Cyclophilin A: An auxiliary but not necessary cofactor for TRIM5α restriction of HIV-1

Virology

Volumn 351, Issue 1, 2006, Pages 112-120

  Stremlau, Matthew ^a   Song, Byeongwoon ^a   Javanbakht, Hassan ^a   Perron, Michel ^a   Sodroski, Joseph ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Cyclophilin; Cyclosporine; Human immunodeficiency virus; Immunophilin; Rapamycin; Restriction factor; Retrovirus; TRIM5

Indexed keywords

CAPSID PROTEIN; CYCLOPHILIN A; CYCLOSPORIN A; PROTEIN; RAPAMYCIN; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA RESTRICTION; FUNCTIONAL PROTEOMICS; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INHIBITION KINETICS; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS ADSORPTION; VIRUS CAPSID; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; CARRIER PROTEINS; CELL LINE; CYCLOPHILIN A; CYCLOSPORINE; DOGS; GENE SILENCING; HAPLORHINI; HIV-1; HUMANS; IMMUNOSUPPRESSIVE AGENTS; PROTEIN BINDING; RNA, SMALL INTERFERING; TACROLIMUS; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 33745861280     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.03.015     Document Type: Article

References (54)

1. 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
2. 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. U.S.A. 102 41 (2005) 14849-14853
3. Besnier C., Takeuchi Y., and Towers G. Restriction of lentivirus in monkeys. Proc. Natl. Acad. Sci. U.S.A. 99 18 (2002) 11920-11925
4. Bieniasz P.D. Intrinsic immunity: a front-line defense against viral attack. Nat. Immunol. 5 11 (2004) 1109-1115
5. Bosco D.A., and Kern D. Catalysis and binding of cyclophilin A with different HIV-1 capsid constructs. Biochemistry 43 20 (2004) 6110-6119
6. 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. U.S.A. 99 8 (2002) 5247-5252
7. Braaten D., and Luban J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J. 20 6 (2001) 1300-1309
8. 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 8 (1996) 5170-5176
9. 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 6 (1996) 3551-3560
10. 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 7 (1996) 4220-4227
11. 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. U.S.A. 94 20 (1997) 10943-10948
12. Davies T.H., and Sanchez E.R. Fkbp52. Int. J. Biochem. Cell Biol. 37 1 (2005) 42-47
13. Fischer G., Bang H., and Mech C. Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides. Biomed. Biochim. Acta 43 10 (1984) 1101-1111
14. Fischer G., Wittmann-Liebold B., Lang K., Kiefhaber T., and Schmid F.X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337 6206 (1989) 476-478
15. 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 1 (1996) 279-282
16. Franke E.K., Yuan H.E., and Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372 6504 (1994) 359-362
17. Galat A. Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity-targets-functions. Curr. Top. Med. Chem. 3 12 (2003) 1315-1347
18. 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 7 (1996) 1285-1294
19. Gitti R.K., Lee B.M., Walker J., Summers M.F., Yoo S., and Sundquist W.I. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273 5272 (1996) 231-235
20. Goff S.P. Retrovirus restriction factors. Mol. Cell 16 6 (2004) 849-859
21. 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 3 (2003) 385-394
22. 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 11 (2004) 6005-6012
23. 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. U.S.A. 101 29 (2004) 10774-10779
24. 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 1 (2005) 176-183
25. 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 12 (1999) 10020-10028
26. Howard B.R., Vajdos F.F., Li S., Sundquist W.I., and Hill C.P. Structural insights into the catalytic mechanism of cyclophilin A. Nat. Struct. Biol. 10 6 (2003) 475-481
27. 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 29 (2005) 26933-26940
28. 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. U.S.A. 101 29 (2004) 10780-10785
29. 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. U.S.A. 100 3 (2003) 1298-1303
30. mac virus that expresses the HIV-1 envelope glycoproteins. J. Acquired Immune Defic. Syndr. 5 7 (1992) 639-646
31. 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 6 (1993) 1067-1078
32. 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. U.S.A. 99 21 (2002) 13843-13848
33. 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 14 (2005) 8870-8877
34. 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. U.S.A. 101 36 (2004) 13324-13328
35. 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 1 (2003) 726-731
36. 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 10 (2004) 5423-5437
37. 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 14 (2005) 8969-8978
38. 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. U.S.A. 101 32 (2004) 11827-11832
39. Saenz D.T., Teo W., Olsen J.C., and Poeschla E.M. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5{alpha} proteins. J. Virol. 79 24 (2005) 15175-15188
40. 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. U.S.A. 102 8 (2005) 2832-2837
41. 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 21 (2004) 12066-12070
42. Sayah D.M., Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430 6999 (2004) 569-573
43. Sokolskaja E., Sayah D.M., and Luban J. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J. Virol. 78 23 (2004) 12800-12808
44. 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 10 (2005) 6111-6121
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 7 (2005) 3930-3937
46. Stevens A., Bock M., Ellis S., LeTissier P., Bishop K.N., Yap M.W., Taylor W., and Stoye J.P. Retroviral capsid determinants of Fv1 NB and NR tropism. J. Virol. 78 18 (2004) 9592-9598
47. 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 6977 (2004) 848-853
48. Stremlau M., Perron M., Welikala S., and Sodroski J. Species-specific variation in the B30.2 (SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J. Virol. 79 5 (2005) 3139-3145
49. Stremlau, M., Perron, M., Lee, M., Yuan, L., Song, B., Javanbakht, H., Diaz-Griffero, F., Anderson, D., Sundquist, W., Sodroski, J., in press. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci U. S. A.
50. 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 6504 (1994) 363-365
51. Towers G., Bock M., Martin S., Takeuchi Y., Stoye J.P., and Danos O. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. U.S.A. 97 22 (2000) 12295-12299
52. 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 9 (2003) 1138-1143
53. 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. U.S.A. 101 29 (2004) 10786-10791
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 1 (2005) 73-78