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Induction and Evasion of the Type I Interferon Response by Cytomegaloviruses

  • Victor R. DeFilippis
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 598)

Abstract

Cytomegaloviruses represent supreme pathogens in that they are capable of occupying healthy mammalian hosts for life in the face of constant antiviral immune reactions. The inability of the host to eliminate the virus likely results from numerous counteractive strategies employed to disrupt the immune response. The role of type I interferon in the antiviral response has been well documented although only recently have the pathways of induction of this powerful cytokine been described. Cytomegaloviruses have been shown to both induce and be sensitive to the effects of type I interferon. Yet these viruses also possess numerous and varied phenotypes capable of inhibiting not only interferon induction but also interferon signaling and interferon-induced antiviral processes. The balance between induction and evasion of type I interferon responses by cytomegaloviruses is discussed in this review.

Keywords

Interferon Regulatory Factor Human Cytomegalovirus Antiviral Response HCMV Infection Interferon Response 
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.

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References

  1. Abate D.A., Watanabe S. and Mocarski E.S. (2004) Major human cytomegalovirus structural protein pp65 (ppUL83) prevents interferon response factor 3 activation in the interferon response. J Virol, 78, 10995-11006.PubMedGoogle Scholar
  2. Abenes G., Lee M., Haghjoo E., Tong T., Zhan X. and Liu F. (2001) Murine cytomegalovirus open reading frame M27 plays an important role in growth and virulence in mice. J Virol, 75, 1697-1707.PubMedGoogle Scholar
  3. Ahmad-Nejad P., Hacker H., Rutz M., Bauer S., Vabulas R.M. and Wagner H. (2002) Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur J Immunol, 32, 1958-1968.PubMedGoogle Scholar
  4. Alford C.A., Stagno S., Pass R.F. and Britt W.j. (1990) Congenital and perinatal cutomegalovirus infection. Rev Infect Dis, 12, 745-753.Google Scholar
  5. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S. and Randall R.E. (2004) The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A, 101, 17264-17269.PubMedGoogle Scholar
  6. Arnon T.I., Achdout H., Levi O., Markel G., Saleh N., Katz G., Gazit R., Gonen-Gross T., Hanna J., Nahari E., Porgador A., Honigman A., Plachter B., Mevorach D., Wolf D.G. and Mandelboim O. (2005) Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat Immunol, 6, 515-523.PubMedGoogle Scholar
  7. Benedict C.A., Angulo A., Patterson G., Ha S., Huang H., Messerle M., Ware C.F. and Ghazal P. (2004) Neutrality of the canonical NF-kappaB-dependent pathway for human and murine cytomegalovirus transcription and replication in vitro. J Virol, 78, 741-750.PubMedGoogle Scholar
  8. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P. and Salazar-Mather T.P. (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol, 17, 189-220.PubMedGoogle Scholar
  9. Biron C.A. and Sen G.C. (2001) Interferon and other cytokines. In: Fields Virology (ed B.N. Fields), pp. 321-351. Lippincott-Raven, Philadelphia.Google Scholar
  10. Boehme K.W. and Compton T. (2006) Virus entry and activation of innate immunity. In: Cytomegaloviruses: Molecular Biology and Immunology (ed M.J. Reddehase), pp. 111-130. Caister Academic Press, Norfolk, UK.Google Scholar
  11. Boehme K.W., Singh J., Perry S.T. and Compton T. (2004) Human cytomegalovirus elicits a coordinated cellular antiviral response via envelope glycoprotein B. J Virol, 78, 1202-1211.PubMedGoogle Scholar
  12. Boyle K.A., Pietropaolo R.L. and Compton T. (1999) Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol Cell Biol, 19, 3607-3613.PubMedGoogle Scholar
  13. Bresnahan W.A. and Shenk T. (2000a) A subset of viral transcripts packaged within human cytomegalovirus particles. Science, 288, 2373-2376.Google Scholar
  14. Bresnahan W.A. and Shenk T.E. (2000b) UL82 virion protein activates expression of immediate early viral genes in human cytomegalovirus-infected cells. Proc Natl Acad Sci U S A, 97, 14506-14511.Google Scholar
  15. Browne E.P. and Shenk T. (2003) Human cytomegalovirus UL83-coded pp65 virion protein inhibits antiviral gene expression in infected cells. Proc Natl Acad Sci U S A, 100, 11439-11444.PubMedGoogle Scholar
  16. Browne E.P., Wing B., Coleman D. and Shenk T. (2001) Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J Virol, 75, 12319-12330.PubMedGoogle Scholar
  17. Cantrell S.R. and Bresnahan W.A. (2005) Interaction between the human cytomegalovirus UL82 gene product (pp71) and hDaxx regulates immediate-early gene expression and viral replication. J Virol, 79, 7792-7802.PubMedGoogle Scholar
  18. Child S.J., Hakki M., De Niro K.L. and Geballe A.P. (2004) Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J Virol, 78, 197-205.PubMedGoogle Scholar
  19. Child S.J., Jarrahian S., Harper V.M. and Geballe A.P. (2002) Complementation of vaccinia virus lacking the double-stranded RNA-binding protein gene E3L by human cytomegalovirus. J Virol, 76, 4912-4918.PubMedGoogle Scholar
  20. Chin K.C. and Cresswell P. (2001) Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci U S A, 98, 15125-15130.PubMedGoogle Scholar
  21. Collins S.E., Noyce R.S. and Mossman K.L. (2004) Innate cellular response to virus particle entry requires IRF3 but not virus replication. J Virol, 78, 1706-1717.PubMedGoogle Scholar
  22. Colonna M., Krug A. and Cella M. (2002) Interferon-producing cells: on the front line in immune responses against pathogens. Curr Opin Immunol, 14, 373-379.PubMedGoogle Scholar
  23. Compton T., Kurt-Jones E.A., Boehme K.W., Belko J., Latz E., Golenbock D.T. and Finberg R.W. (2003) Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J Virol, 77, 4588-4596.PubMedGoogle Scholar
  24. Cull V.S., Bartlett E.J. and James C.M. (2002) Type I interferon gene therapy protects against cytomegalovirus-induced myocarditis. Immunology, 106, 428-437.PubMedGoogle Scholar
  25. DeFilippis V.R. and Früh K.J. (2005) Rhesus cytomegalovirus particles prevent activation of interferon regulatory factor 3. J Virol, 79, 6419-6431.PubMedGoogle Scholar
  26. DeFilippis V.R., Robinson B., Keck T.M., Hansen S.G., Nelson J.A. and Früh K. (2006) Interferon regulatory factor 3 is necessary for induction of antiviral genes during human cytomegalovirus infection. J Virol, 80, 1032-1037.PubMedGoogle Scholar
  27. Diebold S.S., Kaisho T., Hemmi H., Akira S. and Reis e Sousa C. (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science, 303, 1529-1531.PubMedGoogle Scholar
  28. Diebold S.S., Montoya M., Unger H., Alexopoulou L., Roy P., Haswell L.E., Al-Shamkhani A., Flavell R., Borrow P. and Reis e Sousa C. (2003) Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature, 424, 324-328.PubMedGoogle Scholar
  29. Eickhoff J.E. and Cotten M. (2005) NF-kappaB activation can mediate inhibition of human cytomegalovirus replication. J Gen Virol, 86, 285-295.PubMedGoogle Scholar
  30. Erlandsson L., Blumenthal R., Eloranta M.L., Engel H., Alm G., Weiss S. and Leanderson T. (1998) Interferon-beta is required for interferon-alpha production in mouse fibroblasts. Curr Biol, 8, 223-226.PubMedGoogle Scholar
  31. Fitzgerald K.A., McWhirter S.M., Faia K.L., Rowe D.C., Latz E., Golenbock D.T., Coyle A.J., Liao S.M. and Maniatis T. (2003) IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol, 4, 491-496.PubMedGoogle Scholar
  32. Gitlin L., Barchet W., Gilfillan S., Cella M., Beutler B., Flavell R.A., Diamond M.S. and Colonna M. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A, 103, 8459-8464.PubMedGoogle Scholar
  33. Gravel S.P. and Servant M.J. (2005) Roles of an IkappaB kinase-related pathway in human cytomegalovirus-infected vascular smooth muscle cells: a molecular link in pathogen-induced proatherosclerotic conditions. J Biol Chem, 280, 7477-7486.PubMedGoogle Scholar
  34. Greijer A.E., Dekkers C.A. and Middeldorp J.M. (2000) Human cytomegalovirus virions differentially incorporate viral and host cell RNA during the assembly process. J Virol, 74, 9078-9082.PubMedGoogle Scholar
  35. Gribaudo G., Ravaglia S., Caliendo A., Cavallo R., Gariglio M., Martinotti M.G. and Landolfo S. (1993) Interferons inhibit onset of murine cytomegalovirus immediate-early gene transcription. Virology, 197, 303-311.PubMedGoogle Scholar
  36. Hansen S.G., Strelow L.I., Franchi D.C., Anders D.G. and Wong S.W. (2003) Complete sequence and genomic analysis of rhesus cytomegalovirus. J Virol, 77, 6620-6636.PubMedGoogle Scholar
  37. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., Lipford G., Wagner H. and Bauer S. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science, 303, 1526-1529.PubMedGoogle Scholar
  38. Hiscott J., Grandvaux N., Sharma S., Tenoever B.R., Servant M.J. and Lin R. (2003) Convergence of the NF-kappaB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann N Y Acad Sci, 1010, 237-248.PubMedGoogle Scholar
  39. Huff J.L., Eberle R., Capitanio J., Zhou S.S. and Barry P.A. (2003) Differential detection of B virus and rhesus cytomegalovirus in rhesus macaques. J Gen Virol, 84, 83-92.PubMedGoogle Scholar
  40. Ishii K.J., Coban C., Kato H., Takahashi K., Torii Y., Takeshita F., Ludwig H., Sutter G., Suzuki K., Hemmi H., Sato S., Yamamoto M., Uematsu S., Kawai T., Takeuchi O. and Akira S. (2006) A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol, 7, 40-48.PubMedGoogle Scholar
  41. Kato H., Sato S., Yoneyama M., Yamamoto M., Uematsu S., Matsui K., Tsujimura T., Takeda K., Fujita T., Takeuchi O. and Akira S. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity, 23, 19-28.PubMedGoogle Scholar
  42. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.S., Reis e Sousa C., Matsuura Y., Fujita T. and Akira S. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature, 441, 101-105.PubMedGoogle Scholar
  43. Kawai T. and Akira S. (2006) TLR signaling. Cell Death Differ, 13, 816-825.PubMedGoogle Scholar
  44. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O. and Akira S. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol.Google Scholar
  45. Krug A., French A.R., Barchet W., Fischer J.A., Dzionek A., Pingel J.T., Orihuela M.M., Akira S., Yokoyama W.M. and Colonna M. (2004) TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity, 21, 107-119.PubMedGoogle Scholar
  46. Kumar K.P., McBride K.M., Weaver B.K., Dingwall C. and Reich N.C. (2000) Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol Cell Biol, 20, 4159-4168.PubMedGoogle Scholar
  47. Levy D.E., Marie I., Smith E. and Prakash A. (2002) Enhancement and diversification of IFN induction by IRF-7-mediated positive feedback. J Interferon Cytokine Res, 22, 87-93.PubMedGoogle Scholar
  48. Lin R., Heylbroeck C., Pitha P.M. and Hiscott J. (1998) Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol Cell Biol, 18, 2986-2996.PubMedGoogle Scholar
  49. Lin R., Lacoste J., Nakhaei P., Sun Q., Yang L., Paz S., Wilkinson P., Julkunen I., Vitour D., Meurs E. and Hiscott J. (2006) Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol, 80, 6072-6083.PubMedGoogle Scholar
  50. Loenen W.A., Bruggeman C.A. and Wiertz E.J. (2001) Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin Immunol, 13, 41-49.PubMedGoogle Scholar
  51. Marie I., Durbin J.E. and Levy D.E. (1998) Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. Embo J, 17, 6660-6669.PubMedGoogle Scholar
  52. Martin M.U. and Wesche H. (2002) Summary and comparison of the signaling mechanisms of the Toll/interleukin-1 receptor family. Biochim Biophys Acta, 1592, 265-280.PubMedGoogle Scholar
  53. McGeoch D.J., Cook S., Dolan A., Jamieson F.E. and Telford E.A. (1995) Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J Mol Biol, 247, 443-458.PubMedGoogle Scholar
  54. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R. and Tschopp J. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature.Google Scholar
  55. Miller D.M., Rahill B.M., Boss J.M., Lairmore M.D., Durbin J.E., Waldman J.W. and Sedmak D.D. (1998) Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J Exp Med, 187, 675-683.PubMedGoogle Scholar
  56. Miller D.M., Zhang Y., Rahill B.M., Waldman W.J. and Sedmak D.D. (1999) Human cytomegalovirus inhibits IFN-alpha-stimulated antiviral and immunoregulatory responses by blocking multiple levels of IFN-alpha signal transduction. Journal of Immunology, 162, 6107-6113.Google Scholar
  57. Mocarski E.S. (2001) Cytomegaloviruses and their replication. In: Virology (ed B.N. Fields), pp. 2629-2673. Lippincott-Raven, Philadelphia.Google Scholar
  58. Mocarski E.S., Jr. (2002) Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion. Trends Microbiol, 10, 332-339.PubMedGoogle Scholar
  59. Navarro L., Mowen K., Rodems S., Weaver B., Reich N., Spector D. and David M. (1998) Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon- stimulated response element-binding complex. Mol Cell Biol, 18, 3796-3802.PubMedGoogle Scholar
  60. Netterwald J.R., Jones T.R., Britt W.J., Yang S.J., McCrone I.P. and Zhu H. (2004) Postattachment events associated with viral entry are necessary for induction of interferon-stimulated genes by human cytomegalovirus. J Virol, 78, 6688-6691.PubMedGoogle Scholar
  61. Nichols W.G. and Boeckh M. (2000) Recent advances in the therapy and prevention of CMV infections. J Clin Virol, 16, 25-40.PubMedGoogle Scholar
  62. Noyce R.S., Collins S.E. and Mossman K.L. (2006) Identification of a novel pathway essential for the immediate-early, interferon-independent antiviral response to enveloped virions. J Virol, 80, 226-235.PubMedGoogle Scholar
  63. Odeberg J., Plachter B., Branden L. and Soderberg-Naucler C. (2003) Human cytomegalovirus protein pp65 mediates accumulation of HLA-DR in lysosomes and destruction of the HLA-DR alpha-chain. Blood, 101, 4870-4877.PubMedGoogle Scholar
  64. Okabe Y., Kawane K., Akira S., Taniguchi T. and Nagata S. (2005) Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med, 202, 1333-1339.PubMedGoogle Scholar
  65. Pass R.F. (2001) Cytomegalovirus. In: Fields Virology (ed P.M.H. David M. Knipe, Diane E. Griffin, Robert A. Lamb Malcolm A. Martin, Bernard Roizman and Stephen E. Straus), pp. 2675-2705. Lippincott Williams and Wilkins, Philadelphia.Google Scholar
  66. Paulus C., Krauss S. and Nevels M. (2006) A human cytomegalovirus antagonist of type I IFN-dependent signal transducer and activator of transcription signaling. Proc Natl Acad Sci U S A, 103, 3840-3845.PubMedGoogle Scholar
  67. Pestka S., Langer J.A., Zoon K.C. and Samuel C.E. (1987) Interferons and their actions. Annu Rev Biochem, 56, 727-777.PubMedGoogle Scholar
  68. Pinto A.K. and Hill A.B. (2005) Viral interference with antigen presentation to CD8+ T cells: lessons from cytomegalovirus. Viral Immunol, 18, 434-444.PubMedGoogle Scholar
  69. Preston C.M., Harman A.N. and Nicholl M.J. (2001) Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus. J Virol, 75, 8909-8916.PubMedGoogle Scholar
  70. Rajagopalan S. and Long E.O. (2005) Viral evasion of NK-cell activation. Trends Immunol, 26, 403-405.PubMedGoogle Scholar
  71. Reinke P., Prosch S., Kern F. and Volk H.D. (1999) Mechanisms of human cytomegalovirus (HCMV) (re)activation and its impact on organ transplant patients. Transpl Infect Dis, 1, 157-164.PubMedGoogle Scholar
  72. Ruger B., Klages S., Walla B., Albrecht J., Fleckenstein B., Tomlinson P. and Barrell B. (1987) Primary structure and transcription of the genes coding for the two virion phosphoproteins pp65 and pp71 of human cytomegalovirus. J Virol, 61, 446-453.PubMedGoogle Scholar
  73. Sainz B., Jr., LaMarca H.L., Garry R.F. and Morris C.A. (2005) Synergistic inhibition of human cytomegalovirus replication by interferon-alpha/beta and interferon-gamma. Virol J, 2, 14.PubMedGoogle Scholar
  74. Salazar-Mather T.P., Lewis C.A. and Biron C.A. (2002) Type I interferons regulate inflammatory cell trafficking and macrophage inflammatory protein 1 alpha delivery to the liver. J Clin Invest, 110, 321-330.PubMedGoogle Scholar
  75. Sambucetti L.C., Cherrington J.M., Wilkinson G.W. and Mocarski E.S. (1989) NF-kappa B activation of the cytomegalovirus enhancer is mediated by a viral transactivator and by T cell stimulation. Embo J, 8, 4251-4258.PubMedGoogle Scholar
  76. Samuel C.E. (2001) Antiviral actions of interferons. Clin Microbiol Rev, 14, 778-809, table of contents.PubMedGoogle Scholar
  77. Schneider R.J. and Mohr I. (2003) Translation initiation and viral tricks. Trends Biochem Sci, 28, 130-136.Google Scholar
  78. Seth R.B., Sun L., Ea C.K. and Chen Z.J. (2005) Identification and Characterization of MAVS, a Mitochondrial Antiviral Signaling Protein that Activates NF-kappaB and IRF3. Cell, 122, 669-682.PubMedGoogle Scholar
  79. Sharma S., tenOever B.R., Grandvaux N., Zhou G.P., Lin R. and Hiscott J. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science, 300, 1148-1151.PubMedGoogle Scholar
  80. Shuai K. and Liu B. (2003) Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol, 3, 900-911.PubMedGoogle Scholar
  81. Simmen K.A., Singh J., Luukkonen B.G., Lopper M., Bittner A., Miller N.E., Jackson M.R., Compton T. and Fruh K. (2001) Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc Natl Acad Sci U S A, 98, 7140-7145.PubMedGoogle Scholar
  82. Söderberg-Naucler C. and Nelson J.Y. (1999) Human cytomegalovirus latency and reactivation - a delicate balance between the virus and its host’s immune system. Intervirology, 42, 314-321.PubMedGoogle Scholar
  83. Stein J., Volk H.D., Liebenthal C., Kruger D.H. and Prosch S. (1993) Tumour necrosis factor alpha stimulates the activity of the human cytomegalovirus major immediate early enhancer/promoter in immature monocytic cells. J Gen Virol, 74 ( Pt 11), 2333-2338.PubMedGoogle Scholar
  84. Stetson D.B. and Medzhitov R. (2006) Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity, 24, 93-103.PubMedGoogle Scholar
  85. Streblow D.N., Orloff S.L. and Nelson J.A. (2001) Do pathogens accelerate atherosclerosis? J Nutr, 131, 2798S-2804S.PubMedGoogle Scholar
  86. Suhara W., Yoneyama M., Kitabayashi I. and Fujita T. (2002) Direct involvement of CREB-binding protein/p300 in sequence-specific DNA binding of virus-activated interferon regulatory factor-3 holocomplex. J Biol Chem, 277, 22304-22313.PubMedGoogle Scholar
  87. Sylwester A.W., Mitchell B.L., Edgar J.B., Taormina C., Pelte C., Ruchti F., Sleath P.R., Grabstein K.H., Hosken N.A., Kern F., Nelson J.A. and Picker L.J. (2005) Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med, 202, 673-685.PubMedGoogle Scholar
  88. Szomolanyi-Tsuda E., Liang X., Welsh R.M., Kurt-Jones E.A. and Finberg R.W. (2006) Role for TLR2 in NK cell-mediated control of murine cytomegalovirus in vivo. J Virol, 80, 4286-4291.PubMedGoogle Scholar
  89. Tabeta K., Georgel P., Janssen E., Du X., Hoebe K., Crozat K., Mudd S., Shamel L., Sovath S., Goode J., Alexopoulou L., Flavell R.A. and Beutler B. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A, 101, 3516-3521.PubMedGoogle Scholar
  90. Takeuchi O. and Akira S. (2001) Toll-like receptors; their physiological role and signal transduction system. Int Immunopharmacol, 1, 625-635.PubMedGoogle Scholar
  91. Taylor R.T. and Bresnahan W.A. (2005) Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J Virol, 79, 3873-3877.PubMedGoogle Scholar
  92. Taylor R.T. and Bresnahan W.A. (2006) Human cytomegalovirus immediate-early 2 protein IE86 blocks virus-induced chemokine expression. J Virol, 80, 920-928.PubMedGoogle Scholar
  93. Torigoe S., Campbell D.E., Torigoe F., Michelson S. and Starr S.E. (1993) Cytofluorographic analysis of effects of interferons on expression of human cytomegalovirus proteins. J Virol Methods, 45, 219-228.PubMedGoogle Scholar
  94. Varnum S.M., Streblow D.N., Monroe M.E., Smith P., Auberry K.J., Pasa-Tolic L., Wang D., Camp D.G., 2nd, Rodland K., Wiley S., Britt W., Shenk T., Smith R.D. and Nelson J.A. (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol, 78, 10960-10966.PubMedGoogle Scholar
  95. Vogel P., Weigler B.J., Kerr H., Hendrickx A.G. and Barry P.A. (1994) Seroepidemiologic studies of cytomegalovirus infection in a breeding population of rhesus macaques. Lab Anim Sci, 44, 25-30.PubMedGoogle Scholar
  96. Wathelet M.G., Lin C.H., Parekh B.S., Ronco L.V., Howley P.M. and Maniatis T. (1998) Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol Cell, 1, 507-518.PubMedGoogle Scholar
  97. Weaver B.K., Kumar K.P. and Reich N.C. (1998) Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol Cell Biol, 18, 1359-1368.PubMedGoogle Scholar
  98. Weber F., Kochs G. and Haller O. (2004) Inverse interference: how viruses fight the interferon system. Viral Immunol, 17, 498-515.PubMedGoogle Scholar
  99. Werts C., Girardin S.E. and Philpott D.J. (2006) TIR, CARD and PYRIN: three domains for an antimicrobial triad. Cell Death Differ, 13, 798-815.PubMedGoogle Scholar
  100. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z. and Shu H.B. (2005) VISA Is an Adapter Protein Required for Virus-Triggered IFN-beta Signaling. Mol Cell, 19, 727-740.PubMedGoogle Scholar
  101. Yeow W.S., Lawson C.M. and Beilharz M.W. (1998) Antiviral activities of individual murine IFN-alpha subtypes in vivo: intramuscular injection of IFN expression constructs reduces cytomegalovirus replication. J Immunol, 160, 2932-2939.PubMedGoogle Scholar
  102. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S. and Fujita T. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol, 5, 730-737.PubMedGoogle Scholar
  103. Yoneyama M., Suhara W., Fukuhara Y., Fukuda M., Nishida E. and Fujita T. (1998) Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. Embo J, 17, 1087-1095.PubMedGoogle Scholar
  104. Yurochko A.D. and Huang E.S. (1999) Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression. J Immunol, 162, 4806-4816.PubMedGoogle Scholar
  105. Yurochko A.D., Hwang E.S., Rasmussen L., Keay S., Pereira L. and Huang E.S. (1997a) The human cytomegalovirus UL55 (gB) and UL75 (gH) glycoprotein ligands initiate the rapid activation of Sp1 and NF-kappaB during infection. J Virol, 71, 5051-5059.Google Scholar
  106. Yurochko A.D., Kowalik T.F., Huong S.M. and Huang E.S. (1995) Human cytomegalovirus upregulates NF-kappa B activity by transactivating the NF-kappa B p105/p50 and p65 promoters. J Virol, 69, 5391-5400.PubMedGoogle Scholar
  107. Yurochko A.D., Mayo M.W., Poma E.E., Baldwin A.S., Jr. and Huang E.S. (1997b) Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-kappaB promoters. J Virol, 71, 4638-4648.Google Scholar
  108. Zhu H., Cong J.P., Mamtora G., Gingeras T. and Shenk T. (1998) Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc Natl Acad Sci U S A, 95, 14470-14475.PubMedGoogle Scholar
  109. Zhu H., Cong J.P. and Shenk T. (1997) Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc Natl Acad Sci U S A, 94, 13985-13990.PubMedGoogle Scholar
  110. Zhu H., Cong J.P., Yu D., Bresnahan W.A. and Shenk T.E. (2002) Inhibition of cyclooxygenase 2 blocks human cytomegalovirus replication. Proc Natl Acad Sci U S A, 99, 3932-3937.PubMedGoogle Scholar
  111. Zimmermann A., Trilling M., Wagner M., Wilborn M., Bubic I., Jonjic S., Koszinowski U. and Hengel H. (2005) A cytomegaloviral protein reveals a dual role for STAT2 in IFN-{gamma} signaling and antiviral responses. J Exp Med, 201, 1543-1553.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Victor R. DeFilippis
    • 1
  1. 1.Vaccine and Gene Therapy InstituteOregon Health and Science University

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