TRIM5α genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc. Natl. Acad. Sci. USA 101:10780-10785.
26. Kootstra, N. A., C. Munk, N. Tonnu, N. R. Landau, and I. M. Verma. 2003. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. USA 100:1298-1303.
27. Liu, J., J. D. Farmer, Jr., W. S. Lane, J. Friedman, I. Weissman, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807-815.
28. Mallis, R. J., K. N. Brazin, D. B. Fulton, and A. H. Andreotti. 2002. Structural characterization of a proline-driven conformational switch within the Itk SH2 domain. Nat. Struct. Biol 9:900-905.
29. Nakayama, E. E., H. Miyoshi, Y. Nagai, and T. Shioda. 2005. A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5α determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J. Virol. 79:8870-8877.
30. Nisole, S., C. Lynch, J. P. Stoye, and M. W. Yap. 2004. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. USA 101:13324-13328.
31. Passerini, L. D., Z. Keckesova, and G. J. Towers. 2006. Retroviral restriction factors Fv1 and TRIM5α act independently and can compete for incoming virus before reverse transcription. J. Virol. 80:2100-2105.
32. Perez-Caballero, D., T. Hatziioannou, A. Yang, S. Cowan, and P. D. Bieniasz. 2005. Human tripartite motif 5α domains responsible for retrovirus restriction activity and specificity. J. Virol. 79:8969-8978.
33. Perron, M. J., M. Stremlau, B. Song, W. Ulm, R. C. Mulligan, and J. Sodroski. 2004. TRIM5α mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc. Natl. Acad. Sci. USA 101:11827-11832.
34. Quaderi, N. A., S. Schweiger, K. Gaudenz, B. Franco, E. I. Rugarli, W. Berger, G. J. Feldman, M. Volta, G. Andolfi, S. Gilgenkrantz, R. W. Marion, R. C. Hennekam, J. M. Opitz, M. Muenke, H. H. Ropers, and A. Ballabio. 1997. Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat. Genet. 17:285-291.
35. Reymond, A., G. Meroni, A. Fantozzi, G. Merla, S. Cairo, L. Luzi, D. Riganelli, E. Zanaria, S. Messali, S. Cainarca, A. Guffanti, S. Minucci, P. G. Pelicci, and A. Ballabio. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20:2140-2151.
36. Sayah, D. M., E. Sokolskaja, L. Berthoux, and J. Luban. 2004. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430:569-573.
37. Sebastian, S., and J. Luban. 2005. TRIM5α selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2:40.
38. Sharp, P. M., G. M. Shaw, and B. H. Hahn. 2005. Simian immunodeficiency virus infection of chimpanzees. J. Virol. 79:3891-3902.
39. 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.
40. Song, B., B. Gold, C. O'Huigin, H. Javanbakht, X. Li, M. Stremlau, C. Winkler, M. Dean, and J. Sodroski. 2005. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5α exhibits lineage-specific length and sequence variation in primates. J. Virol. 79:6111-6121.
41. Stremlau, M., C. M. Owens, M. J. Perron, M. Kiessling, P. Autissier, and J. Sodroski. 2004. The cytoplasmic body component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427:848-853.
42. Stremlau, M., M. J. Perron, S. Welikala, and J. Sodroski. 2005. Species-specific variation in the B30.2(SPRY) domain of TRIM5α determines the potency of human immunodeficiency virus restriction. J. Virol. 79:3139-3145.
43. 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.
44. Towers, G., M. Bock, S. Martin, Y. Takeuchi, J. P. Stoye, and O. Danos. 2000. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. USA 97:12295-12299.
45. 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.
46. Watashi, K., N. Ishii, M. Hijikata, D. Inoue, T. Murata, Y. Miyanari, and K. Shimotohno. 2005. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol. Cell 19:111-122.
47. Weigers, K., and H. G. Krausslich. 2002. Differential dependence of the infectivity of HIV-1 group O isolates on the cellular protein cyclophilin A. Virology 294:289-295.
48. Yap, M. W., S. Nisole, C. Lynch, and J. P. Stoye. 2004. Trim5α protein restricts both HIV-1 and murine leukemia virus. Proc. Natl. Acad. Sci. USA 101:10786-10791.
49. Yap, M. W., S. Nisole, and J. P. Stoye. 2005. A single amino acid change in the SPRY domain of human Trim5α leads to HIV-1 restriction. Curr. Biol. 15:73-78.
50. 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.
51. Ylinen, L., Z. Keckesova, S. J. Wilson, S. Ranasinghe, and G. J. Towers. 2005. Differential restriction of HIV-2 and SIVmac by TRIM5α alleles. J. Virol. 79:11580-11587.
52. Zufferey, R., D. Nagy, R. J. Mandel, L. Naldini, and D. Trono. 1997. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15:871-875.