TRIM proteins and the innate immune response to viruses

Advances in Experimental Medicine and Biology

Volumn 770, Issue , 2012, Pages 93-104

  Yap, Melvyn W ^a   Stoye, Jonathan P ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; PROTEIN TRIM; PROTEIN TRIM21; PROTEIN TRIM22; PROTEIN TRIM25; PROTEIN TRIM28; PROTEIN TRIM30; REGULATOR PROTEIN; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; PROTEIN;

ARTICLE; CYTOKINE PRODUCTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION; UBIQUITINATION; VIRUS INACTIVATION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS RESISTANCE; CHEMISTRY; GENE SILENCING; IMMUNOLOGY; METABOLISM; PROTEIN MOTIF; REVIEW; VIRUS;

AMINO ACID MOTIFS; GENE SILENCING; HUMANS; IMMUNITY, INNATE; INTERFERON-BETA; PROTEINS; VIRUSES;

MLCS; MLOWN;

EID: 84878897622     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-5398-7_7     Document Type: Article

References (103)

1. Nisole S, Stoye JP, Saib A. TRIM family proteins: retroviral restri ction and antiviral defence. Nat Rev Microbiol 2005; 3(10):799-808.
2. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antivira l responses and virus countermeas ures. J Gen Viro12008; 89(Pt 1):1-4 7.
3. Geiss GK, Salvatore M, Tumpey TM, et al. Cellular transcription al profiling in influenza A virus -infected lung epithelial cells: the role of the nonstructural NS I protein in the evasion of the host innate defense and its potenti al contribution to pandem ic influenza. Proc NatlAcad Sci USA 2002 ; 99(1 6):10736-I074I .
4. Barr SD, Smiley JR, Bushman FD. The interferon response inhibits HIV particle product ion by induction ofTRIM22. PLoS Pathog 2008; 4(2):eI000007.
5. Rajs baum R, Stoye JP, O'Garra A. Type I interferon-dependent and -independent express ion of tripartite motif proteins in immune cells. Eur J Immunol2008; 38(3):619-630.
6. Sawyer SL, Wu Ll, Emerman M, et al. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Nat! Acad Sci USA 2005 ; 102(8):2832-2837.
7. Sawyer SL, Emerman M, Malik HS. Discordant evolution ofthe adjacent antiretrovira l genes TRIM22 and TRIM5 in mammals. PLoS Pathog 200 7; 3(12):e l 97.
8. Yap MW, Nisole S, Lynch C, et al. Trim5alpha protein restricts both HIV-I and murine leukemia virus. Proc Natl Acad Sci USA 2004 ; 101(29):10786-10 791.
9. Zhang F, Hatziioannou T, Perez-Caballero D, et al. Antiretroviral potential of human tripartite motif-5 and related proteins. Virology 2006; 353(2):396-409.
10. Stremlau M, Owens CM, Perron MJ, et al. The cytoplasmic body component TRIM5alpha restricts HIV-I infection in Old World monkeys. Nature 2004 ; 427(6977):848-853
11. lIatziioannou T, Perez-Caballero D, Yang A, et al. Retroviru s resistance factors Ref! and Lv I are species-specific variants ofTRIM5alpha. Proc Nat! Acad Sci USA 2004 ; 101(29): 10774-10 779.
12. Keckesova Z, Ylinen LM, Towers GJ. The human and African green monkey TRIM5alpha genes encode Ref! and Lvi retroviral restriction factor activ ities. Proc Nat!Acad Sci USA 2004; 101(29):10780-I0785.
13. PerronMJ, Strem lauM, Song Betal.TRIM5alpha mediates thepostentry blocktoN-tropic murine leukemia viruses in human cells. Proc Nat! Acad Sci USA 2004; 101(32):11827-11832.
14. Everett RD, Chelbi-Alix MK. PML and PML nuclear bodies: impli cations in antiviral defence. Biochimi e 2007; 89(6-7):8 I9-830.
15. Tissot C, Mechti N. Molecular clonin g of a new interferon-induced factor that represses human immunodeficiency virus type I long terminal repeat expression. J BioIChern 1995;270(25) :1489I-I4898 .
16. GackMU, Shin YC, Joo CH, et al. TRIM25 RING-finger E3 ubiquiti n ligase is essen tia l for RIG-I-medi ated antiviral activity. Nature 200 7; 446 (7138):916-920.
17. Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryon ic cell s. Cell 2007; 131(1):46-57.
18. Fridell RA, Harding LS, Bogerd HI', et al. Identification ofa novel human zinc finger protein that specifically interacts with the activation domain ofle ntiviral Tat proteins. Virology 1995; 209(2) :347-357
19. Orimo A, Tominaga N, Yoshimura K, et al. Molecular clo ning of ring finger protein 21 (RNF2 1)/ interferon-responsive finger protein (ifp I), which possesses two RING-B box-coiled coil domains in tandem. Genomics 2000; 69(1):1 43-149.
20. Hornung V, Ellegast J, Kim S, et al. 5' -Triphosphate RNA is the ligand for RIG-I. Science 2006; 314(5801):994-997.
21. Pichlmair A, Schulz O, Tan CP, et al. RIG-I-mediated antiviral respo nses to single-stranded RNA bearing 5' -phosphates. Science 2006 ; 314(5801) :997-1001.
22. Kato H, Takeuchi 0, Sato S, et al. Differential roles of MDA5 and RIG-I helicases in the recogn ition of RNA viruses. Nature 2006; 441(7089):101-105.
23. Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5(7):730-737 .
24. Johnson CL, Gale M, Jr. CARD games between virus and host get a new player. Trends Immunol 2006; 27 (1):1-4.
25. Meylan E, Tscho pp J, Karin M. Intracellul ar pattern recognition receptors in the host response. Nature 2006; 442(7098):39-44 .
26. Meylan E, Curran J, Hofmann K, et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targete d by hepatitis C virus. Nature 2005; 437(7062):1167-1172.
27. Seth RB, Sun L, Ea CK, et al. Identification and characterization of MAVS, a mitochond rial antiviral signaling protein that activat es NF-kappaB and IRF 3. Cell 2005; 122(5):669-682.
28. Xu LG, Wang YY, Han KJ, et al. VISA is an adapter protein required for virus -triggered If'N-beta signaling. Mol Cell 2005; 19(6):727-740.
29. KawaiT, Takahashi K, Sato S, et al. IPS-I, an adaptor triggering RIG-I-and Mda5-mediated type I interferon induction. Nat Immunol 2005; 6(10):981-988.
30. Karpov AV. Endogenous and exoge nous interferons in I-II V-infection. Eur J Med Res200 1;6 (12):507-524.
31. Bouazzaoui A, Kreutz M, Eisert V, et al. Stimulated trans-acting factor of 50 kDa (Staf50) inhibits HIV-1 replication in human monocyte-derived macrophages. Virology 2006; 356 (1-2):79-94.
32. Pal R, Reitz MS, Jr., Tschachler E, et al. Myristoylation of gag proteins of HIV-I plays an important role in virus assembly. AIDS Res Hum Retroviruses 1990; 6(6):721 -730 .
33. Gott linger HG, Sodroski JG, Haseltine WA. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type I . Proc Natl Acad Sci USA 1989; 86 (15):5781-5785.
34. Bryant M, Ratner L. Myristoyla tion-dependentreplication and assemb ly of human immunodeficiency virus I. Proc Nat! Acad Sci USA 1990; 87(2) :523-527.
35. Bock M, Stoye Jl', Endogeno us retrov iruses and the human germ line. Curr Opin Genet Dev 2000; 10(6):651-655.
36. Barklis E,Mulligan RC, Jaenisch R. Chromosomal position or virus mutation permits retrovirus express ion in embryonal carcinoma cells. Cell 1986; 47(3):391-399.
37. Teich NM, Weiss RA, Martin GR, et al. Virus infection of murine teratocarcinoma stem cell lines. Cell 1977; 12(4):973-982.
38. Feuer G, Taketo M, Haneca k RC, et al. Two blocks in Moloney murine leukemia virus expression in undifferentiated F9 embryonal carcinoma cells as determined by transie nt expression assays . J Virol 1989; 63(5) :2317-2324.
39. Loh Tl', Sievert LL, Scott RW. Proviral sequences that restrict retroviral expressio n in mouse embryo nal carcinoma cells . Mol Cell BioI 1987; 7 (10):3775-3784.
40. Urrutia R. KRAB-co ntaining zinc-finger repressor proteins . Geno me BioI 2003; 4(10):231
41. Friedma n JR, Fredericks WJ, Jensen DE, et al. KAp-l, a nove l corepressor for the highly conserved KRAB repression domai n. Genes Dev 1996; 10(16):2067-2078.
42. Peng II, Begg GE, Schultz DC, et al. Reconstitution of the KRAB-KAp-1 repressor complex: A model system for defining the molecular anatomy ofRING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol BioI 2000; 295(5) :1139-1 162.
43. Schultz DC, Ayya nathan K, Negorev 0, et al. SETDB I: a novel KAP-I-associated histone H3, lysine 9-specific methyltrans ferase that contributes to HI' I-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002; 16(8):919-932.
44. Sripathy SP, Stevens J, Schultz DC. The KAp l corep ressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heteroch romatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol Cell BioI 2006; 26(22) :8623-8638 .
45. Ivanov AV, Peng H, Yurchenko Vet al. PHD domain-mediated E3 ligase activity directs intramol ecular sumoylat ion of an adjacent bromodomain required for gene silencing. Mol Cell 2007; 28 (5):823-837.
46. Ylinen LM, Keckesova Z, Wilson SJ, et al. Differentia l restriction ofhuman immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5a lpha alle les. J Viro12005; 79(18) :11580-11587.
47. Yap MW, Lindema nn 0, Stanke N, et al. Restriction of foamy viruses by primate Trim5alpha. J Virol 2008; 82 (11):5429-5439 .
48. Sakuma R, Noser JA, Ohmine S, et al. Rhesus monkey TRIM5alpha restricts HIV-I production through rapid degrada tion of viral Gag poly proteins . Nat Med 2007; 13(5):631-635 .
49. Zhang F, Perez-Caballero 0, Hatziioannou T, et al. No effect of endogenous TRIM5alpha on HIV-I production. Nat Med 2008; 14(3):235 -236; author reply 236-238 .
50. Besnier C, Takeuchi Y, Towers G. Restriction of lentiviru s in monkeys. Proc Nat! Acad Sci USA 2002; 99(18) :11920-11925.
51. Cowan S, Hatziioannou T, Cunningham T, et al. Cellular inhibitors with Fv l -like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 2002; 99 (18):11914-11919.
52. Hatziioannou T, Cowan S, GoffSP, et al. Rest rictio n of multiple divergent retroviruses by Lv I and Ref! . EMBO J 2003; 22(3):38 5-394.
53. Hatziioannou T, Princiotta M, Piatak M, Jr., et al. Generation of simian-tropic HIV-I by restriction factor evasion. Scienc e 2006; 314(5796):95.
54. Nakayama EE, Miyoshi H, Nagai Y, et al. A specific regio n of 37 amino acid residues in the SPRY (B30 .2) domain ofAfrican green monkey TRIM5alpha determines spec ies-speci fic restriction of simian immunodeficiency virus SIVmac infection. J Virol 2005; 79 (14):8870 -8877.
55. StremlauM, PerronM,WelikalaSctal. Species-specificvariation in thc B30.2(SPRY) domainofTRIM5alpha determines the potency of human immunod eficiency virus restriction. J Viro12005 ; 79(5):3139-3145.
56. Yap MW, Nisole S, Stoye JP. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-I restriction. Curr BioI 2005; 15(1):73-78 .
57. Ohkura S, Yap MW, Sheldon T, et al. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J Viro12006; 80 (17):8554-8565.
58. Stremlau M, Perron M, Lee M et al. Specific recogni tion and accele rated uncoating of retrov iraIcapsids by the TRIM5alpha restri ction factor. Proc Nat! Acad Sci USA 2006; 103(14):5514-5519.
59. Stoye JP, Yap MW. Chance favors a prepared genome. Proc Natl Acad Sci USA 2008 ; 105(9):3177-3 178.
60. Nisole S, Lynch C, Stoye JP, et al. A Trim5-cyc1ophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc Natl Acad Sci USA 2004 .
61. Sayah OM, Sokolskaja E, Berthoux L, et al. Cyclo philin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004; 430(6999):569-573.
62. Liao CH, Kuang YQ, Liu HL, et al. A novel fusion gene, TRIM5-Cyc1ophilin A in the pig-tai led macaque determin es its susceptibility to HIV-I infection. Aids 200 7; 2 1 Suppl 8:S 19-26.
63. Virgen CA, Kratovac Z, Bieniasz PO, et al. Independent genesis of chimeric TRIM5-cyc1ophilin proteins in two primate specie s. Proc Natl Acad Sci USA 2008; 105(9):3563-3568.
64. Wilson SJ, Webb BL, Ylinen LMet al.lndepe ndent evolution ofan antiviralTRIMCyp in rhesus macaques. Proc Natl Acad Sci USA 2008; 105(9):3557-3562 .
65. Brennan G, Kozyrev Y, Hu SL. TRIMCyp expression in Old World primates Macaca nemestri na and Macaca fascicularis. Proc Natl Acad Sci USA 2008; 105(9):3569-3574.
66. Newman RM, Hall L, Kirmaier A, et al. Evolution ofa TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog 2008 ; 4(2):e 1000003.
67. Mische CC, Java nbakht H, Song B, et al. Retroviral restri ction factor TRIM5alpha is a trimer. J Viro12005 ; 79(22) :14446-14450.
68. Javanbakht H, Oiaz-Griffero F, Yuan W et al. The ability ofmultimerized cyclophilinA to restrict retrovirus infection. Virology 2007; 367(1): 19-29.
69. Yap MW, Mortuza GB, Taylor IA, et al. The design of artificial retroviral restriction factors. Virology 2007; 365(2):302-314 .
70. Perez-Caballero 0, Hatziioannou T, Yang A, et al. Human tri partite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Viro12005 ; 79 (14):8969-8978.
71. Javanbakht H, Oiaz-Griffero F, StremlauMet al. The contributionofRING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J Bioi Chern 2005; 280(29) :26933-26940.
72. Oiaz-Griffero F, Kar A, Lee M, et al. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp . Virology 2007; 369(2):400-410.
73. Xu L, Yang L, Moitra PK, et al. BTBO I and BTB02 colocalize to cytoplasmic bodies with the RBCCI tripartite motif protein, TRIM5del ta. Exp Cell Res 2003; 288(1):84-93.
74. Oiaz-Griffero F, LiX, Java nbakht Het al. Rapid turnover and polyubiquitylation ofthe retroviral restriction factor TRIM5. Viro logy 2006 ; 349(2) :300-3 15.
75. Yamauchi K, Wada K, Tanji K, et al. Ubiquitination of E3 ubiquiti n ligase TRIM5 alpha and its potential role. Febs J 2008; 275(7): 1540-1555.
76. Perez-Caballero O, Hatziioan nou T, Zhang F, et al. Restrictio n of human immunodeficiency virus type I by TRIM-CypA occurs with rapid kinetics and independently of cytoplasmic bodies, ubiquitin, and proteasome activity. J Virol 2005; 79(24):15567-15572.
77. Wu X, Ande rson JL, Campbell EM, et al. Proteasom e inhibitors uncouple rhesus TRIM5alpha restriction of HIV-I reverse transcription and infection. Proc Natl Acad Sci USA 2006; 103(19):7465-7470.
78. Ande rson JL, Campbell EM, Wu X, et al. Proteasom e inhibition reveals that a functio nal preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J Viro l 2006; 80(19) :9754-9760 .
79. Camp bell EM, Perez 0, Anderson JL, et al. Visualization ofa proteasome-independent intermediate during restri ct ion ofHIV-I by rhesus TRIM5alpha. J Cell BioI 2008; 180(3):549-561.
80. Chee AV, Lopez P, Pandolfi PPe t al. Promyelocytic leukemia proteinmediates interferon-based anti-herpes simplex virus I effects. J Viro12003; 77(12):710 1-7105
81. Bjorndal AS, Szekely L, Elgh F. Ebola virus infection inversely correlates with the overall express ion levels of promyelocytic leukaemia (PML) protein in cultur ed cells. BMC Microbiol 2003; 3:6.
82. Borden KL, Campbelldwyer EJ, Carlile GW, et al. Two RING finger proteins, the oncoprotein PML and the arenaviru s Z protein, coloca lize with the nuclear fraction of the ribosomal P proteins. J Virol 1998; 72(5):38 19-3826 .
83. OjavaniM, Rodas J, Lukashevich IS, et al. Role ofthe promyelocytic leukemia protein PML in the interferon sensitivity of lymphocytic choriome ningitis virus. J Virol 200 I ; 75 (13):6204-6208.
84. Asper M, Sternsdorf T, Hass M, et al. Inhibition of different Lassa virus strains by alpha and gamma interferons and comparison with a less pathogenic arenavirus . J Viro l 2004; 78(6):3162 -3 169.
85. Bonilla WV, Pinschewer DO, Klenerman Pet al. Effects of promyelocytic leukemia protein on virus-host balance. J Viro12002 ; 76(8):3810-3818 .
86. Chelbi-AlixMK,Quignon F, Pelicano Letal.Resistance to virus infection conferred by the interferon-i nduced promyelocytic leukemia protein. J Viro l 1998; 72(2) : I043-105 1.
87. Blondel 0, Regad T, Poisson N, et al. Rabies virus P and small P products interact directly with PML and reorganize PML nuclear bodies. Oncogene 2002 ; 21(52) :7957-7970.
88. Chelbi-Alix MK, Vidy A, EI Bougri ni J, et al. Rabies viral mechanisms to esca pe the IFN system: the viral protein P interferes with IRF-3, Stat I, and PML nuclear bodies. J Inter feron Cytokine Res 2006; 26(5):271-280.
89. Turelli P, Ooucas V, Craig Eet al.Cytoplasmic recru itmento flN l1 andPMLon incoming HIV preintegration complexes: interference with early steps of viral replication. Mol Cell 2001; 7(6):1245-1254.
90. Regad T, SaibA, Lallemand-Breitenbach Ve t al.PMLmediates the interferon-induced antiv iralstate against a complex retrovirus via its associatio n with the viral transactivator. EMBO J 2001 ; 20 (13):3495-3505
91. Everett RO, Rechter S, Papior P, et al. PML contributes to a cellular mechanism of repression of herpes simplex virus type 1 infection that is inactivated by ICPO. J Viro1 2006 ; 80(16):7995-8005 .
92. Uchil PO, Quin lan BO,Chan WT, et al. TRIM E3 ligases interfere with ear ly and late stages ofthe retroviral life cycle. PLoS Pathog 2008; 4(2):e16.
93. Bancherea u J, Pascual V.Type I interferon in systemic lupus erythematos us and other autoimmune diseases. Immunity 2006; 25(3):383-392.
94. Lin R, Heylbroeck C, Pitha PM, et al. Virus-de pendent phosphorylation of the IRP-3 transcription factor regulates nuclear translocat ion, transactivatio n potential, and proteasome-mediated degradation. Mol Cell Bioi 1998; 18(5):2986-2996.
95. Saitoh T, Tun-Kyi A, Ryo A, et al. Negative regulation of interfero n-regulatory factor 3-de pendent innate antiv iral response by the prolyl isomerase Pin I . Nat Immunol 2006; 7(6):598-605.
96. Bibeau-Poirier A, Gravel SP, Clement JF, et al. Involvement of the IkappaB kinase (IKK)-related kinases tank-binding kinase 1/IKKi and cullin-based ubiquitin ligases in IFN regulatory factor-3 degrada tion. J Immunol 2006; 177(8):5059-5067.
97. Higgs R, Ni Gabhann J, Ben Larbi N, et al. The E3 ubiquitin ligase R052 negatively reg ulates lPN-beta production postpathogen recognition by polyubiquitin-mediated degra dation oflRF3. J Immunol 2008; 181(3):1780-1786.
98. Shi M, Oeng W, Bi E, et al. TRIM30 alpha negatively regulates TLR-mediated NF-ka ppa B act ivation by targeting TAB2 and TAB3 for degrada tion. Nat Immunol 2008; 9(4) :369-377.
99. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003; 21:335-376.
100. Kishida S, Sanjo H,AkiraSetal.TAK I-binding protein 2 facilitates ubiquitination ofTRAF6 and assembly ofTRAF6 with IKK in the IL-I signaling pathway. Genes Cells 2005; 10(5):447-454
101. Asaoka K, Ikeda K, Hishinuma T, et al. A retrov irus restriction factor TRIM5al pha is transcriptionally regulated by interferon s. Biochem Biophys Res Commun 2005; 338(4):1950-1956.
102. CarthagenaL, PariseMC, RingeardMetal. lmplicationofTRIM alpha and TRIMCyp in interferon-induced anti-retroviral restriction activitie s. Retroviro logy 2008; 5:59.
103. Rold CJ, Aiken C. Proteasomal degradation of TRIM5al pha during retrovirus restriction. PLoS Pathog 2008; 4(5):e100007 4.