Unique spectrum of activity of prosimian TRIM5α against exogenous and endogenous retroviruses

Journal of Virology

Volumn 85, Issue 9, 2011, Pages 4173-4183

  Rahm, Nadia ^a   Yap, Melvyn ^b   Snoeck, Joke ^a,c   Zoete, Vincent ^d   Muñoz, Miguel ^a   Radespiel, Ute ^e   Zimmermann, Elke ^e   Michielin, Olivier ^d   Stoye, Jonathan P ^b   Ciuffi, Angela ^a   Telenti, Amalio ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SPROUTY PROTEIN; TRIPARTITE MOTIF PROTEIN 5;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; GENE INSERTION; HOST RESISTANCE; LEMURIDAE; NONHUMAN; PHYLOGENY; PREDICTION; PRIORITY JOURNAL; PROSIMIAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; RETROVIRUS; SEQUENCE ALIGNMENT; VIRUS CAPSID; VIRUS GENOME; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; LEMUR; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; RETROVIRIDAE; SEQUENCE HOMOLOGY, AMINO ACID;

HUMAN IMMUNODEFICIENCY VIRUS 1; LEMUR; LEMUR CATTA; LEMURIDAE; LENTIVIRUS; MICROCEBUS MURINUS; MURINE LEUKEMIA VIRUS; SIMIAE; STREPSIRHINI;

EID: 79955388914     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00075-11     Document Type: Article

References (66)

1. Asaoka, K., et al. 2005. A retrovirus restriction factor TRIM5alpha is tran-scriptionally regulated by interferons. Biochem. Biophys. Res. Commun. 338:1950-1956.
2. Berman, H. M., et al. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
3. Carthagena, L., et al. 2009. Human TRIM gene expression in response to interferons. PLoS One 4:e4894.
4. Carthagena, L., et al. 2008. Implication of TRIM alpha and TRIMCyp in interferon-induced anti-retroviral restriction activities. Retrovirology 5:59.
5. Diaz-Griffero, F., et al. 2008. A human TRIM5alpha B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus. Virology 378:233-242.
6. Diaz-Griffero, F., et al. 2009. A B-box 2 surface patch important for TRIM5alpha self-association, capsid binding avidity, and retrovirus restriction. J. Virol. 83:10737-10751.
7. Diehl, W. E., E. Stansell, S. M. Kaiser, M. Emerman, and E. Hunter. 2008. Identification of postentry restrictions to Mason-Pfizer monkey virus infection in New World monkey cells. J. Virol. 82:11140-11151.
8. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
9. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
10. Emerman, M., and H. S. Malik. 2010. Paleovirology-modern consequences of ancient viruses. PLoS Biol. 8:e1000301.
11. Gifford, R. J., et al. 2008. A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc. Natl. Acad. Sci. U. S. A. 105:20362-20367.
12. Gilbert, C., D. G. Maxfield, S. M. Goodman, and C. Feschotte. 2009. Parallel germline infiltration of a lentivirus in two Malagasy lemurs. PLoS Genet. 5:e1000425.
13. Goldschmidt, V., et al. 2008. Antiretroviral activity of ancestral TRIM5alpha. J. Virol. 82:2089-2096.
14. Goldstone, D. C., et al. 2010. Structural and functional analysis of prehistoric lentiviruses uncovers an ancient molecular interface. Cell Host Microbe 8:248-259.
15. Hatziioannou, T., D. Perez-Caballero, A. Yang, S. Cowan, and P. D. Bien-iasz. 2004. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 101:10774-10779.
16. Horvath, J. E., and H. F. Willard. 2007. Primate comparative genomics: lemur biology and evolution. Trends Genet. 23:173-182.
17. James, L. C., A. H. Keeble, Z. Khan, D. A. Rhodes, and J. Trowsdale. 2007. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. Proc. Natl. Acad. Sci. U. S. A. 104:6200-6205.
18. Javanbakht, H., F. Diaz-Griffero, M. Stremlau, Z. Si, and J. Sodroski. 2005. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J. Biol. Chem. 280:26933-26940.
19. Joly-Radko, M., E. Zimmermann. 2010. Seasonality in gum and honeydew feeding in gray mouse lemurs, p. 141-153. In A. M. Burrows and L. T. Nash (ed.), The evolution of exudativory in primates. Springer, New York, NY.
20. Katzourakis, A., M. Tristem, O. G. Pybus, and R. J. Gifford. 2007. Discovery and analysis of the first endogenous lentivirus. Proc. Natl. Acad. Sci. U. S. A. 104:6261-6265.
21. Keckesova, Z., L. M. Ylinen, and G. J. Towers. 2004. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc. Natl. Acad. Sci. U. S. A. 101:10780-10785.
22. Keckesova, Z., L. M. Ylinen, G. J. Towers, R. J. Gifford, and A. Katzourakis. 2009. Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology 384:7-11.
23. Keeble, A. H., Z. Khan, A. Forster, and L. C. James. 2008. TRIM21 is an IgG receptor that is structurally, thermodynamically, and kinetically conserved. Proc. Natl. Acad. Sci. U. S. A. 105:6045-6050.
24. Kirmaier, A., et al. 2010. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 8:pii=e100462. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=e100462.
25. Kratovac, Z., et al. 2008. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82:6772-6777.
26. Li, X., B. Song, S. H. Xiang, and J. Sodroski. 2007. Functional interplay between the B-box 2 and the B30.2(SPRY) domains of TRIM5alpha. Virology 366:234-244.
27. Lim, S. Y., et al. 2010. TRIM5alpha modulates immunodeficiency virus control in rhesus monkeys. PLoS Pathog. 6:e1000738.
28. Liu, H. L., et al. 2005. Adaptive evolution of primate TRIM5alpha, a gene restricting HIV-1 infection. Gene 362:109-116.
29. Maillard, P. V., G. Ecco, M. Ortiz, and D. Trono. 2010. The specificity of TRIM5 alpha-mediated restriction is influenced by its coiled-coil domain. J. Virol. 84:5790-5801.
30. Maillard, P. V., S. Reynard, F. Serhan, P. Turelli, and D. Trono. 2007. Interfering residues narrow the spectrum of MLV restriction by human TRIM5alpha. PLoS Pathog. 3:e200.
31. McEwan, W. A., et al. 2009. Truncation of TRIM5 in the Feliformia explains the absence of retroviral restriction in cells of the domestic cat. J. Virol. 83:8270-8275.
32. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
33. Mische, C. C, et al. 2005. Retroviral restriction factor TRIM5alpha is a trimer. J. Virol. 79:14446-14450.
34. Mittermeier, R. A., et al. 2010. Lemurs of Madagascar, 3rd ed. Conservation International, Washington, DC.
35. Newman, R. M., et al. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 103:19134-19139.
36. Ohkura, S., M. W. Yap, T. Sheldon, and J. P. Stoye. 2006. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J. Virol. 80:8554-8565.
37. Ortiz, M., G. Bleiber, R. Martinez, H. Kaessmann, and A. Telenti. 2006. Patterns of evolution of host proteins involved in retroviral pathogenesis. Retrovirology 3:11.
38. Ortiz, M., et al. 2009. Evolutionary trajectories of primate genes involved in HIV pathogenesis. Mol. Biol. Evol. 26:2865-2875.
39. Pacheco, B., A. Finzi, K. McGee-Estrada, and J. Sodroski. 2010. Species-specific inhibition of foamy viruses from South American monkeys by New World monkey TRIM5alpha proteins. J. Virol. 84:4095-4099.
40. Perez-Caballero, D., T. Hatziioannou, A. Yang, S. Cowan, and P. D. Bien-iasz. 2005. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J. Virol. 79:8969-8978.
41. Perron, M. J., et al. 2004. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc. Natl. Acad. Sci. U. S. A. 101:11827-11832.
42. Pettersen, E. F., et al. 2004. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
43. Pham, Q. T., A. Bouchard, M. G. Grutter, and L. Berthoux. 2010. Generation of human TRIM5alpha mutants with high HIV-1 restriction activity. Gene Ther. 17:859-871.
44. Radespiel, U. 2006. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.), p. 211-233. In L. Gould and M. L. Sauther (ed.), Lemurs: ecology and adaptation. Springer, New York, NY.
45. Reymond, A., et al. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20:2140-2151.
46. Saenz, D. T., W. Teo, J. C. Olsen, and E. M. Poeschla. 2005. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins. J. Virol. 79:15175-15188.
47. Sakuma, R., A. A. Mael, and Y. Ikeda. 2007. Alpha interferon enhances TRIM5alpha-mediated antiviral activities inhuman and rhesus monkey cells. J. Virol. 81:10201-10206.
48. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
49. Sawyer, S. L., M. Emerman, and H. S. Malik. 2007. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog. 3:e197.
50. Sawyer, S. L., L. I. Wu, M. Emerman, and H. S. Malik. 2005. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U. S. A. 102:2832-2837.
51. Si, Z., et al. 2006. Evolution of a cytoplasmic tripartite motif (TRIM) protein in cows that restricts retroviral infection. Proc. Natl. Acad. Sci. U. S. A. 103:7454-7459.
52. Sondgeroth, K., et al. 2007. Assessing flavivirus, lentivirus, and herpesvirus exposure in free-ranging ring-tailed lemurs in southwestern Madagascar. J. Wildl. Dis. 43:40-47.
53. Song, B., et al. 2005. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J. Virol. 79:6111-6121.
54. Song, B., et al. 2005. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J. Virol. 79:3930-3937.
55. Stremlau, M., et al. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853.
56. Stremlau, M., et al. 2006. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. U. S. A. 103:5514-5519.
57. Stremlau, M., M. Perron, S. Welikala, and J. Sodroski. 2005. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J. Virol. 79: 3139-3145.
58. Tareen, S. U., S. L. Sawyer, H. S. Malik, and M. Emerman. 2009. An expanded clade of rodent Trim5 genes. Virology 385:473-483.
59. Thornton, J. W. 2004. Resurrecting ancient genes: experimental analysis of extinct molecules. Nat. Rev. Genet. 5:366-375.
60. UniProt Consortium. 2010. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Res. 38:D142-D148.
61. Weinert, C., C. Grutter, H. Roschitzki-Voser, P. R. Mittl, and M. G. Grutter. 2009. The crystal structure of human pyrin b30.2 domain: implications for mutations associated with familial Mediterranean fever. J. Mol. Biol. 394: 226-236.
62. Yap, M. W., et al. 2008. Restriction of foamy viruses by primate Trim5alpha. J. Virol. 82:5429-5439.
63. Yap, M. W., S. Nisole, C. Lynch, and J. P. Stoye. 2004. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc. Natl. Acad. Sci. U. S. A. 101:10786-10791.
64. Yap, M. W., S. Nisole, and J. P. Stoye. 2005. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr. Biol. 15:73-78.
65. Ylinen, L. M., et al. 2006. Isolation of an active Lv1 gene from cattle indicates that tripartite motif protein-mediated innate immunity to retroviral infection is widespread among mammals. J. Virol. 80:7332-7338.
66. Ylinen, L. M., Z. Keckesova, S. J. Wilson, S. Ranasinghe, and G. J. Towers. 2005. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J. Virol. 79:11580-11587.