Adaptation of HIV-1 to cells expressing rhesus monkey TRIM5α

Virology

Volumn 408, Issue 2, 2010, Pages 204-212

  Pacheco, Beatriz ^a   Finzi, Andrés ^a   Stremlau, Matthew ^a   Sodroski, Joseph ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Capsid; Cyclophilin binding loop; Mutant; Restriction factor; Retrovirus; Tripartite motif

Indexed keywords

BINDING PROTEIN; CAPSID PROTEIN; CYCLOPHILIN A; CYTOPLASM PROTEIN; TRIM5 ALPHA PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; RHESUS MONKEY; VIRUS ISOLATION; VIRUS REPLICATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CAPSID PROTEINS; CYCLOPHILIN A; HELA CELLS; HIV-1; HUMANS; MACACA MULATTA; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION; PROTEINS; RECOMBINANT PROTEINS; SPECIES SPECIFICITY; VIRUS REPLICATION;

CERCOPITHECIDAE; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; MIRIDAE;

EID: 78149416617     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.09.019     Document Type: Article

References (66)

1. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 1986, 59:284-291.
2. Alexander L., Du Z., Rosenzweig M., Jung J.U., Desrosiers R.C. A role for natural simian immunodeficiency virus and human immunodeficiency virus type 1 nef alleles in lymphocyte activation. J. Virol. 1997, 71:6094-6099.
3. Ambrose Z., KewalRamani V.N., Bieniasz P.D., Hatziioannou T. HIV/AIDS: in search of an animal model. Trends Biotechnol. 2007, 25:333-337.
4. 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.
5. Bishop K.N., Verma M., Kim E.Y., Wolinsky S.M., Malim M.H. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 2008, 4:e1000231.
6. Braaten D., Franke E.K., 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.
7. Bukovsky A.A., Weimann A., Accola M.A., 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 1997, 94:10943-10948.
8. Chatterji U., Bobardt M.D., Stanfield R., Ptak R.G., Pallansch L.A., Ward P.A., Jones M.J., Stoddart C.A., Scalfaro P., Dumont J.M., Besseghir K., Rosenwirth B., Gallay P.A. Naturally occurring capsid substitutions render HIV-1 cyclophilin A independent in human cells and TRIM-cyclophilin-resistant in Owl monkey cells. J. Biol. Chem. 2005, 280:40293-40300.
9. Cowan S., Hatziioannou T., Cunningham T., Muesing M.A., Gottlinger H.G., Bieniasz P.D. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc. Natl. Acad. Sci. USA 2002, 99:11914-11919.
10. Diaz-Griffero F., Qin X.R., Hayashi F., Kigawa T., Finzi A., Sarnak Z., Lienlaf M., Yokoyama S., Sodroski J. A B-box 2 surface patch important for TRIM5alpha self-association, capsid binding avidity, and retrovirus restriction. J. Virol. 2009, 83:10737-10751.
11. Dodding M.P., Bock M., Yap M.W., Stoye J.P. Capsid processing requirements for abrogation of Fv1 and Ref1 restriction. J. Virol. 2005, 79:10571-10577.
12. Feng Y., Broder C.C., Kennedy P.E., Berger E.A. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 1996, 272:872-877.
13. Franke E.K., Yuan H.E., Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 1994, 372:359-362.
14. Gamble T.R., Vajdos F.F., Yoo S., Worthylake D.K., Houseweart M., Sundquist W.I., Hill C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 1996, 87:1285-1294.
15. Ganser B.K., Li S., Klishko V.Y., Finch J.T., Sundquist W.I. Assembly and analysis of conical models for the HIV-1 core. Science 1999, 283:80-83.
16. Gatanaga H., Das D., Suzuki Y., Yeh D.D., Hussain K.A., Ghosh A.K., Mitsuya H. Altered HIV-1 gag protein interactions with cyclophilin A (CypA) on the acquisition of H219Q and H219P substitutions in the CypA binding loop. J. Biol. Chem. 2006, 281:1241-1250.
17. Hahn B.H., Shaw G.M., De Cock K.M., Sharp P.M. AIDS as a zoonosis: scientific and public health implications. Science 2000, 287:607-614.
18. Hatcho K., Kamada K., Yamashita T., Adachi A., Nomaguchi M. Replication potentials of vif variant viruses generated from monkey cell-tropic HIV-1 derivative clones NL-DT5/NL-DT5R. Microbes Infect. 2008, 10:1218-1222.
19. Hatziioannou T., Cowan S., Goff S.P., Bieniasz P.D., Towers G.J. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 2003, 22:385-394.
20. Hatziioannou T., Cowan S., Von Schwedler U.K., Sundquist W.I., Bieniasz P.D. Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J. Virol. 2004, 78:6005-6012.
21. Hatziioannou T., Perez-Caballero D., Cowan S., Bieniasz P.D. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 2005, 79:176-183.
22. Hatziioannou T., Princiotta M., Piatak M., Yuan F., Zhang F., Lifson J.D., Bieniasz P.D. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 2006, 314:95.
23. Heeney J.L., Dalgleish A.G., Weiss R.A. Origins of HIV and the evolution of resistance to AIDS. Science 2006, 313:462-466.
24. Helseth E., Kowalski M., Gabuzda D., Olshevsky U., Haseltine W., Sodroski J. Rapid complementation assays measuring replicative potential of human immunodeficiency virus type 1 envelope glycoprotein mutants. J. Virol. 1990, 64:2416-2420.
25. Hofmann W., Schubert D., LaBonte J., Munson L., Gibson S., Scammell J., Ferrigno P., Sodroski J. Species-specific, postentry barriers to primate immunodeficiency virus infection. J. Virol. 1999, 73:10020-10028.
26. Ikeda Y., Ylinen L., Kahar-Bador M., Towers G.J. The influence of gag on HIV-1 species specific tropism. J. Virol. 2004, 78:1816-11822.
27. Jia B., Serra-Morena R., Neidermyer W., Rahmberg A., Mackey J., Fofana I.B., Johnson W.E., Westmoreland S., Evans D.T. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 2009, 5:e1000429.
28. Kamada K., Igarashi T., Martin M.A., Khamsri B., Hatcho K., Yamashita T., Fujita M., Uchiyama T., Adachi A. Generation of HIV-1 derivatives that productively infect macaque monkey lymphoid cells. Proc. Natl. Acad. Sci. USA 2006, 103:16959-16964.
29. Kamada K., Yamashita T., Hatcho K., Adachi A., Nomaguchi M. Evasion from CypA- and APOBEC-mediated restrictions is insufficient for HIV-1 to efficiently grow in simian cells. Microbes Infect. 2009, 11:164-171.
30. Keele B.F., Van Heuverswyn F., Li Y., Bailes E., Takehisa J., Santiago M.L., Bibollet-Ruche F., Chen Y., Wain L.V., Liegeois F., Loul S., Ngole E.M., Bienvenue Y., Delaporte E., Brookfield J.F., Sharp P.M., Shaw G.M., Peeters M., Hahn B.H. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1. Science 2006, 313:523-526.
31. Kolchinsky P., Mirzabekov T., Farzan M., Kiprilov E., Cayabyab M., Mooney L.J., Choe H., Sodroski J. Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J. Virol. 1999, 73:8120-8126.
32. Kootstra N.A., Munk C., Tonnu N., Landau N.R., Verma I.M. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. USA 2003, 100:1298-1303.
33. Kootstra N.A., Navis M., Beugeling C., Van Dort K.A., Schuitemaker H. The presence of the TRIM5alpha escape mutation H87Q in the capsid of late stage HIV-1 variants is preceded by a prolonged asymptomatic infection phase. AIDS 2007, 21:2015-2023.
34. Kuiken, C., Leitner, T., Foley, B., Hahn, B., Marx, P., McCutchan, F., Wolinsky, S., Korber, B., 2008. HIV Sequence Compendium 2008. (Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, New Mexico.).
35. Lecossier D., Bouchonnet F., Clavel F., Hance A.J. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 2003, 300:1112.
36. Li X., Sodroski J. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J. Virol. 2008, 82:11495-11502.
37. Li J.T., Halloran M., Lord C.I., Watson A., Ranchalis J., Fung M., Letvin N.L., Sodroski J.G. Persistent infection of macaques with simian-human immunodeficiency viruses. J. Virol. 1995, 69:7061-7067.
38. Li Y., Kar A.K., Sodroski J. Target cell type-dependent modulation of human immunodeficiency virus type 1 capsid disassembly by cyclophilin A. J. Virol. 2009, 83:10951-10962.
39. Mariani R., Chen D., Schrofelbauer B., Navarro F., Konig R., Bollman B., Munk C., Nymark-McMahon H., Landau N.R. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003, 114:21-31.
40. Mbisa J.L., Barr R., Thomas J.A., Vandegraaff N., Dorweiler I.J., Svarovskaia E.S., Brown W.L., Mansky L.M., Gorelick R.J., Harris R.S., Engelman A., Pathak V.K. Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J. Virol. 2007, 81:7099-7110.
41. McNatt M.W., Zang T., Hatziioannou T., Bartlett M., Fofana I.B., Johnson W.E., Neil S.J., Bieniasz P.D. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog. 2009, 5:e1000300.
42. Munk C., Brandt S.M., Lucero G., Landau N.R. A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc. Natl. Acad. Sci. USA 2002, 99:13843-13848.
43. Nagao T., Hatcho K., Doi N., Fugiwara S., Adachi A., Nomaguchi M. Amino acid alterations in Gag that confer the ability to grow in simian cells on HIV-1 are located at a narrow CA region. J. Med. Invest. 2009, 56:21-25.
44. Neil S.J., Zang T., Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008, 451:425-430.
45. Nepveu-Traversy M.E., Berube J., Berthoux L. TRIM5alpha and TRIMCyp form apparent hexamers and their multimeric state is not affected by exposure to restriction-sensitive viruses or by treatment with pharmacological inhibitors. Retrovirology 2009, 6:100.
46. Nisole S., Lynch C., Stoye J.P., Yap M.W. 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.
47. Owens C.M., Yang P.C., Gottlinger H., Sodroski J. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J. Virol. 2003, 77:726-731.
48. Owens C.M., Song B., Perron M.J., Yang P.C., Stremlau M., 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. 2004, 78:5423-5437.
49. Pacheco B., Basmaciogullari S., Labonte J.A., Xiang S.H., Sodroski J. Adaptation of the human immunodeficiency virus type 1 envelope glycoproteins to New World monkey receptors. J. Virol. 2008, 82:346-357.
50. Pornillos O., Ganser-Pornillos B.K., Kelly B.N., Hua Y., Whitby F.G., Stout C.D., Sundquist W.I., Hill C.P., Yeager M. X-ray structures of the hexameric building block of the HIV capsid. Cell 2009, 137:1282-1292.
51. Rho H.M., Poiesz B., Ruscetti F.W., Gallo R.C. Characterization of the reverse transcriptase from a new retrovirus (HTLV) produced by a human cutaneous T-cell lymphoma cell line. Virology 1981, 112:355-360.
52. Sawyer S.L., Emerman M., Malik H.S. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog. 2007, 3:e197.
53. Sayah D.M., Sokolskaja E., Berthoux L., Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004, 430:569-573.
54. Schrofelbauer B., Senger T., Manning G., Landau N.R. Mutational alteration of human immunodeficiency virus type 1 Vif allows for functional interaction with nonhuman primate APOBEC3G. J. Virol. 2006, 80:5984-5991.
55. Sebastian S., Luban J. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2005, 2:40.
56. Sharp P.M., Shaw G.M., Hahn B.H. Simian immunodeficiency virus infection of chimpanzees. J. Virol. 2005, 79:3891-3902.
57. Shi J., Aiken C. Saturation of TRIM5 alpha-mediated restriction of HIV-1 infection depends on the stability of the incoming viral capsid. Virology 2006, 350:493-500.
58. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853.
59. Stremlau M., Perron M., Lee M., Li Y., Song B., Javanbakht H., Diaz-Griffero F., Anderson D.J., Sundquist W.I., Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. USA 2006, 103:5514-5519.
60. 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.
61. Towers G.J., Hatziioannou T., Cowan S., Goff S.P., Luban J., Bieniasz P.D. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 2003, 9:1138-1143.
62. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., Guatelli J. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 2008, 3:245-252.
63. Van Heuverswyn F., Peeters M. The origins of HIV and implications for the global epidemic. Curr. Infect. Dis. Rep. 2007, 9:338-346.
64. Van Heuverswyn F., Li Y., Neel C., Bailes E., Keele B.F., Liu W., Loul S., Butel C., Liegeois F., Bienvenue Y., Ngolle E.M., Sharp P.M., Shaw G.M., Delaporte E., Hahn B.H., Peeters M. Human immunodeficiency viruses: SIV infection in wild gorillas. Nature 2006, 444:164.
65. Wilson S.J., Webb B.L., Ylinen L.M., Verschoor E., Heeney J.L., Towers G.J. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. USA 2008, 105:3557-3562.
66. Yu X., Yu Y., Liu B., Luo K., Kong W., Mao P., Yu X.F. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 2003, 302:1056-1060.