Role of TRIM5α RING domain E3 ubiquitin ligase activity in capsid disassembly, reverse transcription blockade, and restriction of simian immunodeficiency virus

Journal of Virology

Volumn 85, Issue 16, 2011, Pages 8116-8132

  Kim, Jonghwa ^a   Tipper, Christopher ^a   Sodroski, Joseph ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRIPARTITE MOTIF PROTEIN 5; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; BINDING AFFINITY; CHLOROCEBUS; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; REVERSE TRANSCRIPTION; RING FINGER MOTIF; SIMIAN IMMUNODEFICIENCY VIRUS; UBIQUITINATION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS UNCOATING;

CERCOPITHECUS AETHIOPS; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; MIRIDAE; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 79961188135     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00341-11     Document Type: Article

References (95)

1. Abe, H., et al. 2007. Solution structure of the zinc finger, C3HC4 type (ring finger) domain of tripartite motif-containing protein 5. Accession number 2ecv. RIKEN Structural Genomics/Proteomic Initiative (FSGI), RCSB Protein Data Bank, Piscataway, NJ.
2. Anderson, J. L., et al. 2006. Proteasome inhibition reveals that a function preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J. Virol. 80, 9754-9760.
3. Aravind, L., and E. V. Koonin. 2000. The U box is a modified RING finger-a common domain in ubiquitination. Curr. Biol. 10, R132-R134.
4. Berthoux, L., S. Sebastian, E. Sokolskaja, and J. Luban. 2005. Cyclophilin A is required for TRIM5(alpha)-mediated resistance to HIV-1 in Old World monkey cells. Proc. Natl. Acad. Sci. U. S. A. 102, 14849-14853.
5. Besnier, C., et al. 2003. Characterization of murine leukemia virus restriction in mammals. J. Virol. 77, 13403-13406.
6. Brennan, G., Y. Kozyrev, T. Kodama, and S. L. Hu. 2007. Novel TRIM5 isoforms expressed by Macaca nemestrina. J. Virol. 81, 12210-12217.
7. Brennan, G., Y. Kozyrev, and S. L. Hu. 2008. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fasciculair. Proc. Natl. Acad. Sci. U. S. A. 105, 3569-3574.
8. Cowan, S., et al. 2002. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc. Natl. Acad. Sci. U. S. A. 99, 11914-11919.
9. Dantuma, N. P., T. A. M. Groothuis, F. A. Salomons, and J. Neefjes. 2006. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J. Cell Biol. 173, 19-26.
10. Diaz-Griffero, F., et al. 2008. A human TRIM5α B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus. Virology 378, 233-242.
11. Diaz-Griffero, F., et al. 2009. A B-box 2 surface patch important for TRIM5(alpha) self-association, capsid-binding avidity, and retrovirus restriction. J. Virol. 83, 10737-10751.
12. Diaz-Griffero, F., et al. 2007. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. Virology 369, 400-410.
13. Diaz-Griffero, F., et al. 2007. Modulation of retroviral restriction and proteasome inhibitor-resistant turnover by changes in the TRIM5{alpha} B-box 2 domain. J. Virol. 81, 10362-10378.
14. Diaz-Griffero, F., et al. 2006. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 349, 300-315.
15. Douglas, C. C., D. Thomas, J. Lanman, and P. E. Prevelige, Jr. 2004. Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1 CA. Biochemistry 43, 10435-10441.
16. Dueck, M., and J. Guatelli. 2007. Evidence against a direct antiviral activity of the proteasome during the early steps of HIV-1 infection. Virology 361, 1-8.
17. Forshey, B. M., U. von Schwedler, W. I. Sundquist, and C. Aiken. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76, 5667-5677.
18. Freemont, P. S. 2000. RING for destruction? Curr. Biol. 10, R84-R87.
19. Gack, M. U., et al. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 448, 916-920.
20. Ganser, B. K., S. Li, V. Y. Klishko, J. T. Finch, and W. Sundquist. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283, 80-83.
21. Goujon, C., et al. 2007. SIVSM/HIV-2 Vpx proteins promote retroviral escape from a proteasome-dependent restriction pathway present in human dendritic cells. Retrovirology 4, 2.
22. Hatziioannou, T., S. Cowan, S. P. Goff, P. D. Bieniasz, and G. J. Tower. 2003. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 22, 385-394.
23. Hatziioannou, T., D. Perez-Caballero, A. Yang, S. Cowan, and P. D. Bieniasz. 2004. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 101, 10774-10779.
24. Hatziioannou, T., D. Perez-Caballero, S. Cowan, and P. D. Bieniasz. 2005. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79, 176-183.
25. Hofmann, W., et al. 1999. Species-specific, post-entry barriers to primate immunodeficiency virus infection. J. Virol. 73, 10020-10028.
26. Jackson, P. K., et al. 2000. The lore of the RINGs, substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol. 10, 429-439.
27. Javanbakht, H., et al. 2006. Characterization of TRIM5alpha trimerization and its contribution to human immunodeficiency virus capsid binding. Virology 353, 234-246.
28. Javanbakht, H., et al. 2007. The ability of multimerized cyclophilin A to restrict retrovirus infection. Virology 367, 19-29.
29. 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 TRIM5α. J. Biol. Chem. 280, 26933-26940.
30. Kallijarvi, J., et al. 2005. TRIM37 defective in mulibrey nanism is a novel RING finger ubiquitin E3 ligase. Exp. Cell Res. 308, 148-155.
31. Kar, A. K., F. Diaz-Griffero, Y. Li, X. Li, and J. Sodroski. 2008. Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. J. Virol. 82, 11669-11681.
32. 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.
33. Keckesova, Z., L. M. Ylinen, and G. J. Towers. 2006. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J. Virol. 80, 4683-4690.
34. Kentsis, A., R. E. Gordon, and K. L. Borden. 2002. Control of biochemical reactions through supramolecular RING domain self-assembly. Proc. Natl. Acad. Sci. U. S. A. 99, 15404-15409.
35. Kootstra, N. A., C. Munk, N. Tonnu, N. R. Landau, and I. M. Verma. 2003. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. U. S. A. 100, 1298-1303.
36. Kootstra, N. A., M. Navis, C. Beugeling, K. A. van Dort, and H. Schuitemaker. 2007. 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 21, 2015-2023.
37. Kratovac, Z., et al. 2008. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82, 6772-6777.
38. Langelier, C. R., et al. 2008. Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type replication. J. Virol. 82, 11682-11694.
39. Lee, S. S., et al. 2009. TRIM39 is a MOAP-1-binding protein that stabilizes MOAP-1 through inhibition of its poly-ubiquitination process. Exp. Cell Res. 315, 1313-1325.
40. Leschonsky, B., C. Ludwig, K. Bieler, and R. Wagner. 2007. Capsid stability and replication of human immunodeficiency virus type 1 are influenced critically by charge and size of Gag residue 183. J. Gen. Virol. 88, 207-216.
41. Li, Y., X. Li, M. Stremlau, M. Lee, and J. Sodroski. 2006. Removal of arginine 332 allows human TRIM5α to bind human immunodeficiency virus (HIV-1) capsids and to restrict infection. J. Virol. 80, 6738-6744.
42. Li, Y., A. Kar, and J. Sodroski. 2009. Target cell type-dependent modulation of human immunodeficiency virus (HIV-1) capsid disassembly by cyclophilin A. J. Virol. 83, 10951-10962.
43. 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.
44. Li, X., and J. Sodroski. 2008. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order selfassociation. J. Virol. 82, 11495-11502.
45. Liao, C. H., Y. Q. Kuang, H. L. Liu, T. Zheng, and B. Su. 2007. A novel fusion gene, TRIM5-Cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. AIDS Suppl. 8, 19-26.
46. Lin, T. Y., and M. Emerman. 2006. Cyclophilin A interacts with diverse lentiviral capsids. Retrovirology 3, 70.
47. Lin, T. Y., and M. Emerman. 2008. Determinants of cyclophilin A-dependent TRIM5 alpha restriction against HIV-1. Virology 379, 335-341.
48. Maegawa, H., T. Miyamoto, J.-I. Sakuragi, T. Shioda, and E. E. Nakayama. 2010. Contribution of RING domain to retrovirus restriction by TRIM5α depends on combination of host and virus. Virology 399, 212-220.
49. Matsuoka, S., E. Dam, D. Lecossier, F. Clavel, and A. J. Hance. 2009. Modulation of HIV-1 infectivity and cyclophilin A-dependence by Gag sequence and target cell type. Retrovirology 6, 21.
50. Meroni, G., and G. Diez-Roux. 2005. TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. Bioessays 27, 1147-1157.
51. Mische, C. C., et al. 2005. Retroviral restriction factor TRIM5alpha is a trimer. J. Virol. 79, 14446-14450.
52. Munk, C., S. M. Brandt, G. Luccero, and N. R. Landau. 2002. A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc. Natl. Acad. Sci. U. S. A. 99, 13843-13848.
53. Nakayama, E. E., H. Miyoshi, Y. Nagai, and T. Shioda. 2005. A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5α determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J. Virol. 79, 8870-8877.
54. Newman, R. M., et al. 2008. Evolution of a TRIM5-Cyp splice isoforms in old world monkeys. PLoS Pathog. 4, e1000003.
55. Niikura, T., et al. 2003. A tripartite motif protein TRIM11 binds and destabilizes Humanin, a neuroprotective peptide against Alzheimer's diseaserelevant insults. Eur. J. Neurosci. 17, 1150-1158.
56. Nisole, S., C. Lynch, J. P. Stoye, and M. W. Yap. 2004. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. U. S. A. 101, 13324-13328.
57. 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.
58. Owens, C. M., P. C. Yang, H. Göttlinger, and J. Sodroski. 2003. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, post-entry replication blocks in simian cells. J. Virol. 77, 726-731.
59. Owens, C. M., et al. 2004. 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. 78, 5423-5437.
60. Perez-Caballero, D., T. Hatziioannou, A. Yang, S. Cowan, and P. D. Bieniasz. 2005. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J. Virol. 79, 8969-8978.
61. Perez-Caballero, D., T. Hatziioannou, F. Zhang, S. Cowan, and P. D. Bieniasz. 2005. Restriction of human immunodeficiency virus type 1 by TRIMCypA occurs with rapid kinetics and independently of cytoplasmic bodies, ubiquitin, and proteasome activity. J. Virol. 79, 15567-15572.
62. 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.
63. Perron, M., M. Stremlau, and J. Sodroski. 2006. Two surface-exposed elements of the B30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5α. J. Virol. 80, 5631-5636.
64. Perron, M. J., et al. 2007. The human TRIM5 2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5α. restriction factor mediates accelerated uncoating of the N-tropic murine leukemia virus capsid. J. Virol. 81, 2138-2148.
65. Reymond, A., et al. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20, 2140-2151.
66. Rold, C. J., and C. Aiken. 2008. Proteasomal degradation of TRIM5(2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5α during retrovirus restriction. PLoS Pathog. 4, 5.
67. 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.
68. Sayah, D. M., E. Sokolskaja, L. Berthoux, and J. Luban. 2004. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
69. Schaller, T., L. M. Ylinen, B. L. Webb, S. Singh, and G. J. Towers. 2007. Fusion of cyclophilin A to Fv1 enables cyclosporine-sensitive restriction of human and feline immunodeficiency viruses. J. Virol. 81, 10055-10063.
70. Schwartz, O., V. Marechal, B. Friguet, F. Arenzana-Seisdedos, and J. M. Heard. 1998. Antiviral activity of the proteasome on incoming human immunodeficiency virus type 1. J. Virol. 72, 3845-3850.
71. Shibata, R., H. Sakai, M. Kawamura, K. Tokunaga, and A. Adachi. 1995. Early replication block of human immunodeficiency virus type 1 in monkey cells. J. Gen. Virol. 76, 3930-3937.
72. Sokolskaja, E., L. Berthous, and J. Luban. 2006. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J. Virol. 80, 2855-2862.
73. Song, B., et al. 2005. Retrovirus restriction by TRIM5(variants from Old World and New World primates. J. Virol. 79, 3930-3937.
74. 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.
75. Stremlau, M., et al. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427, 848-853.
76. 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.
77. Stremlau, M., et al. 2006. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5α restriction factor. Proc. Natl. Acad. Sci. U. S. A. 103, 5514-5519.
78. Stremlau, M., B. Song, H. Javanbakht, M. Perron, and J. Sodroski. 2006. Cyclophilin A, an auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 351, 112-120.
79. Towers, G., et al. 2000. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. U. S. A. 97, 12295-12299.
80. Towers, G. J., et al. 2003. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9, 1138-1143.
81. Virgen, C. A., Z. Kratova, P. D. Bieniasz, and T. Hatziioannou. 2008. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. U. S. A. 105, 3563-3568.
82. Wei, B. L., et al. 2005. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J. Virol. 79, 5705-5712.
83. Wilson, S. J., et al. 2008. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 105, 3557-3562.
84. Wu, X., J. L. Anderson, E. M. Campbell, A. M. Joseph, and T. J. Hope. 2006. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U. S. A. 103, 7465-7470.
85. Xie, Y., and A. Varshavsky. 1999. The E2-E3 interaction in the N-end rule pathway, the RING-H2 finger of E3 is required for the synthesis of multiubiquitin chain. EMBO J. 18, 6832-6844.
86. Xu, Q., M. Farah, J. M. Webster, and R. J. H. Wojcikiewicz. 2004. Bortezomib rapidly suppresses ubiquitin thiolesterification to ubiquitin-conjugating enzymes and inhibits ubiquitination of histones and type 1 inositol 1,4,5-trisphosphate receptor. Mol. Cancer Ther. 3, 1263-1269.
87. Yamauchi, K., K. Wada, K. Tanji, M. Tanaka, and T. Kamitani. 2008. Ubiquitination of E3 ubiquitin ligase TRIM5α and its potential role. FEBS J. 275, 1540-1555.
88. 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.
89. 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.
90. Yap, M. W., M. P. Dodding, and J. P. Stoye. 2006. Trim-cyclophilin A fusion proteins can restrict human immunodeficiency virus type 1 infection at two distinct phases in the viral life cycle. J. Virol. 80, 4061-4067.
91. Ying, M., Z. Zhan, W. Wang, and D. Chen. 2009. Origin and evolution of ubiquitin-conjugating enzymes from Guillardia theta nucleomorph to hominoid. Gene 447, 72-85.
92. 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.
93. Zhang, F., T. Hatziioannou, D. Perez-Caballero, D. Derse, and P. D. Bieniasz. 2006. Antiretroviral potential of human tripartite motif-5 and related proteins. Virology 353, 396-409.
94. Zhen, N., et al. 2002. Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416, 703-708.
95. Zheng, N., P. Wang, P. D. Jeffrey, and N. P. Pavletich. 2007. Structure of a c-Cbl-UbcH7 complex, RING domain function in ubiquitin-protein ligases. Cell 102, 533-539.