Murine double minute 2 as a modulator of retroviral restrictions mediated by TRIM5α

Virology

Volumn 405, Issue 2, 2010, Pages 414-423

  Malbec, Marine ^a   Pham, Quang Toan ^a   Plourde, Mélodie B ^a   Létourneau Hogan, Alexandra ^a   Nepveu Traversy, Marie Édith ^a   Berthoux, Lionel ^a  

^a UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

Author keywords

EIAV; Genetic screen; HIV; MDM2; MLV; Proteasome; Restriction; RNAi; TRIM5

Indexed keywords

ARSENIC TRIOXIDE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; PROTEIN MDM2; SHORT HAIRPIN RNA; TRIPARTITE MOTIF PROTEIN 5;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EQUINE INFECTIOUS ANEMIA VIRUS; GENE EXPRESSION; GENETIC SCREENING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INFECTION RESISTANCE; INNATE IMMUNITY; MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; ARSENICALS; CARRIER PROTEINS; CELL LINE; HIV-1; HUMANS; INFECTIOUS ANEMIA VIRUS, EQUINE; LEUKEMIA VIRUS, MURINE; LEUPEPTINS; MICE; OXIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTO-ONCOGENE PROTEINS C-MDM2; RNA INTERFERENCE;

CERCOPITHECUS AETHIOPS; EQUINE INFECTIOUS ANEMIA VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE; MURINE LEUKEMIA VIRUS;

EID: 77955656729     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.06.021     Document Type: Article

References (66)

1. Anderson J.L., Campbell E.M., Wu X., Vandegraaff N., Engelman A., Hope T.J. Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J. Virol. 2006, 80(19):9754-9760.
2. Asaoka K., Ikeda K., Hishinuma T., Horie-Inoue K., Takeda S., Inoue S. A retrovirus restriction factor TRIM5alpha is transcriptionally regulated by interferons. Biochem. Biophys. Res. Commun. 2005, 338(4):1950-1956.
3. Berthoux L., Sebastian S., Sokolskaja E., 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. 2004, 78(21):11739-11750.
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. U. S. A. 2005, 102(41):14849-14853.
5. Berthoux L., Towers G.J., Gurer C., Salomoni P., Pandolfi P.P., Luban J. As(2)O(3) enhances retroviral reverse transcription and counteracts Ref1 antiviral activity. J. Virol. 2003, 77(5):3167-3180.
6. Bérubé J., Bouchard A., Berthoux L. Both TRIM5alpha and TRIMCyp have only weak antiviral activity in canine D17 cells. Retrovirology 2007, 4:68.
7. Besnier C., Ylinen L., Strange B., Lister A., Takeuchi Y., Goff S.P., Towers G.J. Characterization of murine leukemia virus restriction in mammals. J. Virol. 2003, 77(24):13403-13406.
8. Brennan G., Kozyrev Y., Hu S.L. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(9):3569-3574.
9. Brooks C.L., Gu W. p53 ubiquitination: Mdm2 and beyond. Mol. Cell 2006, 21(3):307-315.
10. Carthagena L., Parise M.C., Ringeard M., Chelbi-Alix M.K., Hazan U., Nisole S. Implication of TRIM alpha and TRIMCyp in interferon-induced anti-retroviral restriction activities. Retrovirology 2008, 5:59.
11. Diaz-Griffero F., Kar A., Lee M., Stremlau M., Poeschla E., Sodroski J. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. Virology 2007, 369(2):400-410.
12. Diaz-Griffero F., Li X., Javanbakht H., Song B., Welikala S., Stremlau M., Sodroski J. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 2006, 349(2):300-315.
13. Hatziioannou T., Perez-Caballero D., Yang A., Cowan S., Bieniasz P.D. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(29):10774-10779.
14. Izumi T., Takaori-Kondo A., Shirakawa K., Higashitsuji H., Itoh K., Io K., Matsui M., Iwai K., Kondoh H., Sato T., Tomonaga M., Ikeda S., Akari H., Koyanagi Y., Fujita J., Uchiyama T. MDM2 is a novel E3 ligase for HIV-1 Vif. Retrovirology 2009, 6:1.
15. Johnson W.E., Sawyer S.L. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 2009, 61(3):163-176.
16. Keckesova Z., Ylinen L.M., 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. 2004, 101(29):10780-10785.
17. Keckesova Z., Ylinen L.M., Towers G.J. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J. Virol. 2006, 80(10):4683-4690.
18. Kratovac Z., Virgen C.A., Bibollet-Ruche F., Hahn B.H., Bieniasz P.D., Hatziioannou T. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 2008, 82(13):6772-6777.
19. Lallemand-Breitenbach V., Jeanne M., Benhenda S., Nasr R., Lei M., Peres L., Zhou J., Zhu J., Raught B., de The H. Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat. Cell Biol. 2008, 10(5):547-555.
20. Li S., Hill C.P., Sundquist W.I., Finch J.T. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 2000, 407(6802):409-413.
21. Li Y., Li X., Stremlau M., Lee M., Sodroski J. Removal of arginine 332 allows human TRIM5alpha to bind human immunodeficiency virus capsids and to restrict infection. J. Virol. 2006, 80(14):6738-6744.
22. Luban J. Cyclophilin A, TRIM5, and resistance to human immunodeficiency virus type 1 infection. J. Virol. 2007, 81(3):1054-1061.
23. MacDuff D.A., Neuberger M.S., Harris R.S. MDM2 can interact with the C-terminus of AID but it is inessential for antibody diversification in DT40 B cells. Mol. Immunol. 2006, 43(8):1099-1108.
24. Mitrophanous K., Yoon S., Rohll J., Patil D., Wilkes F., Kim V., Kingsman S., Kingsman A., Mazarakis N. Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther. 1999, 6(11):1808-1818.
25. Mortuza G.B., Haire L.F., Stevens A., Smerdon S.J., Stoye J.P., Taylor I.A. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 2004, 431(7007):481-485.
26. Naviaux R.K., Costanzi E., Haas M., Verma I.M. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 1996, 70(8):5701-5705.
27. Newman R.M., Hall L., Kirmaier A., Pozzi L.A., Pery E., Farzan M., O'Neil S.P., Johnson W. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 2008, 4(2):e1000003.
28. 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. U. S. A. 2004, 101(36):13324-13328.
29. Nisole S., Stoye J.P., Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 2005, 3(10):799-808.
30. Ohkura S., Yap M.W., Sheldon T., Stoye J.P. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J. Virol. 2006, 80(17):8554-8565.
31. Passerini L.D., Keckesova Z., Towers G.J. Retroviral restriction factors Fv1 and TRIM5alpha act independently and can compete for incoming virus before reverse transcription. J. Virol. 2006, 80(5):2100-2105.
32. Perez-Caballero D., Hatziioannou T., Yang A., Cowan S., Bieniasz P.D. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J. Virol. 2005, 79(14):8969-8978.
33. Perron M.J., Stremlau M., Lee M., Javanbakht H., Song B., Sodroski J. The human TRIM5alpha restriction factor mediates accelerated uncoating of the N-tropic murine leukemia virus capsid. J. Virol. 2007, 81(5):2138-2148.
34. Perron M.J., Stremlau M., Song B., Ulm W., Mulligan R.C., Sodroski J. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(32):11827-11832.
35. Pham Q.T., Bouchard A., Grutter M.G., Berthoux L. Generation of human TRIM5alpha mutants with high HIV-1 restriction activity. Gene Ther. 2010.
36. Pochampally R., Fodera B., Chen L., Shao W., Levine E.A., Chen J. A 60 kd MDM2 isoform is produced by caspase cleavage in non-apoptotic tumor cells. Oncogene 1998, 17(20):2629-2636.
37. 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(7):1282-1292.
38. Rold C.J., Aiken C. Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog. 2008, 4(5):e1000074.
39. Saenz D.T., Teo W., Olsen J.C., Poeschla E.M. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins. J. Virol. 2005, 79(24):15175-15188.
40. Sawyer S.L., Wu L.I., Emerman M., Malik H.S. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(8):2832-2837.
41. Sayah D.M., 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. 2004, 78(21):12066-12070.
42. Sayah D.M., Sokolskaja E., Berthoux L., Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004, 430(6999):569-573.
43. Schaller T., Hue S., Towers G.J. An active TRIM5 protein in rabbits indicates a common antiviral ancestor for mammalian TRIM5 proteins. J. Virol. 2007, 81(21):11713-11721.
44. Sebastian S., Luban J. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2005, 2:40.
45. Sebastian S., Sokolskaja E., Luban J. Arsenic counteracts human immunodeficiency virus type 1 restriction by various TRIM5 orthologues in a cell type-dependent manner. J. Virol. 2006, 80(4):2051-2054.
46. Si Z., Vandegraaff N., O'Huigin C., Song B., Yuan W., Xu C., Perron M., Li X., Marasco W.A., Engelman A., Dean M., Sodroski J. Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(19):7454-7459.
47. Sodroski J.G. Innate intracellular immunity to retroviruses. Harvey Lect. 2004, 100:143-153.
48. Song B., Gold B., O'Huigin C., Javanbakht H., Li X., Stremlau M., Winkler C., Dean M., Sodroski J. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J. Virol. 2005, 79(10):6111-6121.
49. Song B., Javanbakht H., Perron M., Park D.H., Stremlau M., Sodroski J. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J. Virol. 2005, 79(7):3930-3937.
50. Stommel J.M., Wahl G.M. A new twist in the feedback loop: stress-activated MDM2 destabilization is required for p53 activation. Cell Cycle 2005, 4(3):411-417.
51. Strebel K., Luban J., Jeang K.T. Human cellular restriction factors that target HIV-1 replication. BMC Med. 2009, 7:48.
52. 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(6977):848-853.
53. 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. U. S. A. 2006, 103(14):5514-5519.
54. Stremlau M., Perron M., Welikala S., Sodroski J. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J. Virol. 2005, 79(5):3139-3145.
55. 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(1):112-120.
56. Tatham M.H., Geoffroy M.C., Shen L., Plechanovova A., Hattersley N., Jaffray E.G., Palvimo J.J., Hay R.T. RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat. Cell Biol. 2008, 10(5):538-546.
57. Towers G., Bock M., Martin S., Takeuchi Y., Stoye J.P., Danos O. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(22):12295-12299.
58. Towers G.J. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 2007, 4:40.
59. Uchil P.D., Quinlan B.D., Chan W.T., Luna J.M., Mothes W. TRIM E3 ligases interfere with early and late stages of the retroviral life cycle. PLoS Pathog. 2008, 4(2):e16.
60. Van Parijs L., Refaeli Y., Lord J.D., Nelson B.H., Abbas A.K., Baltimore D. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 1999, 11(3):281-288.
61. Virgen C.A., Kratovac Z., Bieniasz P.D., Hatziioannou T. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(9):3563-3568.
62. 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. U. S. A. 2008, 105(9):3557-3562.
63. Wu X., Anderson J.L., Campbell E.M., Joseph A.M., Hope T.J. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(19):7465-7470.
64. Yap M.W., Nisole S., Lynch C., Stoye J.P. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(29):10786-10791.
65. Ylinen L.M., Keckesova Z., Wilson S.J., Ranasinghe S., Towers G.J. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J. Virol. 2005, 79(18):11580-11587.
66. Zufferey R., Nagy D., Mandel R.J., Naldini L., Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 1997, 15(9):871-875.