Cyclophilin, TRIM5, and innate immunity to HIV-1

Current Opinion in Microbiology

Volumn 9, Issue 4, 2006, Pages 404-408

  Sokolskaja, Elena ^a   Luban, Jeremy ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN; CYCLOPHILIN A; CYTOPLASMIC RECEPTOR; DOUBLE STRANDED RNA; LIPOPOLYSACCHARIDE; PROTEIN; PROTEIN FV1; TRIPARTITE MOTIF PROTEIN 5; UBIQUITIN; UNCLASSIFIED DRUG;

ENZYME REGULATION; HUMAN IMMUNODEFICIENCY VIRUS 1; INFECTION; INNATE IMMUNITY; NONHUMAN; RETROVIRUS; REVIEW; VIRUS REPLICATION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMALS; CAPSID; CARRIER PROTEINS; CYCLOPHILIN A; HIV-1; HUMANS; IMMUNITY, NATURAL; SPECIES SPECIFICITY; TROPISM; UBIQUITIN; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; PRIMATES;

EID: 33746270438     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2006.06.011     Document Type: Review

References (70)

1. Lilly F. Susceptibility to two strains of friend leukemia virus in mice. Science 155 (1967) 461-462
2. Best S., Le Tissier P., Towers G., and Stoye J.P. Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382 (1996) 826-829
3. Luban J., Bossolt K.L., Franke E.K., Kalpana G.V., and Goff S.P. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73 (1993) 1067-1078
4. Fischer G., Tradler T., and Zarnt T. The mode of action of peptidyl prolyl cis/trans isomerases in vivo: binding vs. catalysis. FEBS Lett 426 (1998) 17-20
5. Franke E.K., Yuan H.E., and Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372 (1994) 359-362
6. Gamble T.R., Vajdos F.F., Yoo S., Worthylake D.K., Houseweart M., Sundquist W.I., and Hill C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87 (1996) 1285-1294
7. Bosco D.A., Eisenmesser E.Z., Pochapsky S., Sundquist W.I., and Kern D. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc Natl Acad Sci USA 99 (2002) 5247-5252
8. Eisenmesser E.Z., Millet O., Labeikovsky W., Korzhnev D.M., Wolf-Watz M., Bosco D.A., Skalicky J.J., Kay L.E., and Kern D. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438 (2005) 117-121
9. Thali M., Bukovsky A., Kondo E., Rosenwirth B., Walsh C.T., Sodroski J., and Gottlinger H.G. Functional association of cyclophilin A with HIV-1 virions. Nature 372 (1994) 363-365
10. Braaten D., Aberham C., Franke E.K., Yin L., Phares W., and Luban J. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J Virol 70 (1996) 5170-5176
11. Braaten D., Franke E.K., and Luban J. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J Virol 70 (1996) 3551-3560
12. Franke E.K., and Luban J. Inhibition of HIV-1 replication by cyclosporine A or related compounds correlates with the ability to disrupt the Gag-cyclophilin A interaction. Virology 222 (1996) 279-282
13. Braaten D., and Luban J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J 20 (2001) 1300-1309
14. Sokolskaja E., Sayah D.M., and Luban J. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J Virol 78 (2004) 12800-12808
15. Hatziioannou T., Perez-Caballero D., Cowan S., and Bieniasz P.D. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J Virol 79 (2005) 176-183. Along with [14], this report presents formal demonstration that target cell CypA regulates HIV-1 infectivity. Producer cell CypA has no detectable effect on HIV-1 infectivity.
16. Sharp P.M., Shaw G.M., and Hahn B.H. Simian immunodeficiency virus infection of chimpanzees. J Virol 79 (2005) 3891-3902
17. Li J., Lord C.I., Haseltine W., Letvin N.L., and Sodroski J. Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus that expresses the HIV-1 envelope glycoproteins. J Acquir Immune Defic Syndr 5 (1992) 639-646
18. Shibata R., Kawamura M., Sakai H., Hayami M., Ishimoto A., and Adachi A. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J Virol 65 (1991) 3514-3520
19. Himathongkham S., and Luciw P.A. Restriction of HIV-1 (subtype B) replication at the entry step in rhesus macaque cells. Virology 219 (1996) 485-488
20. Balzarini J., De Clercq E., and Uberla K. SIV/HIV-1 hybrid virus expressing the reverse transcriptase gene of HIV-1 remains sensitive to HIV-1-specific reverse transcriptase inhibitors after passage in rhesus macaques. J Acquir Immune Defic Syndr Hum Retrovirol 15 (1997) 1-4
21. Hofmann W., Schubert D., LaBonte J., Munson L., Gibson S., Scammell J., Ferrigno P., and Sodroski J. Species-specific, postentry barriers to primate immunodeficiency virus infection. J Virol 73 (1999) 10020-10028
22. Besnier C., Takeuchi Y., and Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci USA 99 (2002) 11920-11925
23. Cowan S., Hatziioannou T., Cunningham T., Muesing M.A., Gottlinger H.G., and Bieniasz P.D. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 99 (2002) 11914-11919
24. Munk C., Brandt S.M., Lucero G., and Landau N.R. A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc Natl Acad Sci USA 99 (2002) 13843-13848
25. Braaten D., Franke E.K., and Luban J. Cyclophilin A is required for the replication of group M human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus SIV(CPZ)GAB but not group O HIV-1 or other primate immunodeficiency viruses. J Virol 70 (1996) 4220-4227
26. Shibata R., Sakai H., Kawamura M., Tokunaga K., and Adachi A. Early replication block of human immunodeficiency virus type 1 in monkey cells. J Gen Virol 76 (1995) 2723-2730
27. Hatziioannou T., Cowan S., Goff S.P., Bieniasz P.D., and Towers G.J. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J 22 (2003) 385-394
28. Towers G.J., Hatziioannou T., Cowan S., Goff S.P., Luban J., and Bieniasz P.D. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat Med 9 (2003) 1138-1143
29. Dorfman T., and Gottlinger H.G. The human immunodeficiency virus type 1 capsid p2 domain confers sensitivity to the cyclophilin-binding drug SDZ NIM 811. J Virol 70 (1996) 5751-5757
30. Bukovsky A.A., Weimann A., Accola M.A., and Gottlinger H.G. 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 (1997) 10943-10948
31. Owens C.M., Yang P.C., Gottlinger H., and Sodroski J. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J Virol 77 (2003) 726-731
32. Kootstra N.A., Munk C., Tonnu N., Landau N.R., and Verma I.M. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci USA 100 (2003) 1298-1303
33. Berthoux L., Sebastian S., Sokolskaja E., and Luban J. Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J Virol 78 (2004) 11739-11750
34. Hatziioannou T., Cowan S., Von Schwedler U.K., Sundquist W.I., and Bieniasz P.D. Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J Virol 78 (2004) 6005-6012
35. Owens C.M., Song B., Perron M.J., Yang P.C., Stremlau M., and Sodroski J. 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 (2004) 5423-5437
36. Ikeda Y., Ylinen L.M., Kahar-Bador M., and Towers G.J. Influence of Gag on human immunodeficiency virus type 1 species-specific tropism. J Virol 78 (2004) 11816-11822
37. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., and Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in old world monkeys. Nature 427 (2004) 848-853
38. Sayah D.M., Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430 (2004) 569-573
39. Berthoux L., Sebastian S., Sokolskaja E., and Luban J. Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in old world monkey cells. Proc Natl Acad Sci USA 102 (2005) 14849-14853
40. Yin L., Boussard S., Allan J., and Luban J. The HIV type 1 replication block in nonhuman primates is not explained by differences in cyclophilin A primary structure. AIDS Res Hum Retroviruses 14 (1998) 95-97
41. Hatziioannou T., Perez-Caballero D., Yang A., Cowan S., and Bieniasz P.D. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci USA 101 (2004) 10774-10779
42. Keckesova Z., Ylinen L.M., and Towers G.J. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci USA 101 (2004) 10780-10785
43. Perron M.J., Stremlau M., Song B., Ulm W., Mulligan R.C., and Sodroski J. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc Natl Acad Sci USA 101 (2004) 11827-11832
44. Yap M.W., Nisole S., Lynch C., and Stoye J.P. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci USA 101 (2004) 10786-10791
45. Song B., Javanbakht H., Perron M., Park D.H., Stremlau M., and Sodroski J. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J Virol 79 (2005) 3930-3937. Along with [41-44], this report extended the relevance of TRIM5α-mediated retroviral restriction activity to humans and non-human primates other than macaques. The different orthologues used in the above papers each had a particular specificity with respect to retroviral CA.
46. Ylinen L.M., Keckesova Z., Wilson S.J., Ranasinghe S., and Towers G.J. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol 79 (2005) 11580-11587
47. Nisole S., Lynch C., Stoye J.P., and Yap M.W. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc Natl Acad Sci USA 101 (2004) 13324-13328
48. Ribeiro I.P., Menezes A.N., Moreira M.A., Bonvicino C.R., Seuanez H.N., and Soares M.A. Evolution of cyclophilin A and TRIMCyp retrotransposition in New World primates. J Virol 79 (2005) 14998-15003
49. Berthoux L., Sebastian S., Sayah D.M., and Luban J. Disruption of human TRIM5alpha antiviral activity by nonhuman primate orthologues. J Virol 79 (2005) 7883-7888
50. Stremlau M., Perron M., Welikala S., and Sodroski J. Species-specific variation in the B30.2(SPRY) domain of TRIM5{alpha} determines the potency of human immunodeficiency virus restriction. J Virol 79 (2005) 3139-3145
51. Sawyer S.L., Wu L.I., Emerman M., and Malik H.S. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 102 (2005) 2832-2837
52. Song B., Gold B., O'Huigin C., Javanbakht H., Li X., Stremlau M., Winkler C., Dean M., and Sodroski J. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J Virol 79 (2005) 6111-6121
53. Perez-Caballero D., Hatziioannou T., Yang A., Cowan S., and Bieniasz P.D. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol 79 (2005) 8969-8978
54. Yap M.W., Nisole S., and Stoye J.P. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 15 (2005) 73-78
55. Nakayama E.E., Miyoshi H., Nagai Y., and Shioda T. A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5alpha determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J Virol 79 (2005) 8870-8877
56. •].
57. •] provide biochemical evidence that TRIM5α binds in a CA-specific manner to retroviral cores.
58. Colgan J., Yuan H.E., Franke E.K., and Luban J. Binding of the human immunodeficiency virus type 1 Gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires Gag dimerization. J Virol 70 (1996) 4299-4310
59. Bristow R., Byrne J., Squirell J., Trencher H., Carter T., Rodgers B., Saman E., and Duncan J. Human cyclophilin has a significantly higher affinity for HIV-1 recombinant p55 than p24. J Acquir Immune Defic Syndr Hum Retrovirol 20 (1999) 334-336
60. Mische C.C., Javanbakht H., Song B., Diaz-Griffero F., Stremlau M., Strack B., Si Z., and Sodroski J. Retroviral restriction factor TRIM5alpha is a trimer. J Virol 79 (2005) 14446-14450
61. Reymond A., Meroni G., Fantozzi A., Merla G., Cairo S., Luzi L., Riganelli D., Zanaria E., Messali S., Cainarca S., et al. The tripartite motif family identifies cell compartments. EMBO J 20 (2001) 2140-2151
62. Javanbakht H., Diaz-Griffero F., Stremlau M., Si Z., and Sodroski J. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J Biol Chem 280 (2005) 26933-26940
63. Xu L., Yang L., Moitra P.K., Hashimoto K., Rallabhandi P., Kaul S., Meroni G., Jensen J.P., Weissman A.M., and D'Arpa P. BTBD1 and BTBD2 colocalize to cytoplasmic bodies with the RBCC/tripartite motif protein, TRIM5delta. Exp Cell Res 288 (2003) 84-93
64. Diaz-Griffero F., Li X., Javanbakht H., Song B., Welikala S., Stremlau M., and Sodroski J. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 349 (2006) 300-315
65. Perez-Caballero D., Hatziioannou T., Zhang F., Cowan S., and Bieniasz P.D. Restriction of human immunodeficiency virus type 1 by TRIM-CypA occurs with rapid kinetics and independently of cytoplasmic bodies, ubiquitin, and proteasome activity. J Virol 79 (2005) 15567-15572
66. Butler S.L., Johnson E.P., and Bushman F.D. Human immunodeficiency virus cDNA metabolism: notable stability of two-long terminal repeat circles. J Virol 76 (2002) 3739-3747
67. Schwartz O., Marechal V., Friguet B., Arenzana-Seisdedos F., and Heard J.M. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J Virol 72 (1998) 3845-3850
68. Towers G., Collins M., and Takeuchi Y. Abrogation of Ref1 retrovirus restriction in human cells. J Virol 76 (2002) 2548-2550
69. Sayah D.M., and Luban J. Selection for loss of Ref1 activity in human cells releases human immunodeficiency virus type 1 from cyclophilin A dependence during infection. J Virol 78 (2004) 12066-12070
70. Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J Virol 80 (2006) 2855-2862