Characterization of a core fragment of the rhesus monkey TRIM5 protein

BMC Biochemistry

Volumn 12, Issue 1, 2011, Pages

  Kar, Alak K ^a   Mao, Youdong ^a   Bird, Gregory ^a   Walensky, Loren ^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

B BOX 2 PROTEIN; BCCL2 PROTEIN; PROTEIN; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; HYBRID PROTEIN; MULTIPROTEIN COMPLEX; TRIM5(ALPHA) PROTEIN, RHESUS MONKEY; ZINC;

ARTICLE; CIRCULAR DICHROISM; LIGHT SCATTERING; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RHESUS MONKEY; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DIMERIZATION; ESCHERICHIA COLI; GENETICS; ISOLATION AND PURIFICATION; MACACA MULATTA; METABOLISM; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; TEMPERATURE;

MACACA MULATTA;

ANIMALS; DIMERIZATION; ESCHERICHIA COLI; MACACA MULATTA; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; PROTEINS; RECOMBINANT FUSION PROTEINS; TEMPERATURE; ZINC;

EID: 78650769957     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-12-1     Document Type: Article

References (72)

1. Early replication block of human immunodeficiency virus type 1 in monkey cells. R Shibata H Sakai M Kawamura K Tokunaga A Adachi, J Gen Virol 1995 76 Pt 11 2723 2730 10.1099/0022-1317-76-11-2723 7595379
2. Restriction of HIV-1 (subtype B) replication at the entry step in rhesus macaque cells. S Himathongkham PA Luciw, Virology 1996 219 2 485 488 10.1006/viro.1996.0276 8638416
3. Species-specific, postentry barriers to primate immunodeficiency virus infection. W Hofmann D Schubert J LaBonte L Munson S Gibson J Scammell P Ferrigno J Sodroski, J Virol 1999 73 12 10020 10028 10559316
4. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. S Cowan T Hatziioannou T Cunningham MA Muesing HG Gottlinger PD Bieniasz, Proc Natl Acad Sci USA 2002 99 18 11914 11919 10.1073/pnas.162299499 12154227
5. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. B Song H Javanbakht M Perron DH Park M Stremlau J Sodroski, J Virol 2005 79 7 3930 3937 10.1128/JVI.79.7.3930-3937.2005 15767395
6. Anti-retroviral activity of TRIM5alpha. EE Nakayama T Shioda, Rev Med Virol 2010 20 2 77 92 10.1002/rmv.637 20049904
7. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. M Stremlau CM Owens MJ Perron M Kiessling P Autissier J Sodroski, Nature 2004 427 6977 848 853 10.1038/nature02343 14985764
8. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. T Hatziioannou D Perez-Caballero A Yang S Cowan PD Bieniasz, Proc Natl Acad Sci USA 2004 101 29 10774 10779 10.1073/pnas.0402361101 15249685
9. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Z Keckesova LM Ylinen GJ Towers, Proc Natl Acad Sci USA 2004 101 29 10780 10785 10.1073/pnas.0402474101 15249687
10. Primate lentivirus capsid sensitivity to TRIM5 proteins. Z Kratovac CA Virgen F Bibollet-Ruche BH Hahn PD Bieniasz T Hatziioannou, J Virol 2008 82 13 6772 6777 10.1128/JVI.00410-08 18417575
11. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. MW Yap S Nisole C Lynch JP Stoye, Proc Natl Acad Sci USA 2004 101 29 10786 10791 10.1073/pnas.0402876101 15249690
12. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. LM Ylinen Z Keckesova SJ Wilson S Ranasinghe GJ Towers, J Virol 2005 79 18 11580 11587 10.1128/JVI.79.18.11580-11587.2005 16140735
13. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. F Diaz-Griffero A Kar M Lee M Stremlau E Poeschla J Sodroski, Virology 2007 369 2 400 410 10.1016/j.virol.2007.08.032 17920096
14. Modulation of retroviral restriction and proteasome inhibitor-resistant turnover by changes in the TRIM5alpha B-box 2 domain. F Diaz-Griffero A Kar M Perron SH Xiang H Javanbakht X Li J Sodroski, J Virol 2007 81 19 10362 10378 10.1128/JVI.00703-07 17626085
15. A human TRIM5alpha B30.2/SPRY domain mutant gains the ability to restrict and prematurely uncoat B-tropic murine leukemia virus. F Diaz-Griffero M Perron K McGee-Estrada R Hanna PV Maillard D Trono J Sodroski, Virology 2008 378 2 233 242 10.1016/j.virol.2008.05.008 18586294
16. A B-box 2 surface patch important for TRIM5alpha self-association, capsid binding avidity, and retrovirus restriction. F Diaz-Griffero XR Qin F Hayashi T Kigawa A Finzi Z Sarnak M Lienlaf S Yokoyama J Sodroski, J Virol 2009 83 20 10737 10751 10.1128/JVI.01307-09 19656869
17. The human TRIM5alpha restriction factor mediates accelerated uncoating of the N-tropic murine leukemia virus capsid. MJ Perron M Stremlau M Lee H Javanbakht B Song J Sodroski, J Virol 2007 81 5 2138 2148 10.1128/JVI.02318-06 17135314
18. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. S Sebastian J Luban, Retrovirology 2005 2 40 10.1186/1742-4690-2-40 15967037
19. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. M Stremlau M Perron M Lee Y Li B Song H Javanbakht F Diaz-Griffero DJ Anderson WI Sundquist J Sodroski, Proc Natl Acad Sci USA 2006 103 14 5514 5519 10.1073/pnas.0509996103 16540544
20. TRIM/RBCC, a novel class of 'single protein RING finger' E3 ubiquitin ligases. G Meroni G Diez-Roux, Bioessays 2005 27 11 1147 1157 10.1002/bies.20304 16237670
21. The tripartite motif family identifies cell compartments. A Reymond G Meroni A Fantozzi G Merla S Cairo L Luzi D Riganelli E Zanaria S Messali S Cainarca,, et al. EMBO J 2001 20 9 2140 2151 10.1093/emboj/20.9.2140 11331580
22. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. H Javanbakht F Diaz-Griffero M Stremlau Z Si J Sodroski, J Biol Chem 2005 280 29 26933 26940 10.1074/jbc.M502145200 15897199
23. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. D Perez-Caballero T Hatziioannou A Yang S Cowan PD Bieniasz, J Virol 2005 79 14 8969 8978 10.1128/JVI.79.14.8969-8978.2005 15994791
24. Contribution of RING domain to retrovirus restriction by TRIM5alpha depends on combination of host and virus. H Maegawa T Miyamoto J Sakuragi T Shioda EE Nakayama, Virology 2010 399 212 220 10.1016/j.virol.2010.01.003 20110098
25. Functional interplay between the B-box 2 and the B30.2(SPRY) domains of TRIM5alpha. X Li B Song SH Xiang J Sodroski, Virology 2007 366 2 234 244 10.1016/j.virol.2007.04.022 17543365
26. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. X Li J Sodroski, J Virol 2008 82 23 11495 11502 10.1128/JVI.01548-08 18799578
27. Characterization of TRIM5alpha trimerization and its contribution to human immunodeficiency virus capsid binding. H Javanbakht W Yuan DF Yeung B Song F Diaz-Griffero Y Li X Li M Stremlau J Sodroski, Virology 2006 353 1 234 246 10.1016/j.virol.2006.05.017 16808955
28. Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. AK Kar F Diaz-Griffero Y Li X Li J Sodroski, J Virol 2008 82 23 11669 11681 10.1128/JVI.01559-08 18799572
29. Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. CR Langelier V Sandrin DM Eckert DE Christensen V Chandrasekaran SL Alam C Aiken JC Olsen AK Kar JG Sodroski,, et al. J Virol 2008 82 23 11682 11694 10.1128/JVI.01562-08 18799573
30. TRIM5alpha and TRIMCyp form apparent hexamers and their multimeric state is not affected by exposure to restriction-sensitive viruses or by treatment with pharmacological inhibitors. ME Nepveu-Traversy J Berube L Berthoux, Retrovirology 2009 6 100 10.1186/1742-4690-6-100 19886997
31. Molecular evolution of the antiretroviral TRIM5 gene. WE Johnson SL Sawyer, Immunogenetics 2009 61 3 163 176 10.1007/s00251-009-0358-y 19238338
32. Evolution of TRIM5alpha B30.2 (SPRY) domain in New World primates. EA Soares AN Menezes CG Schrago MA Moreira CR Bonvicino MA Soares HN Seuanez, Infect Genet Evol 2010 10 246 253 10.1016/j.meegid.2009.11.012 19931648
33. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. SL Sawyer LI Wu M Emerman HS Malik, Proc Natl Acad Sci USA 2005 102 8 2832 2837 10.1073/pnas.0409853102 15689398
34. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. B Song B Gold C O'Huigin H Javanbakht X Li M Stremlau C Winkler M Dean J Sodroski, J Virol 2005 79 10 6111 6121 10.1128/JVI.79.10.6111-6121.2005 15857996
35. Molecular evolution of the antiretroviral TRIM5 gene. WE Johnson SL Sawyer, Immunogenetics 2009 61 3 163 176 10.1007/s00251-009-0358-y 19238338
36. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. SL Sawyer M Emerman HS Malik, PLoS Pathog 2007 3 197 10.1371/journal.ppat.0030197 18159944
37. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. M Stremlau M Perron S Welikala J Sodroski, J Virol 2005 79 5 3139 3145 10.1128/JVI.79.5. 3139-3145.2005 15709033
38. Impact of a single amino acid in the variable region 2 of the Old World monkey TRIM5alpha SPRY (B30.2) domain on anti-human immunodeficiency virus type 2 activity. K Kono K Bozek FS Domingues T Shioda EE Nakayama, Virology 2009 388 1 160 168 10.1016/j.virol.2009.03.004 19342071
39. Two surface-exposed elements of the B30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5alpha. MJ Perron M Stremlau J Sodroski, J Virol 2006 80 11 5631 5636 10.1128/JVI.00219-06 16699044
40. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. S Ohkura MW Yap T Sheldon JP Stoye, J Virol 2006 80 17 8554 8565 10.1128/JVI.00688-06 16912305
41. 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. EE Nakayama H Miyoshi Y Nagai T Shioda, J Virol 2005 79 14 8870 8877 10.1128/JVI.79.14.8870-8877.2005 15994780
42. Removal of arginine 332 allows human TRIM5alpha to bind human immunodeficiency virus capsids and to restrict infection. Y Li X Li M Stremlau M Lee J Sodroski, J Virol 2006 80 14 6738 6744 10.1128/JVI.00270-06 16809279
43. Restriction of an extinct retrovirus by the human TRIM5alpha antiviral protein. SM Kaiser HS Malik M Emerman, Science 2007 316 1756 1758 10.1126/science.1140579 17588933
44. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. MW Yap S Nisole JP Stoye, Curr Biol 2005 15 1 73 78 10.1016/j.cub.2004.12.042 15649369
45. Interfering residues narrow the spectrum of MLV restriction by human TRIM5 PV Maillard S Reymond F Serhan P Turelli D Trono, PLoS Pathog 2007 3 200 10.1371/journal.ppat.0030200 18166079
46. TRIM5alpha modulates immunodeficiency virus control in rhesus monkeys. SY Lim T Rogers T Chan JB Whitney J Kim J Sodroski N Letvin, PLoS Pathog 2010 6 1 1000738 10.1371/journal.ppat.1000738 20107597
47. The specificity of TRIM5 alpha-mediated restriction is influenced by its coiled-coil domain. PV Maillard G Ecco M Ortiz D Trono, J Virol 2010 84 5790 5801 10.1128/JVI.02413-09 20219908
48. Acute promyelocytic leukemia: from genetics to treatment. F Grignani M Fagioli M Alcalay L Longo PP Pandolfi E Donti A Biondi F Lo Coco PG Pelicci, Blood 1994 83 10 25 8274729
49. A candidate gene for familial Mediterranean fever. The French FMF Consortium, Nature Genet 1997 17 25 31 10.1038/ng0997-25 9288094
50. Ancient missense mutations in a new member of the RoRet gene family are likely to cause familial Mediterranean fever. The International FMF Consortium, Cell 1997 90 797 807 10.1016/S0092-8674(00)80539-5 9288758
51. Opitz G/BBB syndrome, a defect of midline development is due to mutations in a new RING finger gene on Xp22. NA Quaderi S Schweiger K Gaudenz B Franco EL Rugarli W Berger GJ Feldman,, et al. Nature Genet 1997 17 285 291 10.1038/ng1197-285 9354791
52. A 52-kD protein is a novel component of the SS-A/Ro antigenic particle. E Ben-Chetrit EK Chan KF Sullivan EM Tan, J Exp Med 1988 167 1560 1571 10.1084/jem.167.5.1560 3367095
53. Anti-Ro(SSA) positive rheumatoid arthritis (RA): a clinicoserological group of patients with high incidence of D-penicillamine side effects. HM Moutsopoulos FN Skopouli AK Sarras C Tsampoulas AK Mavridis SH Constantopoulos PJ Maddison, Ann Rheum Dis 1985 44 215 219 10.1136/ard.44.4.215 3872635
54. Gene encoding a new RING-B-box-coiled-coil protein is mutated in mulibrey nanism. K Avela M Lipsanen-Nyman N Idanheimo E Seemanova S Rosengren TP Makela J Perheentupa A Chapelle AE Lehesjoki, Nature Genet 2000 25 298 301 10.1038/77053 10888877
55. Solution structure of the zinc finger, C3HC4 type (RING finger) domain of tripartite motif-containing protein 5. H Abe K Miyamoto N Tochio S Koshiba T Kigawa S Yokoyama, RCSB Protein Data Bank, Piscataway, NJ. vol. RIKEN Structural Genomics/Proteomics Initiative (RSGI), Accession number 2ecv RIKEN Structural Genomics/Proteomics Initiative (RSGI) 2008
56. Structure of the MID1 tandem B-boxes reveals an interaction reminiscent of intermolecular ring heterodimers. H Tao BN Simmons S Singireddy M Jakkidi KM Short TC Cox MA Massiah, Biochemistry 2008 47 8 2450 2457 10.1021/bi7018496 18220417
57. Structural analysis of B-Box 2 from MuRF1: identification of a novel self-association pattern in a RING-like fold. M Mrosek S Meier Z Ucurum-Fotiadis E von Castelmur E Hedbom A Lustig S Grzesiek D Labeit S Labeit O Mayans, Biochemistry 2008 47 40 10722 10730 10.1021/bi800733z 18795805
58. Solution structure of the MID1 B-box2 CHC(D/C)C(2)H(2) zinc-binding domain: insights into an evolutionarily conserved RING fold. MA Massiah JA Matts KM Short BN Simmons S Singireddy Z Yi TC Cox, J Mol Biol 2007 369 1 1 10 10.1016/j.jmb.2007.03.017 17428496
59. Solution structure of the RBCC/TRIM B-box1 domain of human MID1: B-box with a RING. MA Massiah BN Simmons KM Short TC Cox, J Mol Biol 2006 358 2 532 545 10.1016/j.jmb.2006.02.009 16529770
60. The SPRY domain of SSB-2 adopts a novel fold that presents conserved Par-4-binding residues. SL Masters S Yao TA Willson JG Zhang KR Palmer BJ Smith JJ Babon NA Nicola RS Norton SE Nicholson, Nat Struct Mol Biol 2006 13 1 77 84 10.1038/nsmb1034 16369487
61. Structural basis for protein recognition by B30.2/SPRY domains. JS Woo HY Suh SY Park BH Oh, Mol Cell 2006 24 6 967 976 10.1016/j.molcel.2006.11.009 17189197
62. Structure of the PRYSPRY-domain: implications for autoinflammatory diseases. C Grutter C Briand G Capitani PR Mittl S Papin J Tschopp MG Grutter, FEBS Lett 2006 580 1 99 106 10.1016/j.febslet.2005.11.076 16364311
63. Structural basis for PRYSPRY-mediated tripartite motif (TRIM) protein function. LC James AH Keeble Z Khan DA Rhodes J Trowsdale, Proc Natl Acad Sci USA 2007 104 15 6200 6205 10.1073/pnas.0609174104 17400754
64. SPRY domain-containing SOCS box protein 2: crystal structure and residues critical for protein binding. Z Kuang S Yao Y Xu RS Lewis A Low SL Masters TA Willson TB Kolesnik SE Nicholson TJ Garrett,, et al. J Mol Biol 2009 386 3 662 674 10.1016/j.jmb.2008.12.078 19154741
65. Predicting coiled coils from protein sequences. A Lupas M Van Dyke J Stock, Science 1991 252 1162 1164 10.1126/science.252.5009.1162
66. Coiled-coils in alpha-helix-containing proteins: analysis of the residue types within the heptad repeat and the use of these data in the prediction of coiled coils in other proteins. DAD Parry, Biosci Rep 1981 2 1017 1024 10.1007/BF01122170
67. Predicting coiled coils by use of pairwise residue correlations. B Berger DB Wilson E Wolf T Tonchev M Milla PS Kim, Proc Natl Acad Sci USA 1995 92 8259 8263 10.1073/pnas.92.18.8259 7667278
68. Retroviral restriction factor TRIM5alpha is a trimer. CC Mische H Javanbakht B Song F Diaz-Griffero M Stremlau B Strack Z Si J Sodroski, J Virol 2005 79 22 14446 14450 10.1128/JVI.79.22.14446-14450.2005 16254380
69. Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. L Whitmore BA Wallace, Biopolymers 2008 89 392 400 10.1002/bip.20853 17896349
70. High-throughput limited proteolysis/mass spectrometry for protein domain elucidation. X Gao K Bain JB Bonanno M Buchanan D Henderson D Morimer C Marsch JA Reynes JM Sauder K Schwinn C Thai SK Burley, J Struct Funct Genomics 2005 6 129 134 10.1007/s10969-005-1918-5 16211509
71. Crystallizing proteins: a rational approach? A D'Arcy, Acta Cryst 1994 D50 469 471
72. Dynamic light scattering in evaluating crystallizability of macromolecules. A Ferre-D'Amare S Burley, Methods in Enzymol 1997 276 157 166