Host cell species-specific effect of cyclosporine A on simian immunodeficiency virus replication

Retrovirology

Volumn 9, Issue , 2012, Pages

  Takeuchi, Hiroaki ^a   Ishii, Hiroshi ^b,c   Kuwano, Tetsuya ^b   Inagaki, Natsuko ^b   Akari, Hirofumi ^d   Matano, Tetsuro ^b,c  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Cyclophilin A; Cyclophilin B; Cyclosporine A; HIV 1; SIV; Tropism

Indexed keywords

CYCLOSPORIN A; ANTIVIRUS AGENT; CYCLOPHILIN A; CYCLOSPORIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA; NONHUMAN; NUCLEOTIDE SEQUENCE; SIMIAN IMMUNODEFICIENCY VIRUS; SPECIES DIFFERENCE; T LYMPHOCYTE; VIRAL TROPISM; VIRUS REPLICATION; ANIMAL; CELL CULTURE; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTIVIRAL AGENTS; CELLS, CULTURED; CYCLOPHILIN A; CYCLOSPORINE; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES;

EID: 84855422768     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-3     Document Type: Article

References (55)

1. Gautsch JW, Elder JH, Schindler J, Jensen FC, Lerner RA. Structural markers on core protein p30 of murine leukemia virus: functional correlation with Fv-1 tropism. Proc Natl Acad Sci USA 1978, 75:4170-4174. 10.1073/pnas.75.9.4170, 336073, 212738.
2. Rein A, Kashmiri SV, Bassin RH, Gerwin BL, Duran-Troise G. Phenotypic mixing between N- and B-tropic murine leukemia viruses: infectious particles with dual sensitivity to Fv-1 restriction. Cell 1976, 7:373-379. 10.1016/0092-8674(76)90166-5, 181144.
3. Towers G, Bock M, Martin S, Takeuchi Y, Stoye JP, Danos O. A conserved mechanism of retrovirus restriction in mammals. Proc Natl Acad Sci USA 2000, 97:12295-12299. 10.1073/pnas.200286297, 17335, 11027299.
4. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853. 10.1038/nature02343, 14985764.
5. Keckesova Z, Ylinen LM, Towers GJ. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci USA 2004, 101:10780-10785. 10.1073/pnas.0402474101, 490011, 15249687.
6. Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J Virol 2005, 79:3930-3937. 10.1128/JVI.79.7.3930-3937.2005, 1061569, 15767395.
7. Yap MW, Nisole S, Lynch C, Stoye JP. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci USA 2004, 101:10786-10791. 10.1073/pnas.0402876101, 490012, 15249690.
8. Ylinen LM, Keckesova Z, Wilson SJ, Ranasinghe S, Towers GJ. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol 2005, 79:11580-11587. 10.1128/JVI.79.18.11580-11587.2005, 1212619, 16140735.
9. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci USA 2004, 101:10774-10779. 10.1073/pnas.0402361101, 490010, 15249685.
10. Goff SP. Genetic control of retrovirus susceptibility in mammalian cells. Annu Rev Genet 2004, 38:61-85. 10.1146/annurev.genet.38.072902.094136, 15568972.
11. Kozak CA, Chakraborti A. Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance. Virology 1996, 225:300-305. 10.1006/viro.1996.0604, 8918916.
12. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006, 103:5514-5519. 10.1073/pnas.0509996103, 1459386, 16540544.
13. Thali M, Bukovsky A, Kondo E, Rosenwirth B, Walsh CT, Sodroski J, Gottlinger HG. Functional association of cyclophilin A with HIV-1 virions. Nature 1994, 372:363-365. 10.1038/372363a0, 7969495.
14. Franke EK, Yuan HE, Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 1994, 372:359-362. 10.1038/372359a0, 7969494.
15. Towers GJ, Hatziioannou T, Cowan S, Goff SP, Luban J, Bieniasz PD. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat Med 2003, 9:1138-1143. 10.1038/nm910, 12897779.
16. Braaten D, Luban J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. Embo J 2001, 20:1300-1309. 10.1093/emboj/20.6.1300, 145517, 11250896.
17. Braaten D, Franke EK, 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 1996, 70:4220-4227. 190352, 8676442.
18. Franke EK, 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 1996, 222:279-282. 10.1006/viro.1996.0421, 8806510.
19. Hatziioannou T, Perez-Caballero D, Cowan S, Bieniasz PD. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J Virol 2005, 79:176-183. 10.1128/JVI.79.1.176-183.2005, 538701, 15596813.
20. Braaten D, Franke EK, 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 1996, 70:3551-3560. 190230, 8648689.
21. Braaten D, Aberham C, Franke EK, Yin L, Phares W, Luban J. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J Virol 1996, 70:5170-5176. 190472, 8764025.
22. Ott DE, Coren LV, Johnson DG, Sowder RC, Arthur LO, Henderson LE. Analysis and localization of cyclophilin A found in the virions of human immunodeficiency virus type 1 MN strain. AIDS Res Hum Retroviruses 1995, 11:1003-1006. 10.1089/aid.1995.11.1003, 8554896.
23. Ackerson B, Rey O, Canon J, Krogstad P. Cells with high cyclophilin A content support replication of human immunodeficiency virus type 1 Gag mutants with decreased ability to incorporate cyclophilin A. J Virol 1998, 72:303-308. 109377, 9420228.
24. Bukovsky AA, Weimann A, Accola MA, Gottlinger HG. 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 1997, 94:10943-10948. 10.1073/pnas.94.20.10943, 23539, 9380739.
25. Sokolskaja E, Sayah DM, Luban J. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J Virol 2004, 78:12800-12808. 10.1128/JVI.78.23.12800-12808.2004, 524981, 15542632.
26. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci USA 2003, 100:1298-1303. 10.1073/pnas.0337541100, 298767, 12547912.
27. Takeuchi H, Buckler-White A, Goila-Gaur R, Miyagi E, Khan MA, Opi S, Kao S, Sokolskaja E, Pertel T, Luban J, Strebel K. Vif counteracts a cyclophilin A-imposed inhibition of simian immunodeficiency viruses in human cells. J Virol 2007, 81:8080-8090. 10.1128/JVI.02727-06, 1951326, 17522232.
28. Keckesova Z, Ylinen LM, Towers GJ. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J Virol 2006, 80:4683-4690. 10.1128/JVI.80.10.4683-4690.2006, 1472055, 16641261.
29. Ikeda Y, Ylinen LM, Kahar-Bador M, Towers GJ. Influence of gag on human immunodeficiency virus type 1 species-specific tropism. J Virol 2004, 78:11816-11822. 10.1128/JVI.78.21.11816-11822.2004, 523279, 15479823.
30. Sokolskaja E, Olivari S, Zufferey M, Strambio-De-Castillia C, Pizzato M, Luban J. Cyclosporine blocks incorporation of HIV-1 envelope glycoprotein into virions. J Virol 2010, 84:4851-4855. 10.1128/JVI.01699-09, 2863729, 20181694.
31. Berthoux L, Sebastian S, Sokolskaja E, Luban J. Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells. Proc Natl Acad Sci USA 2005, 102:14849-14853. 10.1073/pnas.0505659102, 1239943, 16203999.
32. Stremlau M, Song B, Javanbakht H, Perron M, Sodroski J. Cyclophilin A: an auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 2006, 351:112-120. 10.1016/j.virol.2006.03.015, 16643975.
33. Noser JA, Towers GJ, Sakuma R, Dumont JM, Collins MK, Ikeda Y. Cyclosporine increases human immunodeficiency virus type 1 vector transduction of primary mouse cells. J Virol 2006, 80:7769-7774. 10.1128/JVI.02427-05, 1563702, 16840358.
34. Lin TY, Emerman M. Cyclophilin A interacts with diverse lentiviral capsids. Retrovirology 2006, 3:70. 10.1186/1742-4690-3-70, 1622752, 17038183.
35. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 1993, 73:1067-1078. 10.1016/0092-8674(93)90637-6, 8513493.
36. Bram RJ, Hung DT, Martin PK, Schreiber SL, Crabtree GR. Identification of the immunophilins capable of mediating inhibition of signal transduction by cyclosporin A and FK506: roles of calcineurin binding and cellular location. Mol Cell Biol 1993, 13:4760-4769. 360102, 7687744.
37. Hanoulle X, Melchior A, Sibille N, Parent B, Denys A, Wieruszeski JM, Horvath D, Allain F, Lippens G, Landrieu I. Structural and functional characterization of the interaction between cyclophilin B and a heparin-derived oligosaccharide. J Biol Chem 2007, 282:34148-34158. 10.1074/jbc.M706353200, 17855358.
38. Pakula R, Melchior A, Denys A, Vanpouille C, Mazurier J, Allain F. Syndecan-1/CD147 association is essential for cyclophilin B-induced activation of p44/42 mitogen-activated protein kinases and promotion of cell adhesion and chemotaxis. Glycobiology 2007, 17:492-503.
39. Vanpouille C, Deligny A, Delehedde M, Denys A, Melchior A, Lienard X, Lyon M, Mazurier J, Fernig DG, Allain F. The heparin/heparan sulfate sequence that interacts with cyclophilin B contains a 3-O-sulfated N-unsubstituted glucosamine residue. J Biol Chem 2007, 282:24416-24429. 10.1074/jbc.M701835200, 17588944.
40. Price ER, Zydowsky LD, Jin MJ, Baker CH, McKeon FD, Walsh CT. Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc Natl Acad Sci USA 1991, 88:1903-1907. 10.1073/pnas.88.5.1903, 51134, 2000394.
41. Misumi S, Fuchigami T, Takamune N, Takahashi I, Takama M, Shoji S. Three isoforms of cyclophilin A associated with human immunodeficiency virus type 1 were found by proteomics by using two-dimensional gel electrophoresis and matrix-assisted laser desorption ionization-time of flight mass spectrometry. J Virol 2002, 76:10000-10008. 10.1128/JVI.76.19.10000-10008.2002, 136499, 12208976.
42. Lammers M, Neumann H, Chin JW, James LC. Acetylation regulates cyclophilin A catalysis, immunosuppression and HIV isomerization. Nat Chem Biol 2010, 6:331-337.
43. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, Towers GJ. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc Natl Acad Sci USA 2008, 105:3557-3562. 10.1073/pnas.0709003105, 2265179, 18287035.
44. Sayah DM, Sokolskaja E, Berthoux L, Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004, 430:569-573. 10.1038/nature02777, 15243629.
45. Nisole S, Lynch C, Stoye JP, Yap MW. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc Natl Acad Sci USA 2004, 101:13324-13328. 10.1073/pnas.0404640101, 516566, 15326303.
46. Virgen CA, Kratovac Z, Bieniasz PD, Hatziioannou T. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci USA 2008, 105:3563-3568. 10.1073/pnas.0709258105, 2265128, 18287034.
47. Brennan G, Kozyrev Y, Hu SL. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci USA 2008, 105:3569-3574. 10.1073/pnas.0709511105, 2265124, 18287033.
48. Akari H, Mori K, Terao K, Otani I, Fukasawa M, Mukai R, Yoshikawa Y. In vitro immortalization of Old World monkey T lymphocytes with Herpesvirus saimiri: its susceptibility to infection with simian immunodeficiency viruses. Virology 1996, 218:382-388. 10.1006/viro.1996.0207, 8610465.
49. Hirsch VM, Dapolito G, Johnson PR, Elkins WR, London WT, Montali RJ, Goldstein S, Brown C. Induction of AIDS by simian immunodeficiency virus from an African green monkey: species-specific variation in pathogenicity correlates with the extent of in vivo replication. J Virol 1995, 69:955-967. 188664, 7815563.
50. Regier DA, Desrosiers RC. The complete nucleotide sequence of a pathogenic molecular clone of simian immunodeficiency virus. AIDS Res Hum Retroviruses 1990, 6:1221-1231.
51. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 1986, 59:284-291. 253077, 3016298.
52. Willey RL, Smith DH, Lasky LA, Theodore TS, Earl PL, Moss B, Capon DJ, Martin MA. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J Virol 1988, 62:139-147. 250512, 3257102.
53. Takeuchi H, Kao S, Miyagi E, Khan MA, Buckler-White A, Plishka R, Strebel K. Production of infectious SIVagm from human cells requires functional inactivation but not viral exclusion of human APOBEC3G. J Biol Chem 2005, 280:375-382.
54. Campbell BJ, Hirsch VM. Vpr of simian immunodeficiency virus of African green monkeys is required for replication in macaque macrophages and lymphocytes. J Virol 1997, 71:5593-5602. 191801, 9188633.
55. Roos JW, Maughan MF, Liao Z, Hildreth JE, Clements JE. LuSIV cells: a reporter cell line for the detection and quantitation of a single cycle of HIV and SIV replication. Virology 2000, 273:307-315. 10.1006/viro.2000.0431, 10915601.