RING domain mutations uncouple TRIM5α restriction of HIV-1 from inhibition of reverse transcription and acceleration of uncoating

Journal of Virology

Volumn 86, Issue 3, 2012, Pages 1717-1727

  Roa, Amanda ^a   Hayashi, Fumiaki ^c   Yang, Yang ^a   Lienlaf, Maritza ^a   Zhou, Jing ^b   Shi, Jiong ^b   Watanabe, Satoru ^c   Kigawa, Takanori ^c,d   Yokoyama, Shigeyuki ^c,e   Aiken, Christopher ^b   Diaz Griffero, Felipe ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; TRIPARTITE MOTIF PROTEIN 5;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MURINE LEUKEMIA VIRUS; N TROPIC MURINE LEUKEMIA VIRUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PELLETABLE CAPSID; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN RESTRICTION; REVERSE TRANSCRIPTION; RING FINGER MOTIF; VIRUS CAPSID; VIRUS DNA CELL DNA INTERACTION; VIRUS ENTRY; VIRUS INHIBITION; VIRUS MUTANT; VIRUS MUTATION; VIRUS UNCOATING;

ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; CELL LINE; DNA PROBES; DOGS; HIV LONG TERMINAL REPEAT; HIV-1; HUMANS; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; THYMOCYTES; TRANSCRIPTION, GENETIC; VIRUS UNCOATING;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; MURINE LEUKEMIA VIRUS;

EID: 84863140722     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05811-11     Document Type: Article

References (59)

1. Anderson JL, et al. 2006. Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J. Virol. 80:9754 -9760.
2. Aoki M, et al. 2009. Automated system for high-throughput protein production using the dialysis cell-free method. Protein Expr. Purif. 68: 128-136.
3. Arfi V, et al. 2009. Characterization of the behavior of functional viral genomes during the early steps of human immunodeficiency virus type 1 infection. J. Virol. 83:7524 -7535.
4. Arfi V, et al. 2008. Characterization of the early steps of infection of primary blood monocytes by human immunodeficiency virus type 1. J. Virol. 82:6557- 6565.
5. Berube J, Bouchard A, Berthoux L. 2007. Both TRIM5alpha and TRIMCyp have only weak antiviral activity in canine D17 cells. Retrovirology 4:68.
6. Bock M, Bishop KN, Towers G, Stoye JP. 2000. Use of a transient assay for studying the genetic determinants of Fv1 restriction. J. Virol. 74: 7422-7430.
7. Butler SL, Hansen MS, Bushman FD. 2001. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 7:631- 634.
8. Diaz-Griffero F. 2011. Caging the beast: TRIM5_ binding to the HIV-1 core. Viruses 3:423- 428.
9. Diaz-Griffero F, Gallo DE, Hope TJ, Sodroski J. 2011. Trafficking of some old world primate TRIM5alpha proteins through the nucleus. Retrovirology 8:38.
10. Diaz-Griffero F, et al. 2007. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. Virology 369: 400-410.
11. Diaz-Griffero F, et al. 2007. Modulation of retroviral restriction and proteasome inhibitor-resistant turnover by changes in the TRIM5alpha B-box 2 domain. J. Virol. 81:10362-10378.
12. Diaz-Griffero F, et al. 2006. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 349:300 -315.
13. 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.
14. 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.
15. Diaz-Griffero F, et al. 2006. Requirements for capsid-binding and an effector function in TRIMCyp-mediated restriction of HIV-1. Virology 351:404-419.
16. Dismuke DJ, Aiken C. 2006. Evidence for a functional link between uncoating of the human immunodeficiency virus type 1 core and nuclear import of the viral preintegration complex. J. Virol. 80:3712-3720.
17. Forshey BM, Aiken C. 2003. Disassembly of human immunodeficiency virus type 1 cores in vitro reveals association of Nef with the subviral ribonucleoprotein complex. J. Virol. 77:4409-4414.
18. Forshey BM, von Schwedler U, Sundquist WI, Aiken C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76:5667-5677.
19. Ganser BK, Li S, Klishko VY, Finch JT, Sundquist WI. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283:80-83.
20. Ganser-Pornillos BK, et al. 2011. Hexagonal assembly of a restricting TRIM5alpha protein. Proc. Natl. Acad. Sci. U. S. A. 108:534 -539.
21. Ganser-Pornillos BK, von Schwedler UK, Stray KM, Aiken C, Sundquist WI. 2004. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78:2545-2552.
22. Javanbakht H, Diaz-Griffero F, Stremlau M, Si Z, Sodroski J. 2005. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J. Biol. Chem. 280:26933-26940.
23. Kar AK, Diaz-Griffero F, Li Y, Li X, Sodroski J. 2008. Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. J. Virol. 82:11669 -11681.
24. Keckesova Z, Ylinen LM, Towers GJ. 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.
25. Kigawa T, et al. 1999. Cell-free production and stable-isotope labeling of milligram quantities of proteins. FEBS Lett. 442:15-19.
26. Kim J, Tipper C, Sodroski J. 2011. Role of TRIM5{alpha} RING domain E3 ubiquitin ligase activity in capsid disassembly, reverse transcription blockade, and restriction of simian immunodeficiency virus. J. Virol. 85: 8116-8132.
27. 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:e1000462.
28. Langelier CR, et al. 2008. Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. J. Virol. 82:11682-11694.
29. Li X, Sodroski J. 2008. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J. Virol. 82:11495-11502.
30. Li X, Yeung DF, Fiegen AM, Sodroski J. 2011. Determinants of the higher-order association of the restriction factor TRIM5{alpha} and other tripartite motif (TRIM) proteins. J. Biol. Chem. 286:27959 -27970.
31. Lienlaf M, et al. 2011. Contribution of E3-ubiquitin ligase activity to HIV-1 restriction by TRIM5{alpha}rh: structure of the RING domain of TRIM5{alpha}. J. Virol. 85:8725- 8737.
32. Maegawa H, Miyamoto T, Sakuragi J, Shioda T, Nakayama EE. 2010. Contribution of RING domain to retrovirus restriction by TRIM5alpha depends on combination of host and virus. Virology 399:212-220.
33. Matsuda T, et al. 2006. Cell-free synthesis of zinc-binding proteins. J. Struct. Funct. Genomics 7:93-100.
34. Mrosek M, et al. 2008. Structural analysis of B-Box 2 from MuRF1: identification of a novel self-association pattern in a RING-like fold. Biochemistry 47:10722-10730.
35. Nakayama EE, Miyoshi H, Nagai Y, Shioda T. 2005. 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. 79:8870-8877.
36. Ohagen A, Gabuzda D. 2000. Role of Vif in stability of the human immunodeficiency virus type 1 core. J. Virol. 74:11055-11066.
37. Ohkura S, et al. 2011. Novel escape mutants suggest an extensive TRIM5alpha binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog. 7:e1002011.
38. Owens CM, Yang PC, Gottlinger H, Sodroski J. 2003. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J. Virol. 77: 726-731.
39. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD. 2005. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J. Virol. 79:8969-8978.
40. Perez-Caballero D, Hatziioannou T, Zhang F, Cowan S, Bieniasz PD. 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.
41. Perron MJ, et al. 2007. The human TRIM5alpha restriction factor mediates accelerated uncoating of the N-tropic murine leukemia virus capsid. J. Virol. 81:2138 -2148.
42. Pertel T, et al. 2011. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472:361-365.
43. Reymond A, et al. 2001. The tripartite motif family identifies cell compartments. EMBO J. 20:2140 -2151.
44. Rold CJ, Aiken C. 2008. Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog. 4:e1000074.
45. Sawyer SL, Wu LI, Emerman M, Malik HS. 2005. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U. S. A. 102:2832-2837.
46. Sayah DM, Sokolskaja E, Berthoux L, Luban J. 2004. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430:569 -573.
47. Sebastian S, Luban J. 2005. TRIM5alpha selectively binds a restrictionsensitive retroviral capsid. Retrovirology 2:40.
48. Shi J, Zhou J, Shah VB, Aiken C, Whitby K. 2011. Small-molecule inhibition of human immunodeficiency virus type 1 infection by virus capsid destabilization. J. Virol. 85:542-549.
49. Song B, et al. 2005. TRIM5alpha association with cytoplasmic bodies is not required for antiretroviral activity. Virology.
50. 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.
51. Stremlau M, et al. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853.
52. 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.
53. Stremlau M, Perron M, Welikala S, Sodroski J. 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.
54. Suzuki Y, Craigie R. 2007. The road to chromatin - nuclear entry of retroviruses. Nat. Rev. Microbiol. 5:187-196.
55. Wu X, Anderson JL, Campbell EM, Joseph AM, Hope TJ. 2006. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U. S. A. 103: 7465-7470.
56. Yabuki T, et al. 2007. A robust two-step PCR method of template DNA production for high-throughput cell-free protein synthesis. J. Struct. Funct. Genomics 8:173-191.
57. Yamauchi K, Wada K, Tanji K, Tanaka M, Kamitani T. 2008. Ubiquitination of E3 ubiquitin ligase TRIM5 alpha and its potential role. FEBS J. 275:1540 -1555.
58. Yap MW, Dodding MP, Stoye JP. 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.
59. Yap MW, Nisole S, Stoye JP. 2005. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr. Biol. 15:73-78.