Advertisement

TRIM Proteins and the Innate Immune Response to Viruses

  • Melvyn W. Yap
  • Jonathan P. Stoye
Part of the Advances in Experimental Medicine and Biology book series (AEMB)

Abstract

Many TRIM proteins are up-regulated by interferons, suggesting that they might be involved in the innate immune response against viruses. Indeed, some members of the family have been shown to be either regulators of the interferon pathways or to be directly involved in the restriction of viruses. While the mechanisms of actions are varied, the modular organization of these proteins seems to be important for their activities, many of which are linked to the ubiquitination/proteasomal degradation system. The different domains enable the TRIM proteins to interact with either viral components or signaling molecules in the interferon induction pathways.

Keywords

Human Immunodeficiency Virus Type Coiled Coil Embryonal Carcinoma Cell Foamy Virus Ring Motif 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Nisole S, Stoye JP, Saib A. TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 2005; 3(10):799–808.PubMedCrossRefGoogle Scholar
  2. 2.
    Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus counter measures. J Gen Virol 2008; 89(Pt 1):1–47.PubMedCrossRefGoogle Scholar
  3. 3.
    Geiss GK, Salvatore M, Tumpey TM et al. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci USA2002; 99(16): 10736–10741.Google Scholar
  4. 4.
    Barr SD, Smiley JR, Bushman FD. The interferon response inhibits HIV particle production by induction of TRIM22. PLoS Pathog 2008; 4(2):e1000007.PubMedCrossRefGoogle Scholar
  5. 5.
    Rajsbaum R, Stoye JP, O’Garra A. Type I interferon-dependent and-independent expression of tripartite motif proteins in immune cells. Eur J Immunol 2008; 38(3):619–630.PubMedCrossRefGoogle Scholar
  6. 6.
    Sawyer SL, Wu LI, Emerman M et al. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 2005; 102(8):2832–2837.PubMedCrossRefGoogle Scholar
  7. 7.
    Sawyer SL, Emerman M, Malik HS. Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog 2007; 3(12):el97.CrossRefGoogle Scholar
  8. 8.
    Yap MW, Nisole S, Lynch C et al. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci USA 2004; 101(29):10786–10791.PubMedCrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 10.
    Stremlau M, Owens CM, Perron MJ et al. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004; 427(6977):848–853.PubMedCrossRefGoogle Scholar
  11. 11.
    Hatziioannou T, Perez-Caballero D, Yang A et al. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci USA 2004; 101(29):10774–10779.PubMedCrossRefGoogle Scholar
  12. 12.
    Keckesova Z, Ylinen LM, Towers GJ. The human and African green monkey TRIM5alpha genes encode Refl and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci USA 2004; 101(29):10780–10785.PubMedCrossRefGoogle Scholar
  13. 13.
    Perron MJ, Stremlau M, Song B et al. TRIM5alphamediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc Natl Acad Sci USA 2004; 101(32): 11827–11832.PubMedCrossRefGoogle Scholar
  14. 14.
    Everett RD, Chelbi-Alix MK. PML and PML nuclear bodies: implications in antiviral defence. Biochimie 2007; 89(6–7):819–830.PubMedCrossRefGoogle Scholar
  15. 15.
    Tissot C, Mechti N. Molecular cloning of a new interferon-induced factor that represses human immunodeficiency virus type 1 long terminal repeat expression. J Biol Chem 1995;270(25):14891–14898.PubMedCrossRefGoogle Scholar
  16. 16.
    Gack MU, Shin YC, Joo CH et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007; 446(7138):916–920.PubMedCrossRefGoogle Scholar
  17. 17.
    Wolf D, Goff SP. TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 2007; 131(1):46–57.PubMedCrossRefGoogle Scholar
  18. 18.
    Fridell RA, Harding LS, Bogerd HP et al. Identification of a novel human zinc finger protein that specifically interacts with the activation domain of lentiviral Tat proteins. Virology 1995; 209(2):347–357.PubMedCrossRefGoogle Scholar
  19. 19.
    Orimo A, Tominaga N, Yoshimura K et al. Molecular cloning of ring finger protein 21 (RNF21)/ interferon-responsive finger protein (ifp1), which possesses two RING-B box-coiled coil domains in tandem. Genomics 2000; 69(1):143–149.PubMedCrossRefGoogle Scholar
  20. 20.
    Hornung V, Ellegast J, Kim S et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 2006; 314(5801):994–997.PubMedCrossRefGoogle Scholar
  21. 21.
    Pichlmair A, Schulz O, Tan CP et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 2006; 314(5801):997–1001.PubMedCrossRefGoogle Scholar
  22. 22.
    Kato H, Takeuchi O, Sato S et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441(7089):101–105.PubMedCrossRefGoogle Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. 24.
    Johnson CL, Gale M, Jr. CARD games between virus and host get a new player. Trends Immunol 2006; 27(1):1–4.PubMedCrossRefGoogle Scholar
  25. 25.
    Meylan E, Tschopp J, Karin M. Intracellular pattern recognition receptors in the host response. Nature 2006; 442(7098):39–44.PubMedCrossRefGoogle Scholar
  26. 26.
    Meylan E, Curran J, Hofmann K et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005; 437(7062):1167–1172.PubMedCrossRefGoogle Scholar
  27. 27.
    Seth RB, Sun L, Ea CK et al. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005; 122(5):669–682.PubMedCrossRefGoogle Scholar
  28. 28.
    Xu LG, Wang YY, Han KJ et al. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 2005; 19(6):727–740.PubMedCrossRefGoogle Scholar
  29. 29.
    Kawai T, Takahashi K, Sato S et al. IPS-1, an adaptor triggering RIG-I and Mda5-mediatedtype I interferon induction. Nat Immunol 2005; 6(10):981–988.PubMedCrossRefGoogle Scholar
  30. 30.
    Karpov AV. Endogenous and exogenous interferons in HIV-infection. Eur J Med Res 2001; 6(12): 507–524.PubMedGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. 32.
    Pal R, Reitz MS, Jr., Tschachler E et al. Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res Hum Retroviruses 1990; 6(6):721–730.PubMedCrossRefGoogle Scholar
  33. 33.
    Gottlinger HG, Sodroski JG, Haseltine WA. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1989; 86(15):5781–5785.PubMedCrossRefGoogle Scholar
  34. 34.
    Bryant M, Ratner L. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc Natl Acad Sci USA 1990; 87(2): 523–527.PubMedCrossRefGoogle Scholar
  35. 35.
    Bock M, Stoye JP. Endogenous retroviruses and the human germline. Curr Opin Genet Dev 2000; 10(6):651–655.PubMedCrossRefGoogle Scholar
  36. 36.
    Barklis E, Mulligan RC, Jaenisch R. Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells. Cell 1986; 47(3):391–399.PubMedCrossRefGoogle Scholar
  37. 37.
    Teich NM, Weiss RA, Martin GR et al. Virus infection of murine teratocarcinoma stem cell lines. Cell 1977; 12(4):973–982.PubMedCrossRefGoogle Scholar
  38. 38.
    Feuer G, Taketo M, Hanecak RC et al. Two blocks in Moloney murine leukemia virus expression in undifferentiated F9 embryonal carcinoma cells as determined by transient expression assays. J Virol 1989; 63(5):2317–2324.PubMedGoogle Scholar
  39. 39.
    Loh TP, Sievert LL, Scott RW. Proviral sequences that restrict retroviral expression in mouse embryonal carcinoma cells. Mol Cell Biol 1987; 7(10):3775–3784.PubMedGoogle Scholar
  40. 40.
    Urrutia R. KRAB-containing zinc-finger repressor proteins. Genome Biol 2003; 4(10):231.PubMedCrossRefGoogle Scholar
  41. 41.
    Friedman JR, Fredericks WJ, Jensen DE et al. KAP-1, a novel corepressor for the highly conserved KRAB repression domain. Genes Dev 1996; 10(16):2067–2078.PubMedCrossRefGoogle Scholar
  42. 42.
    Peng H, Begg GE, Schultz DC et al. Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol Biol 2000; 295(5): 1139–1162.PubMedCrossRefGoogle Scholar
  43. 43.
    Schultz DC, Ayyanathan K, Negorev D et al. SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 2002; 16(8):919–932.PubMedCrossRefGoogle Scholar
  44. 44.
    Sripathy SP, Stevens J, Schultz DC. The KAP1 corepressor functions to coordinate the assembly of de novo HP1-demarcated microenvironments of heterochromatin required for KRAB zinc finger protein-mediated transcriptional repression. Mol Cell Biol 2006; 26(22):8623–8638.PubMedCrossRefGoogle Scholar
  45. 45.
    Ivanov AV, Peng H, Yurchenko V et al. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 2007; 28(5):823–837.PubMedCrossRefGoogle Scholar
  46. 46.
    Ylinen LM, Keckesova Z, Wilson SJ et al. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol 2005; 79(18): 11580–11587.PubMedCrossRefGoogle Scholar
  47. 47.
    Yap MW, Lindemann D, Stanke N et al. Restriction of foamy viruses by primate Trim5alpha. J Virol 2008; 82(11):5429–5439.PubMedCrossRefGoogle Scholar
  48. 48.
    Sakuma R, Noser JA, Ohmine S et al. Rhesus monkey TRIM5alpha restricts HIV-1 production through rapid degradation of viral Gag polyproteins. Nat Med 2007; 13(5):631–635.PubMedCrossRefGoogle Scholar
  49. 49.
    Zhang F, Perez-Caballero D, Hatziioannou T et al. No effect of endogenous TRIM5alpha on HIV-1 production. Nat Med 2008; 14(3):235-236; author reply 236–238.CrossRefGoogle Scholar
  50. 50.
    Besnier C, Takeuchi Y, Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci USA 2002; 99(18):11920–11925.PubMedCrossRefGoogle Scholar
  51. 51.
    Cowan S, Hatziioannou T, Cunningham T et al. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 2002; 99(18):11914–11919.PubMedCrossRefGoogle Scholar
  52. 52.
    Hatziioannou T, Cowan S, Goff SP et al. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J 2003; 22(3):385–394.PubMedCrossRefGoogle Scholar
  53. 53.
    Hatziioannou T, Princiotta M, Piatak M, Jr. et al. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 2006; 314(5796):95.PubMedCrossRefGoogle Scholar
  54. 54.
    Nakayama EE, Miyoshi H, Nagai Y et al. 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(14):8870–8877.PubMedCrossRefGoogle Scholar
  55. 55.
    Stremlau M, Perron M, Welikala S et al. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol 2005; 79(5):3139–3145.PubMedCrossRefGoogle Scholar
  56. 56.
    Yap MW, Nisole S, Stoye JP. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 2005; 15(1):73–78.PubMedCrossRefGoogle Scholar
  57. 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 Virol 2006; 80(17):8554–8565.PubMedCrossRefGoogle Scholar
  58. 58.
    Stremlau M, Perron M, Lee M et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006; 103(14):5514–5519.PubMedCrossRefGoogle Scholar
  59. 59.
    Stoye JP, Yap MW. Chance favors a prepared genome. Proc Natl Acad Sci USA 2008; 105(9):3177–3178.PubMedCrossRefGoogle Scholar
  60. 60.
    Nisole S, Lynch C, Stoye JP et al. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc Natl Acad Sci USA 2004.Google Scholar
  61. 61.
    Sayah DM, Sokolskaja E, Berthoux L et al. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004; 430(6999):569–573.PubMedCrossRefGoogle Scholar
  62. 62.
    Liao CH, Kuang YQ, Liu HL et al. A novel fusion gene, TRIM5-Cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. Aids 2007; 21 Suppl 8:S19–26.PubMedCrossRefGoogle Scholar
  63. 63.
    Virgen CA, Kratovac Z, Bieniasz PD et al. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci USA 2008; 105(9):3563–3568.PubMedCrossRefGoogle Scholar
  64. 64.
    Wilson SJ, Webb BL, Ylinen LM et al. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc Natl Acad Sci USA 2008; 105(9):3557–3562.PubMedCrossRefGoogle Scholar
  65. 65.
    Brennan G, Kozyrev Y, Hu SL. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci USA 2008; 105(9):3569–3574.PubMedCrossRefGoogle Scholar
  66. 66.
    Newman RM, Hall L, Kirmaier A et al. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog 2008; 4(2):el000003.CrossRefGoogle Scholar
  67. 67.
    Mische CC, Javanbakht H, Song B et al. Retroviral restriction factor TRIM5alpha is a trimer. J Virol 2005; 79(22): 14446–14450.PubMedCrossRefGoogle Scholar
  68. 68.
    Javanbakht H, Diaz-Griffero F, Yuan W et al. The ability of multimerized cyclophilin A to restrict retrovirus infection. Virology 2007; 367(1): 19–29.PubMedCrossRefGoogle Scholar
  69. 69.
    Yap MW, Mortuza GB, Taylor IA et al. The design of artificial retroviral restriction factors. Virology 2007; 365(2):302–314.PubMedCrossRefGoogle Scholar
  70. 70.
    Perez-Caballero D, Hatziioannou T, Yang A et al. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol 2005; 79(14):8969–8978.PubMedCrossRefGoogle Scholar
  71. 71.
    Javanbakht H, Diaz-Griffero F, Stremlau M et al. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J Biol Chem 2005; 280(29):26933–26940.PubMedCrossRefGoogle Scholar
  72. 72.
    Diaz-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.PubMedCrossRefGoogle Scholar
  73. 73.
    Xu L, Yang L, Moitra PK et al. BTBD1 and BTBD2 colocalize to cytoplasmic bodies with the RBCC/ tripartite motif protein, TRIM5delta. Exp Cell Res 2003; 288(1):84–93.PubMedCrossRefGoogle Scholar
  74. 74.
    Diaz-Griffero F, Li X, Javanbakht H et al. Rapid turnover and polyubiquitylation of the retroviral restriction factor TRIM5. Virology 2006; 349(2):300–315.PubMedCrossRefGoogle Scholar
  75. 75.
    Yamauchi K, Wada K, Tanji K et al. Ubiquitination of E3 ubiquitin ligase TRIM5 alpha and its potential role. Febs J 2008; 275(7):1540–1555.PubMedCrossRefGoogle Scholar
  76. 76.
    Perez-Caballero D, Hatziioannou T, Zhang F et al. Restriction of human immunodeficiency virus type 1 by TRIM-CypA occurs with rapid kinetics and independently of cytoplasmic bodies, ubiquitin, and proteasome activity. J Virol 2005; 79(24):15567–15572.PubMedCrossRefGoogle Scholar
  77. 77.
    Wu X, Anderson JL, Campbell EM et al. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc Natl Acad Sci USA 2006; 103(19):7465–7470.PubMedCrossRefGoogle Scholar
  78. 78.
    Anderson JL, Campbell EM, Wu X et al. Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J Virol 2006; 80(19):9754–9760.PubMedCrossRefGoogle Scholar
  79. 79.
    Campbell EM, Perez O, Anderson JL et al. Visualization of a proteasome-independent intermediate during restriction of HIV-1 by rhesus TRIM5alpha. J Cell Biol 2008; 180(3):549–561.PubMedCrossRefGoogle Scholar
  80. 80.
    Chee AV, Lopez P, Pandolfi PP et al. Promyelocytic leukemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J Virol 2003; 77(12):7101–7105.PubMedCrossRefGoogle Scholar
  81. 81.
    Bjorndal AS, Szekely L, Elgh F. Ebola virus infection inversely correlates with the overall expression levels of promyelocytic leukaemia (PML) protein in cultured cells. BMC Microbiol 2003; 3:6.PubMedCrossRefGoogle Scholar
  82. 82.
    Borden KL, Campbelldwyer EJ, Carlile GW et al. Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J Virol 1998; 72(5):3819–3826.PubMedGoogle Scholar
  83. 83.
    Djavani M, Rodas J, Lukashevich IS et al. Role of the promyelocytic leukemia protein PML in the interferon sensitivity of lymphocytic choriomeningitis virus. J Virol 2001; 75(13):6204–6208.PubMedCrossRefGoogle Scholar
  84. 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 Virol 2004; 78(6):3162–3169.PubMedCrossRefGoogle Scholar
  85. 85.
    Bonilla WV, Pinschewer DD, Klenerman P et al. Effects of promyelocytic leukemia protein on virus-host balance. J Virol 2002; 76(8):3810–3818.PubMedCrossRefGoogle Scholar
  86. 86.
    Chelbi-Alix MK, Quignon F, Pelicano L et al. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein. J Virol 1998; 72(2):1043–1051.PubMedGoogle Scholar
  87. 87.
    Blondel D, 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.PubMedCrossRefGoogle Scholar
  88. 88.
    Chelbi-Alix MK, Vidy A, El Bougrini J et al. Rabies viral mechanisms to escape the IFN system: the viral protein P interferes with IRF-3, Stat1, and PML nuclear bodies. J Interferon Cytokine Res 2006; 26(5):271–280.PubMedCrossRefGoogle Scholar
  89. 89.
    Turelli P, Doucas V, Craig E et al. Cytoplasmic recruitment of INI1 and PML on incoming HIV preintegration complexes: interference with early steps of viral replication. Mol Cell 2001; 7(6): 1245–1254.PubMedCrossRefGoogle Scholar
  90. 90.
    Regad T, Saib A, Lallemand-Breitenbach V et al. PMLmediates the interferon-induced antiviral state against a complex retrovirus via its association with the viral transactivator. EMBO J 2001; 20(13):3495–3505.PubMedCrossRefGoogle Scholar
  91. 91.
    Everett RD, 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 ICP0. J Virol 2006; 80(16):7995–8005.PubMedCrossRefGoogle Scholar
  92. 92.
    Uchil PD, Quinlan BD, Chan WT et al. TRIM E3 ligases interfere with early and late stages of the retroviral life cycle. PLoS Pathog 2008; 4(2):el6.CrossRefGoogle Scholar
  93. 93.
    Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006; 25(3):383–392.PubMedCrossRefGoogle Scholar
  94. 94.
    Lin R, Heylbroeck C, Pitha PM et al. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol 1998; 18(5):2986–2996.PubMedGoogle Scholar
  95. 95.
    Saitoh T, Tun-Kyi A, Ryo A et al. Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat Immunol 2006; 7(6):598–605.PubMedCrossRefGoogle Scholar
  96. 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 degradation. J Immunol 2006; 177(8):5059–5067.PubMedGoogle Scholar
  97. 97.
    Higgs R, Ni Gabhann J, Ben Larbi N et al. The E3 ubiquitin ligase Ro52 negatively regulates IFN-beta production postpathogen recognition by polyubiquitin-mediated degradation of IRF3. J Immunol 2008; 181(3):1780–1786.PubMedGoogle Scholar
  98. 98.
    Shi M, Deng W, Bi E et al. TRIM30 alpha negatively regulates TLR-mediated NF-kappa B activation by targeting TAB2 and TAB3 for degradation. Nat Immunol 2008; 9(4):369–377.PubMedCrossRefGoogle Scholar
  99. 99.
    Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003; 21:335–376.PubMedCrossRefGoogle Scholar
  100. 100.
    Kishida S, Sanjo H, Akira S et al. TAK1-binding protein 2 facilitates ubiquitination of TRAF 6 and assembly of TRAF6 with IKK in the IL-1 signaling pathway. Genes Cells 2005; 10(5):447–454.PubMedCrossRefGoogle Scholar
  101. 101.
    Asaoka K, Ikeda K, Hishinuma T et al. A retrovirus restriction factor TRIM5alpha is transcriptionally regulated by interferons. Biochem Biophys Res Commun 2005; 338(4):1950–1956.PubMedCrossRefGoogle Scholar
  102. 102.
    Carthagena L, Parise MC, Ringeard M et al. Implication of TRIM alpha and TRIMCyp in interferon-induced anti-retroviral restriction activities. Retrovirology 2008; 5:59.PubMedCrossRefGoogle Scholar
  103. 103.
    Rold CJ, Aiken C. Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog 2008;4(5):el000074.CrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Melvyn W. Yap
    • 1
  • Jonathan P. Stoye
    • 1
  1. 1.Division of VirologyNational Institute for Medical ResearchLondonUK

Personalised recommendations