The interferon-α/β system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors

The efficient induction of interferons alpha and beta (IFN-alpha/beta) in virus-infected cells is central to the antiviral response of a host and is regulated mainly at the level of gene transcription. Once produced, IFN-alpha/beta transmit signals to the cell interior via a specific receptor complex to induce an antiviral response. Recently, the auto-amplification mechanism of the IFN-alpha/beta system that follows viral infection has been identified. This mechanism is mediated by transcription factors of the IFN regulatory factor family and, in fact, may have evolved to render the system more robust in antiviral responses.

[1]  R. Zinkernagel,et al.  Neutralizing antiviral B cell responses. , 1997, Annual review of immunology.

[2]  T. Taniguchi,et al.  Gene induction pathways mediated by distinct IRFs during viral infection. , 2001, Biochemical and biophysical research communications.

[3]  T. Taniguchi,et al.  Distinct and Essential Roles of Transcription Factors IRF-3 and IRF-7 in Response to Viruses for IFN-α/β Gene Induction , 2000 .

[4]  T. Taniguchi,et al.  IRF family of transcription factors as regulators of host defense. , 2001, Annual review of immunology.

[5]  M Kitagawa,et al.  Anti-oncogenic and oncogenic potentials of interferon regulatory factors-1 and -2 , 1993, Science.

[6]  D. Levy,et al.  Targeted Disruption of the Mouse Stat1 Gene Results in Compromised Innate Immunity to Viral Disease , 1996, Cell.

[7]  Claude Desplan,et al.  Identification of a Stat Gene That Functions in Drosophila Development , 1996, Cell.

[8]  J. Sprent,et al.  T Cell Stimulation In Vivo by Lipopolysaccharide (LPS) , 1997, The Journal of experimental medicine.

[9]  G. Stark,et al.  How cells respond to interferons. , 1998, Annual review of biochemistry.

[10]  T. Maniatis,et al.  Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements , 1993, Cell.

[11]  E. Nishida,et al.  Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF‐3 and CBP/p300 , 1998, The EMBO journal.

[12]  P. Moore,et al.  Regulation of Type I Interferon Gene Expression by Interferon Regulatory Factor-3* , 1998, The Journal of Biological Chemistry.

[13]  C. Biron,et al.  Natural killer cells in antiviral defense: function and regulation by innate cytokines. , 1999, Annual review of immunology.

[14]  T. Taniguchi,et al.  Constitutive IFN-a/ Signal for Efficient IFN-a/ Gene Induction by Virus , 2001 .

[15]  T. Taniguchi,et al.  Regulation of IFN‐α/β genes: evidence for a dual function of the transcription factor complex ISGF3 in the production and action of IFN‐α/β , 1996, Genes to cells : devoted to molecular & cellular mechanisms.

[16]  H. Kirchner,et al.  Local interferon induction by bacterial lipopolysaccharide in mice after pretreatment with Corynebacterium parvum. , 1986, Journal of interferon research.

[17]  J. Hiscott,et al.  The growing family of interferon regulatory factors. , 1997, Cytokine & growth factor reviews.

[18]  H. Ploegh,et al.  Viral subversion of the immune system. , 2000, Annual review of immunology.

[19]  T. Mak,et al.  Involvement of the IRF-1 transcription factor in antiviral responses to interferons. , 1994, Science.

[20]  T. Taniguchi,et al.  Essential and non‐redundant roles of p48 (ISGF3γ) and IRF‐1 in both type I and type II interferon responses, as revealed by gene targeting studies , 1996, Genes to cells : devoted to molecular & cellular mechanisms.

[21]  T. Maniatis,et al.  Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. , 1998, Molecular cell.

[22]  K C Zoon,et al.  Interferons and their actions. , 1987, Annual review of biochemistry.

[23]  J. Darnell,et al.  Purification and cloning of interferon-stimulated gene factor 2 (ISGF2): ISGF2 (IRF-1) can bind to the promoters of both beta interferon- and interferon-stimulated genes but is not a primary transcriptional activator of either , 1990, Molecular and cellular biology.

[24]  F. Belardelli.  Role of interferons and other cytokines in the regulation of the immune response , 1995, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[25]  T. Taniguchi,et al.  Positive feedback regulation of type I IFN genes by the IFN‐inducible transcription factor IRF‐7 , 1998, FEBS letters.

[26]  N. Hageman,et al.  Regulation of the Promoter Activity of Interferon Regulatory Factor-7 Gene , 2000, The Journal of Biological Chemistry.

[27]  M. Yoneyama,et al.  Induction of IRF‐3/‐7 kinase and NF‐κB in response to double‐stranded RNA and virus infection: common and unique pathways , 2001, Genes to cells : devoted to molecular & cellular mechanisms.

[28]  T. Leanderson,et al.  Interferon-β is required for interferon-α production in mouse fibroblasts , 1998, Current Biology.

[29]  T. Taniguchi,et al.  Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. , 1994, Science.

[30]  C. Bogdan.  The function of type I interferons in antimicrobial immunity. , 2000, Current opinion in immunology.

[31]  J. Hiscott,et al.  Virus-Dependent Phosphorylation of the IRF-3 Transcription Factor Regulates Nuclear Translocation, Transactivation Potential, and Proteasome-Mediated Degradation , 1998, Molecular and Cellular Biology.

[32]  Stefania Gallucci,et al.  Natural adjuvants: Endogenous activators of dendritic cells , 1999, Nature Medicine.

[33]  J. Darnell,et al.  Interferon-induced transcription of a gene encoding a 15-kDa protein depends on an upstream enhancer element. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[34]  B. Tombal,et al.  Characterization of the Interferon Regulatory Factor-7 and Its Potential Role in the Transcription Activation of Interferon A Genes* , 1998, The Journal of Biological Chemistry.

[35]  T. Mak,et al.  Requirement for the Transcription Factor LSIRF/IRF4 for Mature B and T Lymphocyte Function , 1997, Science.

[36]  L Cohen,et al.  Synergism between distinct enhanson domains in viral induction of the human beta interferon gene , 1990, Molecular and cellular biology.

[37]  D. Levy,et al.  ISGF3γ p48, a specificity switch for interferon activated transcription factors , 1996 .

[38]  T. Taniguchi,et al.  Recognition DNA sequences of interferon regulatory factor 1 (IRF-1) and IRF-2, regulators of cell growth and the interferon system , 1993, Molecular and cellular biology.

[39]  J. Waring,et al.  Immunodeficiency and Chronic Myelogenous Leukemia-like Syndrome in Mice with a Targeted Mutation of the ICSBP Gene , 1996, Cell.

[40]  D. Levy,et al.  Differential viral induction of distinct interferon‐α genes by positive feedback through interferon regulatory factor‐7 , 1998, The EMBO journal.

[41]  F. Belardelli,et al.  Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. , 2001, Immunity.

[42]  A. Haas,et al.  Immunoregulatory properties of ISG15, an interferon-induced cytokine. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Mann,et al.  SH2 Signaling in a Lower Eukaryote: A STAT Protein That Regulates Stalk Cell Differentiation in Dictyostelium , 1997, Cell.

[44]  S. Navarro,et al.  Transcriptional repression of type I IFN genes. , 1998, Biochimie.

[45]  V. Bocci.  The physiological interferon response. , 1985, Immunology today.

[46]  T. Taniguchi,et al.  Cellular commitment to oncogene-induced transformation or apoptosis is dependent on the transcription factor IRF-1 , 1994, Cell.

[47]  T. Taniguchi,et al.  Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development , 1993, Cell.

[48]  T. Taniguchi,et al.  Involvement of the IRF family transcription factor IRF‐3 in virus‐induced activation of the IFN‐β gene , 1998, FEBS letters.

[49]  T. Taniguchi,et al.  Cross talk between interferon-gamma and -alpha/beta signaling components in caveolar membrane domains. , 2000, Science.

[50]  M. Brunda,et al.  Interferons and Other Cytokines , 1997 .

[51]  N. Perrimon,et al.  Stripe-specific regulation of pair-rule genes by hopscotch, a putative Jak family tyrosine kinase in Drosophila. , 1994, Genes & development.

[52]  T. Taniguchi,et al.  Type I interferons are essential mediators of apoptotic death in virally infected cells , 1998, Genes to cells : devoted to molecular & cellular mechanisms.

[53]  N. Reich,et al.  Interferon Regulatory Factor 3 and CREB-Binding Protein/p300 Are Subunits of Double-Stranded RNA-Activated Transcription Factor DRAF1 , 1998, Molecular and Cellular Biology.

[54]  N. Raj,et al.  Upstream regulatory elements of murine alpha 4-interferon gene confer inducibility and cell type-restricted expression. , 1989, The Journal of biological chemistry.

[55]  N. Reich,et al.  Characterization of Specific DNA-binding Factors Activated by Double-stranded RNA as Positive Regulators of Interferon α/β-stimulated Genes (*) , 1995, The Journal of Biological Chemistry.

[56]  E. Demaeyer,et al.  Interferons and other regulatory cytokines , 1988 .

[57]  S. Goodbourn,et al.  Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. , 2000, The Journal of general virology.

[58]  C. Weissmann,et al.  The interferon genes. , 1986, Progress in nucleic acid research and molecular biology.

[59]  I. Kerr,et al.  Jaks and Stats in signaling by the cytokine receptor superfamily. , 1995, Trends in genetics : TIG.

[60]  Tae Hoon Kim,et al.  PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. , 1999, Genes & development.

[61]  T. Taniguchi,et al.  A weak signal for strong responses: interferon-alpha/beta revisited , 2001, Nature Reviews Molecular Cell Biology.

[62]  Tom Maniatis,et al.  Transcriptional activation: A complex puzzle with few easy pieces , 1994, Cell.

[63]  I. Gresser.  Biologic effects of interferons. , 1990, The Journal of investigative dermatology.

[64]  T. Taniguchi,et al.  Cross talk of the interferon‐α/β signalling complex with gp130 for effective interleukin‐6 signalling , 2001 .

[65]  H. Kwon,et al.  Interferon regulatory factors: the next generation. , 1999, Gene.

[66]  C. Biron.  Interferons α and β as Immune Regulators—A New Look , 2001 .

[67]  T. Maniatis,et al.  Two different virus‐inducible elements are required for human beta‐interferon gene regulation. , 1989, The EMBO journal.

[68]  Antonio Alcami,et al.  Viral mechanisms of immune evasion , 2000, Immunology Today.

[69]  J. Ryals,et al.  A 46-nucleotide promoter segment from an IFN-α gene renders an unrelated promoter inducible by virus , 1985, Cell.

[70]  T. Taniguchi,et al.  Cooperation of the tumour suppressors IRF-1 and p53 in response to DNA damage , 1996, Nature.

[71]  Takashi Miyata,et al.  Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes , 1989, Cell.

[72]  W. Leonard,et al.  Jaks and STATs: biological implications. , 1998, Annual review of immunology.

[73]  L. Wahl,et al.  BCG-induced enhancement of endotoxin sensitivity in C3H/HeJ mice. II. T cell modulation of macrophage sensitivity to LPS in vitro. , 1982, Immunobiology.

[74]  J. Darnell,et al.  Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. , 1994, Science.

[75]  F. Belardelli,et al.  The essential role of endogenous IFN α/β in the anti‐metastatic action of sensitized T lymphocytes in mice injected with friend erythroleukemia cells , 1995 .

[76]  D. Kalvakolanu,et al.  Virus interception of cytokine-regulated pathways. , 1999, Trends in microbiology.

[77]  R. Schreiber,et al.  Targeted Disruption of the Stat1 Gene in Mice Reveals Unexpected Physiologic Specificity in the JAK–STAT Signaling Pathway , 1996, Cell.

[78]  T. Taniguchi.  Regulation of cytokine gene expression. , 1988, Annual review of immunology.

[79]  F. Chisari,et al.  Noncytolytic control of viral infections by the innate and adaptive immune response. , 2001, Annual review of immunology.

[80]  Norbert Perrimon,et al.  marelle Acts Downstream of the Drosophila HOP/JAK Kinase and Encodes a Protein Similar to the Mammalian STATs , 1996, Cell.