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RNase L: Effector Nuclease of an Activatable RNA Degradation System in Mammals

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Cytoplasmic fate of messenger RNA

Part of the book series: Progress in Molecular and Subcellular Biology ((PMSB,volume 18))

Abstract

In eukaryotic cells, the degradation of messenger RNA (mRNA) is an essential determinant in the regulation of gene expression. Indeed, the need to rapidly interrupt cellular responses to various stimuli (growth or developmental) upon the disappearance of the inducing signal necessitates the tight regulation of the degradation process.

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References

  • Aguet M, Dembic Z, Merlin G (1988) Molecular cloning and expression of the human interferon Y receptor. Cell 55: 273–280

    Article  PubMed  CAS  Google Scholar 

  • Baglioni C, Minks MA, Maroney PA (1978) Interferon action may be mediated by activation of a nuclease by pppA2´p5A2´p5´A. Nature 273: 784–787

    Article  Google Scholar 

  • Bayard B, Bisbal C, Silhol M, Cnockaert J, Huez G, Lebleu B (1984) Increased stability and antiviral activity of 2´-0-phosphoglyceryl derivatives of (2´–5´)oligo(adenylate). Eur J Biochem 142: 291–298

    Article  PubMed  CAS  Google Scholar 

  • Bayard B, Bette-Bobillo P, Aliau S (1994) Affinity purification and characterization of (2´5´)oligo(adanylate)-dependent RNase from mouse spleen. Eur J Biochem 223: 403–410

    Article  PubMed  CAS  Google Scholar 

  • Benech P, Mory Y, Revel M, Chebath J (1985) Structure of two forms of the interferon-induced (2´–5´) oligo A synthetase of human cells based on cDNAs and gene sequences. EMBO J 4: 2249–2256

    PubMed  CAS  Google Scholar 

  • Bisbal C, Silhol M, Lemaitre M, Bayard B, Salehzada T, Lebleu B (1987) 5´-modified agonist and antagonist (2´-5´)(A)n analogues: synthesis and biological activity. Biochemistry 26:5172–5178

    Google Scholar 

  • Bisbal C, Salehzada T, Lebleu B, Bayard B (1989) Characterization of two murine (2´-5´)(A)n-dependent endonucleases of different molecular mass. Eur J Biochem 179: 595–602

    Article  PubMed  CAS  Google Scholar 

  • Bisbal C, Martinand C, Silhol M, Lebleu B, Salehzada T (1995) Cloning and characterization of a RNase L inhibitor. J Biol Chem 270: 13308–13317

    Article  PubMed  CAS  Google Scholar 

  • Brown GE, Lebleu B, Kawakita M, Shaila S, Sen GC, Lengyel P (1976) Increased endonuclease activity in an extract from mouse Ehrlich ascites tumor cells which had been treated with a partially purified interferon preparation: dependence on double-stranded RNA. Biochem Biophys Res Commun 69: 114–122

    Article  PubMed  CAS  Google Scholar 

  • Cayley P, Knight M, Kerr IM (1982) Virus-mediated inhibition of the ppp(A2´p)nA system and its prevention by interferon. Biochem Biophys Res Commun 104: 376–382

    Article  PubMed  CAS  Google Scholar 

  • Chebath J, Benech P, Hovanessian AG, Galabru J, Revel M (1987a) Four different forms of interferon-induced 2´,5´ oligo(A)synthetase identified by immunoblotting in human cells. J Biol Chem 262: 3852–3857

    CAS  Google Scholar 

  • Chebath J, Benech P, Revel M, Vigneron M (1987b) Constitutive expression of (2´-5´)oligo A synthetase confers resistance to Picornavirus infection. Nature 330: 587–588

    Article  CAS  Google Scholar 

  • Clemens MJ, Williams BRG (1978) Inhibition of cell-free protein synthesis by pppA2´p5´A2´p5´A a novel oligonucleotide synthesized by interferon-treated L cell extracts. Cell 13: 565–572

    Article  PubMed  CAS  Google Scholar 

  • Decker T, Lew D, Mirkovitch J, Darnell JE jr (1991) Cytoplasmic activation of GAF, an IFN-y-regulated DNA binding factor. EMBO J 10: 927–932

    PubMed  CAS  Google Scholar 

  • Dong B, Silverman R (1995) 2-5A-dependent RNase molecules dimerize during activation by 2–5A. J Biol Chem 270:4133–4137

    Google Scholar 

  • Dong B, Xu L, Hassel B, Lee X, Torrence P, Silverman R (1994) Intrinsic molecular activities of the interferon-induced 2-5A-dependent RNase. J Biol Chem 269: 14153–14158

    PubMed  CAS  Google Scholar 

  • Einat M, Resnitzki D, Kimchi A (1985) Close link between reduction of c-myc expression by interferon and G0/G1 arrest. Nature 313: 597–600

    Article  PubMed  CAS  Google Scholar 

  • Eppstein DA, Marsh VY, Schryver BB, Larsem MA, Barnett JW, Verheyden JPH, Prisbe E (1982) Analogs of (A2´p)nA. Correlation of structure of analogs of ppp(A2´p)2A and (A2´p)2A with stability and biological activity. J Biol Chem 257: 13390–13397

    PubMed  CAS  Google Scholar 

  • Floyd-Smith G, Slattery E, Lengyel P (1981) Interferon action: RNA cleavage pattern of a (2´–5´)oligoadenylate-dependent endonuclease. Science 212: 1030–1032

    Article  PubMed  CAS  Google Scholar 

  • Floyd-Smith G, Yoshie O, Lengyel P (1982) Covalent linkage of (2´–5´)pppApApA(32P)pCp to (2´–5´)(A)n-dependent ribonuclease in cell extracts by ultraviolet irradiation. J Biol Chem 257: 8584—8587

    Google Scholar 

  • Fu XY, Schindler C, Improta T, Aebersold R, Darnell JE jr (1992) The proteins of ISGF-3, the interferon α-induced transcriptional activator, define a gene family involved in signal transduction. Proc Natl Acad Sci USA 89: 7840–7843

    Article  PubMed  CAS  Google Scholar 

  • Gray PW, Leung DW, Pennica D, Yelverton E, Najaria P, Simonsen CC, Derynnck D, Sherwood PJ, Wallace DM, Berger SL, Levinson AD, Goeddel DV (1982) Expression of human immune interferon cDNA in E. coli and monkey cells. Nature 295: 503–508

    Article  PubMed  CAS  Google Scholar 

  • Gribaudo G, Lembo D, Cavallo G, Landolfo S, Lengyel P (1991) Interferon action: binding of viral RNA to the 40-kilodalton 2´-5´-oligoadenylate synthetase in interferon-treated HeLa cells infected with encephalomyocarditis virus. J Virol 65: 1748–1757

    PubMed  CAS  Google Scholar 

  • Harada H, Fujita T, Miyamoto M, Kimura Y, Maruyama M, Furia A, Miyata T, Taniguchi T (1989) Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell 58: 729–739

    Article  PubMed  CAS  Google Scholar 

  • Hassel B, Zhou A, Sotomayor C, Maran A, Silverman R (1993) A dominant negative mutant of 2-5A-dependent RNase suppresses antiproliferative and antiviral effects of interferon EMBO J 12: 3297–3304

    CAS  Google Scholar 

  • Hovanessian AG, Kerr IM (1978) Synthesis of an oligonucleotide inhibitor of protein synthesis in rabbit reticulocyte lysates analogous to that formed in extracts from interferon-treated cells. Eur J Biochem 84: 149–159

    Article  PubMed  CAS  Google Scholar 

  • Hovanessian AG, Brown RE, Kerr IM (1977) Synthesis of low molecular weight inhibitor of protein synthesis with enzyme from interferon-treated cells. Nature 268: 537–540

    Article  PubMed  CAS  Google Scholar 

  • Hovanessian AG, Laurent AG, Chebath J, Galabru J, Robert N, Svab J (1987) Identification of 69 kd and 100 kd forms of 2-5A synthetase in interferon-treated human cells by specific monoclonal antibodies. EMBO J 6: 1273–1280

    PubMed  CAS  Google Scholar 

  • Hovanessian G, Svab J, Marié I, Robert N, Chamaret S, Laurent AG (1988) Characterization of 69-100-kDa forms of 2-5A synthetase from interferon-treated human cells. J Biol Chem 263: 4945–4949

    PubMed  CAS  Google Scholar 

  • Isaacs A, Lindenmann J (1957) Virus interference. I. The interferon. Proc R Soc Lond Biol Sci 147: 258–267

    Article  CAS  Google Scholar 

  • Jackson RJ (1993) Cytoplasmic regulation of mRNA function: the importance of the 3´ untranslated region. Cell 74: 9–14

    Article  PubMed  CAS  Google Scholar 

  • Jaramillo M, Abraham N, Bell JC (1995) The interferon system: a review with emphasis on the role of PKR in growth control. Cancer Invest 13 (3): 327–338

    Article  PubMed  CAS  Google Scholar 

  • Johnston MI, Head WG (1987) Characterization of a 2´-phosphodiesterase from bovine spleen. J Biol Chem 262: 8377–8382

    PubMed  CAS  Google Scholar 

  • Jonak GJ, Knight E jr (1984) Selective reduction of c-myc mRNA in Daudi cells by human ß interferon. Proc Natl Acad Sci USA 81: 1747–1750

    Article  PubMed  CAS  Google Scholar 

  • Kerr IM, Brown RE (1978) pppA2´p5´A2´p5´A an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc Natl Acad Sci USA 75:256–260

    Google Scholar 

  • Kerr IM, Brown RE, Ball LA (1974a) Increased sensitivity of cell-free protein synthesis to double-stranded RNA after interferon treatment. Nature 250: 57–59

    Article  CAS  Google Scholar 

  • Kerr IM, Friedman RE, Brown RE, Ball A, Brown JC (1974b) Inhibition of protein synthesis in cell-free systems from interferon-treated infected cells: furter characterization and effect of formylmethionyl-t-RNA. J Virol 13: 9–21

    CAS  Google Scholar 

  • Kerr IM, Brown RE, Clemens MJ, Gilbert CS (1976) Interferon-mediated inhibition of cell-free-protein synthesis in response to double-stranded RNA. Eur J Biochem 69: 551–561

    Article  CAS  Google Scholar 

  • Knight M, Cayley PJ, Silverman RH, Wreschner DH, Gilbert CS, Brown RE, Kerr IM (1980) Radioimmune, radiobinding and HPLC analysis of 2-5A and related oligonucleotides from intact cells. Nature 288: 189–192

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Haque J, Lacoste J, Hiscott J, Williams BRG (1994) Double-stranded RNA-dependent protein kinase activates transcription factor NF-кB by phosphorylating IкB. Proc Natl Acad Sci USA 91: 6288–6292

    Article  PubMed  CAS  Google Scholar 

  • Lin SL, Garber EA, Wang E, Galiguiri LA, Schellekens H, Goldberg AR, Tamm I (1983) Reduced synthesis of pp60 Src and expression of the transformation-related phenotypes in interferon-treated Rous sarcoma virus-transformed rat cells. Mol Cell Biol 3: 1656–1664

    PubMed  CAS  Google Scholar 

  • Maitra RK, Li G, Xiao W, Dong B, Torrence P, Silverman R (1995) Catalytic cleavage of an RNA target by 2–5A antisense and RNase L. J Biol Chem 270: 15071–15075

    Article  PubMed  CAS  Google Scholar 

  • Maran A, Maitra R, Kumar A, Dong B, Xia W, Li G, William BRG, Torrence P, Silverman R (1994) Blockage of NF-кB signaling by selective ablation of an mRNA target by 2–5A antisens chimeras. Science 265: 789–792

    Article  PubMed  CAS  Google Scholar 

  • Marié I, Hovanessian AG (1992) The 69-kDa 2–5A synthetase is composed of two homologous and adjacent functional domains. J Biol Chem 267: 9933–9939

    PubMed  Google Scholar 

  • Martinand C, Bisbal C, Silhol M, Lebleu B. Salehzada T (1994) Constitutive expression of sense and antisense constructions of RLI in human cells modify the RNase L pathway. J Interferon Res 14 (Suppl 1): 102

    Google Scholar 

  • Martinand C, Salehzada T, Silhol M, Lebleu B, Bisbal C (1995) The RNase L inhibitor (RLI) is induced by poly(I)poly(C). J Interferon Res 15 (Suppl 1): 148

    Google Scholar 

  • Merlin G, Chebath J, Benech P, Metz, Revel M (1983) Molecular cloning and sequence of partial cDNA for interferon-induced (2´5´)oligo(A)synthetase mRNA from human cells. Proc Natl Acad Sci USA 80: 4904–4908

    Article  PubMed  CAS  Google Scholar 

  • Meurs E, Hovanessian AG (1988) α-Interferon inhibits the expression of heavy µ messager RNA in Daudi cells. EMBO J 7:1689–1696

    Google Scholar 

  • Meurs E, Chong K, Galabru J, Thomas N, Kerr I, Williams BRG, Hovanessian AG (1990) Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62: 379–390

    Article  PubMed  CAS  Google Scholar 

  • Miyamoto M, Fujita T, Kimura Y, Maruyama M, Harada H, Sudo Y, Miyata T, Taniguchi T (1988) Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-ß gene regulatory elements. Cell 54: 903–913

    Article  PubMed  CAS  Google Scholar 

  • Mory Y, Vaks B, Chebath J (1989) Production of two human 2´-5´-oligoadenylate synthetase enzymes in Escherichia coli . J Interferon Res 9: 295–304

    Article  PubMed  CAS  Google Scholar 

  • Mundschau L, Faller D (1995) Platelet-derived growth factor signal transduction through the interferon-inducible kinase PKR. J Biol Chem 270: 3100–3106

    Article  PubMed  CAS  Google Scholar 

  • Nagata S, Mantei N, Weissmann C (1980) The structure of one of the eight or more chromosomal genes for human interferon α. Nature 28: 401–408

    Article  Google Scholar 

  • Naylor SL, Sakagushi AY, Shows TB, Law ML, Goeddel DV, Gray PW (1983) Human immune interferon gene is located on chromosome 12. J Exp Med 157: 1020–1027

    Article  PubMed  CAS  Google Scholar 

  • Nilsen TW, Maroney PA, Baglioni C (1981) Double-stranded RNA causes synthesis of 2´-5´-oligo(A) and degradation of messenger RNA in interferon-treated cells. J Biol Chem 256: 7806–7811

    PubMed  CAS  Google Scholar 

  • Owerbach D, Rutter WJ, Shows TB, Gray P, Goeddel DV, Lawn RM (1981) Leucocyte and fibroblast interferon genes are located on human chromosome 9. Proc Natl Acad Sci USA 78: 3123–3127

    Article  PubMed  CAS  Google Scholar 

  • Paucker K, Can tell K, Henle W (1962) Quantitative studies on viral interference in suspended L cells. III. Effect of interfering viruses and interferon on the growth rate of cells. Virology 17: 324–334

    Article  PubMed  CAS  Google Scholar 

  • Pellegrini S, Schindler C (1993) Early events in signalling by interferons. Trends Biochem Sci 18: 338–342

    Article  PubMed  CAS  Google Scholar 

  • Proud CG (1995) PKR: a new name and new roles TIBS 20: 241–246

    CAS  Google Scholar 

  • Ratner L, Wiegand RC, Farrell PJ, Sen GC, Cabrer B, Lengyel P (1978) Interferon, double stranded RNA and RNA degradation. Fractionation of the endonuclease TNT system into two macromolecular components: role of a small molecule in nuclease activation. Biochem Biophys Res Commun 81: 947–954

    Article  PubMed  CAS  Google Scholar 

  • Rosa F, Cochet M, Fellous M (1986) Interferon and major histocompatibility complex genes: a model to analyse eucaryotic gene regulation ? Interferon 7:47–87, Harcourt Brace Jovanovich, Academic Press, London

    Google Scholar 

  • Sach B (1993) Messenger RNA degradation in eucaryotes. Cell 74: 413–421

    Article  Google Scholar 

  • Salehzada T, Silhol M, Lebleu B, Bisbal C (1991a) Polyclonal antibodies against RNase L. Subcellular localization of this enzyme in mouse cells. J Biol Chem 266: 5808–5813

    CAS  Google Scholar 

  • Salehzada T, Silhol M, Lebleu B, Bisbal C (1991b) Regeneration of enzyme activity after Western blot: activation of RNase L by 2–5A on filter. Importance for its detection. Anal Biochem 196: 410–414

    Article  CAS  Google Scholar 

  • Salehzada T, Silhol M, Steff AM, Lebleu B, Bisbal C (1993) 2´,5´-oligoadenylate-dependent RNase L is a dimer of regulatory and catalytic subunits. J Biol Chem 268:7733–7740

    Google Scholar 

  • Schindler C, Darnell JE (1995) Transcriptional responses to polypeptide ligands: the Jak-STAT pathway. Annu Rev Biochem 64: 621–651

    Article  PubMed  CAS  Google Scholar 

  • Schindler C, Fu XY, Improta T, Aebersold R, Darnell JE Jr (1992) Proteins of transcription factor ISGF-3: one gene encodes the 91- and 84-kDa ISGF-3 proteins that are activated by interferon α. Proc Natl Acad Sci USA 89: 7836–7839

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Zilberstein A, Shulman L, Federman P, Berissi H, Revel M (1978) Interferon action: isolation of nuclease F, a translation inhibitor activated by interferon-induced (2´-5´)oligo-isoadenylate. Febs Lett 95: 257–264

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Chernajovsky Y, Shulman L, Federman P, Berissi H, Revel M (1979) An interferon-induced phosphodiesterase degrading (2´,5´) oligoisoadenylate and C-C-A terminus of tRNA. Proc Natl Acad Sci USA 76: 4788–4792

    Article  PubMed  CAS  Google Scholar 

  • Sen GC, Lengyel P (1992) The interferon system, a bird’s eye view of its biochemistry. J Biol Chem 267: 5017–5020

    PubMed  CAS  Google Scholar 

  • Sen GC, Lebleu B, Brown GE, Kawakita M, Slattery E, Lengyel P (1976) Interferon, double-stranded RNA and mRNA degradation. Nature 264: 370–373

    Article  PubMed  CAS  Google Scholar 

  • Silverman RH (1985) Functional analysis of 2–5A-dependent RNase and 2–5A using 2´5´ oligo-adenylate-cellulose. Anal Biochem 144: 450–460

    Article  PubMed  CAS  Google Scholar 

  • Silverman R, Skehel J, James T, Wreschner D, Kerr IM (1984) rRNA cleavage as an index of ppp(A2´p)nA activity in interferon-treated encephalomyocarditis virus-infected cells. J Virol 46:1051–1055

    Google Scholar 

  • Slattery E, Ghosh N, Samanta H, Lengyel P (1979) Interferon, double-stranded RNA and RNA degradation: activation of an endonuclease by (2´-5´)An. Proc Natl Acad Sci USA 76: 4778–4782

    Article  PubMed  CAS  Google Scholar 

  • Sperling J, Chebath J, Arad-Dann H, Offen D, Spann P, Lehrer R, Goldblatt D, Jolles B, Sperling R (1991) Possible involvement of (2´–5´)oligoadenylate synthetase activity in pre-mRNA splicing. Proc Natl Acad Sci USA 88: 10377–10381

    Article  PubMed  CAS  Google Scholar 

  • Staeheli P, Haller O, Boll W, Lindenmann J, Weissman C (1986) Mx protein: constitutive expression in 3T3 cells transformed with cloned Mx cDNA confers selective resistance to influenza virus. Cell 44: 147–158

    Article  PubMed  CAS  Google Scholar 

  • Taniguchi T, Mantei N, Swarztein M, Nagata S, Muramatsu M, Weissmann C (1980) Human leukocyte and fibroblast interferons are structurally related. Nature 285: 547–549

    Article  PubMed  CAS  Google Scholar 

  • Tavernier J, Derynck R, Fiers W (1981) Evidence for a unique human fibroblast interferon (IFN-ß l) chromosomal gene, devoid of intervening sequences. Nucl Acids Res 9: 461–471

    Article  PubMed  CAS  Google Scholar 

  • Torrence PF, Xiao W, Li G, Khamnei S (1994) Development of 2´,5´-oligonucleotides as potential therapeutic agents. Curr Med Chem 1: 176–191

    CAS  Google Scholar 

  • Trent YM, Olson S, Lawr RM (1982) Chromosomal localization of human leucocyte, fibroblaste and immune interferon genes by means of in situ hybridization. Proc Natl Acad Sci USA 79: 7809–7813

    Article  PubMed  CAS  Google Scholar 

  • Uzé G, Lutfalla G, Gresser I (1990) Genetic transfer of functional human interferon α receptor into mouse cells: cloning and expression of its cDNA. Cell 60: 225–234

    Article  PubMed  Google Scholar 

  • Uzé G, Lutfalla G, Mogensen K (1995) α and ß interferons and their receptor and their friends and relations. J Interferon Res 15:3–26

    Google Scholar 

  • Williams BRG (1991) Transcriptional regulation of interferon-stimulated genes. Eur J Biochem 200: 1–11

    Article  PubMed  CAS  Google Scholar 

  • Williams BRG, Saunders ME, Williard HF (1986) Interferon-regulated human 2´-5´ synthetase gene maps to chromosome 12. Somat Cell Mol Genet 12: 403–408

    Article  PubMed  CAS  Google Scholar 

  • Wreschner DH, McCauley JW, Skehel JJ, Kerr IM (1981) Interferon action-sequence specificity of the ppp(A2´p)nA-dependent ribonuclease. Nature 289: 414–417

    Article  PubMed  CAS  Google Scholar 

  • Zhou A, Hassel B, Silverman R (1993) Expression cloning of 2-5A-dependent RNase: a uniquely regulated mediator of interferon action. Cell 72: 753–765

    Article  PubMed  CAS  Google Scholar 

  • Zilberstein A, Kimchi A, Schmidt A, Revel M (1978) Isolation of two interferon-induced translational inhibitors: a protein kinase and an oligo-isoadenylate synthetase. Proc Natl Acad Sci USA 75: 4734–4738

    Article  PubMed  CAS  Google Scholar 

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Bisbal, C. (1997). RNase L: Effector Nuclease of an Activatable RNA Degradation System in Mammals. In: Jeanteur, P. (eds) Cytoplasmic fate of messenger RNA. Progress in Molecular and Subcellular Biology, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-60471-3_2

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