Contribution of SUMO-interacting motifs and SUMOylation to the antiretroviral properties of TRIM5α

Virology

Volumn 435, Issue 2, 2013, Pages 463-471

  Brandariz Nuñez, Alberto ^a   Roa, Amanda ^a   Valle Casuso, Jose Carlos ^a   Biris, Nikolaos ^b   Ivanov, Dmitri ^b   Diaz Griffero, Felipe ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b University of Texas Health Science Center at San Antonio   (United States)

Author keywords

HIV 1; Restriction; SUMO interacting motif; SUMOylation; TRIM5 rh

Indexed keywords

PROTEIN GAM1; SUMO 1 PROTEIN; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN TRANSPORT; STRUCTURE ACTIVITY RELATION; SUMO INTERACTING MOTIF; SUMOYLATION; VIRUS CORE; VIRUS INHIBITION;

AMINO ACID MOTIFS; ANIMALS; ANTIVIRAL AGENTS; CELL LINE; HIV-1; HUMANS; MUTATION; PROTEINS; SUMO-1 PROTEIN; SUMOYLATION; TRANSFECTION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84871706030     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.09.042     Document Type: Article

References (53)

1. Arriagada G., Muntean L.N., Goff S.P. SUMO-interacting motifs of human TRIM5alpha are important for antiviral activity. PLoS Pathog. 2011, 7:e1002019.
2. Biris N., Yang Y., Taylor A.B., Tomashevski A., Guo M., Hart P.J., Diaz-Griffero F., Ivanov D.N. Structure of the rhesus monkey TRIM5alpha PRYSPRY domain, the HIV capsid recognition module. Proc. Nat. Acad. Sci. USA 2012.
3. Boggio R., Colombo R., Hay R.T., Draetta G.F., Chiocca S. A mechanism for inhibiting the SUMO pathway. Mol. Cell 2004, 16:549-561.
4. Boggio R., Passafaro A., Chiocca S. Targeting SUMO E1 to ubiquitin ligases: a viral strategy to counteract sumoylation. J. Biol. Chem. 2007, 282:15376-15382.
5. Chiocca S., Baker A., Cotten M. Identification of a novel antiapoptotic protein, GAM-1, encoded by the CELO adenovirus. J. Virol. 1997, 71:3168-3177.
6. Colombo R., Boggio R., Seiser C., Draetta G.F., Chiocca S. The adenovirus protein Gam1 interferes with sumoylation of histone deacetylase 1. EMBO Rep. 2002, 3:1062-1068.
7. Diaz-Griffero F., Gallo D.E., Hope T.J., Sodroski J. Trafficking of some old world primate TRIM5alpha proteins through the nucleus. Retrovirology 2011, 8:38.
8. Diaz-Griffero F., Hoschander S.A., Brojatsch J. Endocytosis is a critical step in entry of subgroup B avian leukosis viruses. J. Virol. 2002, 76:12866-12876.
9. 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.
10. Diaz-Griffero F., Kar A., Perron M., Xiang S.H., Javanbakht H., Li X., Sodroski J. Modulation of retroviral restriction and proteasome inhibitor-resistant turnover by changes in the TRIM5alpha B-box 2 domain. J. Virol. 2007, 81:10362-10378.
11. 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, 349:300-315.
12. Diaz-Griffero F., Vandegraaff N., Li Y., McGee-Estrada K., Stremlau M., Welikala S., Si Z., Engelman A., Sodroski J. Requirements for capsid-binding and an effector function in TRIMCyp-mediated restriction of HIV-1. Virology 2006, 351:404-419.
13. Diaz-Griffero F., Perron M., McGee-Estrada K., Hanna R., Maillard P.V., Trono D., Sodroski J. A human TRIM5alpha B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus. Virology 2008, 378:233-242.
14. 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.
15. Fornerod M., Ohno M., Yoshida M., Mattaj I.W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90:1051-1060.
16. Ganser-Pornillos B.K., Chandrasekaran V., Pornillos O., Sodroski J.G., Sundquist W.I., Yeager M. Hexagonal assembly of a restricting TRIM5alpha protein. Proc. Nat. Acad. Sci. USA 2011, 108:534-539.
17. Javanbakht H., Diaz-Griffero F., Stremlau M., Si Z., Sodroski J. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J. Biol. Chem. 2005, 280:26933-26940.
18. Javanbakht H., Yuan W., Yeung D.F., Song B., Diaz-Griffero F., Li Y., Li X., Stremlau M., Sodroski J. Characterization of TRIM5alpha trimerization and its contribution to human immunodeficiency virus capsid binding. Virology 2006, 353:234-246.
19. Johnson E.S. Protein modification by SUMO. Annu. Rev. Biochem. 2004, 73:355-382.
20. Kar A.K., Diaz-Griffero F., Li Y., Li X., Sodroski J. Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. J. Virol. 2008, 82:11669-11681.
21. 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. Nat. Acad. Sci. USA 2004, 101:10780-10785.
22. Kim J., Tipper C., Sodroski J. Role of TRIM5{alpha} RING domain E3 ubiquitin ligase activity in capsid disassembly, reverse transcription blockade, and restriction of simian immunodeficiency virus. J. Virol. 2011, 85:8116-8132.
23. Kirmaier A., Wu F., Newman R.M., Hall L.R., Morgan J.S., O'Connor S., Marx P.A., Meythaler M., Goldstein S., Buckler-White A., Kaur A., Hirsch V.M., Johnson W.E. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 2010, 8.
24. Kudo N., Wolff B., Sekimoto T., Schreiner E.P., Yoneda Y., Yanagida M., Horinouchi S., Yoshida M. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 1998, 242:540-547.
25. Kuersten S., Ohno M., Mattaj I.W. Nucleocytoplasmic transport: ran, beta and beyond. Trends Cell Biol. 2001, 11:497-503.
26. Langelier C.R., Sandrin V., Eckert D.M., Christensen D.E., Chandrasekaran V., Alam S.L., Aiken C., Olsen J.C., Kar A.K., Sodroski J.G., Sundquist W.I. Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. J. Virol. 2008, 82:11682-11694.
27. Lienlaf M., Hayashi F., Di Nunzio F., Tochio N., Kigawa T., Yokoyama S., Diaz-Griffero F. Contribution of E3-ubiquitin ligase activity to HIV-1 restriction by TRIM5alpha(rh): structure of the RING domain of TRIM5alpha. J. Virol. 2011, 85:8725-8737.
28. Maegawa, H., Miyamoto, T., Sakuragi, J., Shioda, T., Nakayama, E.E., 2010. Contribution of RING domain to retrovirus restriction by TRIM5alpha depends on combination of host and virus. Virology 399, 212-220.
29. Mohr D., Frey S., Fischer T., Guttler T., Gorlich D. Characterisation of the passive permeability barrier of nuclear pore complexes. EMBO J. 2009, 28:2541-2553.
30. Mrosek M., Meier S., Ucurum-Fotiadis Z., von Castelmur E., Hedbom E., Lustig A., Grzesiek S., Labeit D., Labeit S., Mayans O. Structural analysis of B-Box 2 from MuRF1: identification of a novel self-association pattern in a RING-like fold. Biochemistry 2008, 47:10722-10730.
31. Nakayama E.E., Miyoshi H., Nagai Y., 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. 2005, 79:8870-8877.
32. 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, 80:8554-8565.
33. 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.
34. 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, 79:8969-8978.
35. 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, 81:2138-2148.
36. Reymond A., Meroni G., Fantozzi A., Merla G., Cairo S., Luzi L., Riganelli D., Zanaria E., Messali S., Cainarca S., Guffanti A., Minucci S., Pelicci P.G., Ballabio A. The tripartite motif family identifies cell compartments. EMBO J. 2001, 20:2140-2151.
37. Roa A., Hayashi F., Yang Y., Lienlaf M., Zhou J., Shi J., Watanabe S., Kigawa T., Yokoyama S., Aiken C., Diaz-Griffero F. RING domain mutations uncouple TRIM5alpha restriction of HIV-1 from inhibition of reverse transcription and acceleration of uncoating. J. Virol. 2012, 86:1717-1727.
38. 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. Nat. Acad. Sci. USA 2005, 102:2832-2837.
39. 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.
40. Sebastian S., Luban J. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2005, 2:40.
41. Song B., Diaz-Griffero F., Park D.H., Rogers T., Stremlau M., Sodroski J. TRIM5alpha association with cytoplasmic bodies is not required for antiretroviral activity. Virology 2005.
42. 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, 79:6111-6121.
43. 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, 79:3930-3937.
44. 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.
45. 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. Nat. Acad. Sci. USA 2006, 103:5514-5519.
46. 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, 79:3139-3145.
47. Wang Y.E., Pernet O., Lee B. Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin-related modifiers. Biol. Cell 2012, 104:121-138.
48. Watanabe M., Fukuda M., Yoshida M., Yanagida M., Nishida E. Involvement of CRM1, a nuclear export receptor, in mRNA export in mammalian cells and fission yeast. Genes Cells 1999, 4:291-297.
49. Wolff B., Sanglier J.J., Wang Y. Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 1997, 4:139-147.
50. Yamauchi K., Wada K., Tanji K., Tanaka M., Kamitani T. Ubiquitination of E3 ubiquitin ligase TRIM5 alpha and its potential role. FEBS J. 2008, 275:1540-1555.
51. Yap M.W., Nisole S., Stoye J.P. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr. Biol. 2005, 15:73-78.
52. Yee J.K., Friedmann T., Burns J.C. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 1994, 43(Pt. A):99-112.
53. Yueh A., Leung J., Bhattacharyya S., Perrone L.A., de los Santos K., Pu S.Y., Goff S.P. Interaction of moloney murine leukemia virus capsid with Ubc9 and PIASy mediates SUMO-1 addition required early in infection. J. Virol. 2006, 80:342-352.