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Genetic changes in mammalian cells reminiscent of an SOS response

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Summary

Prior to the isolation of mammalian DNA repair genes and identification of their gene products, the comparison between the bacterial SOS response and various similar reactions in mammalian cells remains rather speculative. The increasing number of observed phenomena including enhanced DNA repair, virus induction, induced cellular differentiation, and neoplastic transformation, all following DNA damage or arrest of replication, are, however, suggestive of an SOS-like system of growth control and may form an entry into this fascinating area.

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References

  • Acheson NH (1980) Lytic cycle of SV 40 and polyoma virus. In: Tooze J (ed) DNA tumor viruses. Cold Spring Harbor Laboratory, pp 125–204

  • Althaus FR, Lawrence SD, He YZ, Sattler GL, Tsukada Y, Pitot HC (1982) Effects of altered [ADP-robose]n metabolism on expression of fetal functions by adult hepatocytes. Nature 300:366–368

    Google Scholar 

  • Arya SK (1980) Phorbol ester-mediated stimulation of the synthesis of mouse mammary tumour virus. Nature 284:71–72

    Google Scholar 

  • Ashburner M, Bonner JJ (1979) The induction of gene activity in Drosophila by heat shock. Cell 17:241–254

    Google Scholar 

  • Baran N, Neer A, Manor H (1983) “Onion skin” replication of integrated polyoma virus DNA and flanking sequences in polyomatransformed rat cells: termination within a specific cellular DNA segment. Proc Natl Acad Sci USA 80:105–109

    Google Scholar 

  • Bishop JM (1983) Cancer genes come of age. Cell 32:1018–1020

    Google Scholar 

  • Bockstahler LE, Lytle D (1970) Ultraviolet light enhanced reactivation of a mammalian virus. Biochem Biophys Res Commun 41:184–189

    Google Scholar 

  • Bockstahler LE, Lytle CD (1977) Radiation enhanced reactivation of nuclear replicating mammalian viruses. Photochem Photobiol 25:477–482

    Google Scholar 

  • Bodner AJ, Ting RC, Gallo RC (1981) Induction of differentiation of human promyelocytic cells (HL-60) by nucleosides and methotrexate. JNCI 67:1025–1030

    Google Scholar 

  • Botchan M, Topp S, Sambrook J (1979) Studies on simian virus 40 excision from cellular chromosomes. Cold Spring Harbor Symp Quant Biol 43:709–719

    Google Scholar 

  • Bresler SE, Kalinin VL, Shelegedin VN (1978) W-reactivation and W-mutagenesis of gamma-irradiated phage lambda. Mutat Res 49:341–355

    Google Scholar 

  • Campisi J, Medrano EE, Morreo G, Pardee AB (1982) Restriction point control of cell growth by a labile protein: evidence for increased stability in transformed cells. Proc Natl Acad Sci USA 79:436–440

    Google Scholar 

  • Cavenee WK, Dryja TP, Phillips RA, Benedict WF, Godbout R, Gallie BL, Murphree AL, Strong LC, White RL (1983) Expression of recessive alleles by chromosomal mechanisms in retinoblastoma. Nature 305:779–784

    Google Scholar 

  • Chan R, Buehring GC (1983) Antiglucocorticoids block the enhancement of mouse mammary tumor virus production by 12-0-tetradecanoylphorbol-13-acetate. Carcinogenesis 4:1611–1614

    Google Scholar 

  • Cleaver JE, Bodell WJ, Gruenert DC, Kapp LN, Kaufmann WK, Park SD, Zelle B (1982) In: Harris CC, Cerutti PA (eds) Mechanisms of chemical carcinogenesis. Alan R Liss, New York, pp 409–418

    Google Scholar 

  • Cornelis JJ, Lupker JH, van der Eb AJ (1980) UV-reactivation, virus production and mutagenesis of SV40 in UV-irradiated monkey kidney cells. Mutat Res 71:139–146

    Google Scholar 

  • Das Gupta UB, Summers WC (1978) Ultraviolet reactivation of herpes simplex virus is mutagenic and inducible in mammalian cells. Proc Natl Acad Sci USA 75:2378–2381

    Google Scholar 

  • Day RS III, Ziolkowski CHJ (1981) UV-induced reversion of adenovirus 5ts2 infecting human cells. Photochem Photobiol 34:403–406

    Google Scholar 

  • Defais MJ, Fauquet P, Radman M, Errera M (1971) Ultraviolet reactivation and ultraviolet mutagenesis of λ in different genetic systems. Virology 43:495–503

    Google Scholar 

  • Defais MJ, Hanawalt PC, Sarasin AR (1982) Viral probes for DNA repair. Adv Radiat Biol 10:1–37

    Google Scholar 

  • Ebert PS, Wars I, Buell DN (1976) Erythroid differentiation in cultured Friend leukemia cells treated with metabolic inhibitors. Cancer Res 36:1809–1813

    Google Scholar 

  • Emerit I, Cerutti P (1981) Clastogenic activity from Bloom syndrome fibroblast cultures. Proc Natl Acad Sci USA 78:1868–1872

    Google Scholar 

  • Fahmy MJ, Fahmy OG (1980) Intervening DNA insertions and the alteration of gene expression by carcinogens. Cancer Res 40:3374–3382

    Google Scholar 

  • Farzaneh F, Zalin R, Brill D, Shall S (1982) DNA strand breaks and ADP-ribosyl transferase activation during cell differentiation. Nature 300:362–366

    Google Scholar 

  • Fridman WH, Gresser I, Bandu MT, Aguet M, Neauport-Sautes C (1980) Interferon enhances the expression of Fcγ receptors. J Immunol 124:2436–2441

    Google Scholar 

  • Friend C, Scher W, Holland JG, Sato T (1971) Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethylsulfoxide. Proc Natl Acad Sci USA 68:378–382

    Google Scholar 

  • Gallant JA (1979) Stringent control in E. coli. Annu Rev Genet 13:393–415

    Google Scholar 

  • Gearhart PJ, Bogenhagen DF (1983) Clusters of point mutations are found exclusively around rearranged antibody variable genes. Proc Natl Acad Sci USA 80:3439–3443

    Google Scholar 

  • Gentil A, Margot A, Sarasin A (1982) Enhanced reactivation and nutagenesis after transfection of carcinogen-treated monkey kidney cells with UV-irradiated Simian virus 40 (SV40) DNA. Biochimie 64:693–696

    Google Scholar 

  • Gillies RJ (1982) Calcium, calmodulin and cAMP and the control of cellular proliferation. TIBS 7:233–235

    Google Scholar 

  • Griffin J, Munroe D, Major P, Kufe D (1982) Induction of differentiation of human mycloid leukemia cells by inhibitors of DNA synthesis. Exp Hematol 10:774–781

    Google Scholar 

  • Grummt F, Waltl G, Jantzen HM, Hamprecht K, Huebscher U, Kuenzle CC (1979) Diadenosine 5′, 5‴-P1, P4-tetraphosphate, a ligand of the 57-kilodalton subunit of DNA polymerase. Proc Natl Acad Sci USA 76:6081–6085

    Google Scholar 

  • Gunther M, Wicker R, Tiravy S, Coppey J (1980) Enhanced survival of ultraviolet-damaged parvovirus LuIII and Herpes virus in carcinogen-pretreated transformed human cells. In: Seeberg E, Kleppe K (eds) Chromosome damage and repair. Plenum, New York, pp 605–609

    Google Scholar 

  • Hampar B, Aaronson SA, Derge JG, Chakrabarty M, Showalter SD, Dunn CY (1976) Activation of an endogenous mouse type C virus by ultraviolet irradiated herpes simplex virus types 1 and 2. Proc Natl Acad Sci USA 73:646–650

    Google Scholar 

  • Hayward WS, Neel BG, Astrin SM (1981) Activation of a cellular one gene by promoter insertion in ALV-induced lymphoid leukosis. Nature 290:475–480

    Google Scholar 

  • Hentschel CC, Birnstiel ML (1981) The organization and expression of histone gene families. Cell 25:301–313

    Google Scholar 

  • Hill CK, Buonaguro FM, Myers CP, Han A, Elkind MM (1982) Fission-spectrum neutrons at reduced dose rates enhance neoplastic transformation. Nature 298:67–69

    Google Scholar 

  • Hynes NE, Groner B (1982) Mammary tumor formation and hormonal control of mouse mammary tumor virus expression. Curr Top Microbiol Immunol 101:51–74

    Google Scholar 

  • Jeeves WP, Rainbow AJ (1979a) γ-Ray enhanced reactivation of UV-irradiated adenovirus in normal human fibroblasts. Mutat Res 60: 33–41

    Google Scholar 

  • Jeeves WP, Rainbow AJ (1979b) γ-Ray enhanced reactivation of γ-irradiated adenovirus in human cells. Biochem Biophys Res Commun 90:567–574

    Google Scholar 

  • Johnstone AP, Williams GT (1982) Role of DNA breaks and ADP-ribosyl transferase activity in eurkaryotic differentiation demonstrated in human lymphocytes. Nature 300:368–370

    Google Scholar 

  • Kelley PM, Schlesinger MJ (1978) The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell 15:1277–1286

    Google Scholar 

  • Kennedy AR, Cairns J, Little JB (1984) Timing of the steps in transformation of C3H 10T 1/2 cells by X-irradiation. Nature 307:85–86

    Google Scholar 

  • Kenyon CJ (1983) The bacterial response to DNA damage. TIBS 8:84–87

    Google Scholar 

  • Kim S, Davis M, Sinn E, Patten P, Hood L (1981) Antibody diversity: somatic hypermutation of rearranged VH genes. Cell 27:573–581

    Google Scholar 

  • Kimchi A, Shure H, Revel M (1981) Anti-mitogenic function of interferon-induced (2′–5′) oligo (adenylate) and growth-related variations in enzymes that synthesize and degrade this oligonucleotide. Eur J Biochem 114:5–10

    Google Scholar 

  • Klein G, Lenoir G (1982) Translocations involving Ig-locus-carrying chromosomes: a model for genetic transcription in carcinogenesis. Adv Cancer Res 37:381–387

    Google Scholar 

  • Knudson AG (1981) Human cancer genes. In: Arrighi FE, Rao PN, Stubblefied E (eds) Genes, chromosomes and neoplasia. Raven Press, New York, pp 453–462

    Google Scholar 

  • Koch G, Bilello JA, Kruppa J, Koch F, Oppermann H (1980) Amplification of translational control by membrane-mediated events: a pleiotropic effect on cellular and viral gene expression. Ann NY Acad Sci 339:280–306

    Google Scholar 

  • Kogoma T, Lark KG (1975) Characterization of the replication of Escherichia coli DNA in the absence of protein synthesis: stable DNA replication. J Mol Biol 94:243–256

    Google Scholar 

  • Kogoma T, Torrey TA, Connaughton MJ (1979) Induction of UV-resistant DNA replication in Escherichia coli: induced stable DNA replication as an SOS function. Mol Gen Genet 176:1–9

    Google Scholar 

  • Land H, Parada LF, Weinberg RA (1983) Cellular oncogenes and multistep carcinogenesis. Science 222:771–778

    Google Scholar 

  • Lau CC, Pardee AB (1982) Mechanism by which caffeine potentiates lethality of nitrogen mustard. Proc Natl Acad Sci USA 79:2942–2946

    Google Scholar 

  • Lavi S (1982) Carcinogen-mediated activation of SV40 replicons: a model system for initiation of carcinogenesis. In: Schimke RT (ed) Gene amplification. Cold Spring Harbor Laboratory, pp 225–230

  • Lawrence CW, Christensen RB (1982) The mechanism of untargeted mutagenesis in UV-irradiated yeast. Mol Gen Genet 186:1–9

    Google Scholar 

  • Leder A, Leder P (1975) Butyric acid, a potent inducer of erythroid differentiation in cultured erythroleukemic cells. Cell 5:319–322

    Google Scholar 

  • Lee PC, Bochner BR, Ames BN (1983) AppppA, heat-shock stress, and cell ocidation. Proc Natl Acad Sci USA 80:7496–7500

    Google Scholar 

  • Lengyel P (1982) Biochemistry of interferons and their actions. Annu Rev Biochem 51:251–282

    Google Scholar 

  • Levenson R, Housman D (1981) Commitment: how do cells make the decision to differentiate? Cell 25:5–6

    Google Scholar 

  • Links J, Calafat J, Buijs F, Tol O (1977) Simultaneous chemical induction of MTV and MLV in vitro. Eur J Cancer 13:577–587

    Google Scholar 

  • Little JW, Mount DW (1982) The SOS regulatory system of Escherichia coli. Cell 29:11–22

    Google Scholar 

  • Livneh Z (1983) Directed mutagenesis method for analysis of mutagen specificity: application to ultraviolet-induced mutagenesis. Proc Natl Acad Sci USA 80:237–241

    Google Scholar 

  • Lytle CD, Goddard JG (1979) UV-enhanced virus reactivation in mammalian cells: effects of metabolic inhibitors. Photochem Photobiol 29:959–962

    Google Scholar 

  • Lytle CD, Day RS III, Hellman KB, Bockstahler LE (1976) Infection of UV-irradiated xeroderma pigmentosum fibroblasts by herpes simplex virus: study of capacity and Weigle reactivation. Mutat Res 36:257–264

    Google Scholar 

  • Lytle CD, Coppey J, Taylor WD (1978) Enhanced survival of ultraviolet-lirradiated herpes simplex virus in carcinogen-pretreated cells. Nature 272:60–62

    Google Scholar 

  • Mallick U, Rahmsdorf HJ, Yamamoto N, Ponta H, Wegner R-D, Herrlich P (1982) 12-0-Tetradecanoylphorbol 13-acetate-inducible proteins are synthesized at an increased rate in Bloom syndrome fibroblasts. Proc Natl Acad Sci USA 79:7886–7890

    Google Scholar 

  • Maness PF, Perry ME, Levy BT (1983) P1,P4-Di (adenosine-5′) tetraphosphate inhibits phosphorylation of Immunoglobulin G by Rous Sarcoma Virus pp60src. J Biol Chem 258:4055–4058

    Google Scholar 

  • Marks PA, Rifkind RA (1978) Erythroleucemic differentiation. Annu Rev Biochem 47:419–448

    Google Scholar 

  • Michalides R, van Deemter L, Nusse R, Hageman P (1979) Induction of mouse mammary tumor virus RNA in mammary tumors of BALB/c mice treated with urethane, X-irradiation, and hormones. J Virol 31:63–72

    Google Scholar 

  • Miller JH (1982) Carcinogens induce targeted mutations in Escherichia coli. Cell 31:5–7

    Google Scholar 

  • Miller JH (1983) Mutational specificity in bacteria. Annu Rev Genet 17:215–238

    Google Scholar 

  • Miskin R, Reich E (1980) Plasminogen activator: induction of synthesis by DNA damage. Cell 19:217–224

    Google Scholar 

  • Nomura S, Oishi M (1983) Indirect induction of erythroid differentiation in mouse Friend cells: evidence for two intracellular reactions involved in the differentiation. Proc Natl Acad Sci USA 80:210–214

    Google Scholar 

  • Okamura J, Letarte M, Stein LD, Sigal NH, Gelfand EW (1982) Modulation of chronic lymphocytic leukemia cells by phorbol ester: increase in la expression, IgM secretion and MLR stimulatory capacity. J Immunol 128:2276–2280

    Google Scholar 

  • Painter RB, Young BR (1980) Radiosensitivity in ataxia telangiectasia: a new explanation. Proc Natl Acad Sci USA 77:7315–7317

    Google Scholar 

  • Pech M, Höchtl J, Schnell H, Zachau HG (1981) Differences between germ-line and rearranged immunoglobulin VK coding sequences suggest a localized mutation mechanism. Nature 291:668–670

    Google Scholar 

  • Pelham HRB (1982) A regulatory upstream promoter element in the Drosophila Hsp 70 heat-shock gene. Cell 30:517–528

    Google Scholar 

  • Radman M (1980) Is there SOS induction in mammalian cells? Photochem Photobiol 32:823–830

    Google Scholar 

  • Rahmsdorf HJ, Mallick U, Ponta H, Herrlich P (1982) A B-lymphocyte specific high-turnover protein: constitutive expression in resting B cells and induction of synthesis in proliferating cells. Cell 29:459–468

    Google Scholar 

  • Rahmsdorf HJ, Koch N, Mallick U, Herrlich P (1983) Regulation of MHC class II invariant chain expression: induction of synthesis in human and murine plasmocytoma cells by arresting replication. EMBO J 2:811–816

    Google Scholar 

  • Rapaport E, Zamecnik PC (1976) Presence of diadenosine 5′,5‴-P1,P4-tetraphosphate (Ap4A) in mammalian cells in levels varying widely with proliferative activity of the tissue: a possible positive “pleiotypic activator”. Proc Natl Acad Sci USA 73:3984–3988

    Google Scholar 

  • Rommelaere J, Vos JM, Cornelis JJ, Ward DC (1981) UV-enhanced reactivation of minute-virus-of-mice: stimulation of a late step in the viral life cycle. Photochem Photobiol 33:845–854

    Google Scholar 

  • Rosén A, Klein G (1983) UV light-induced immunoglobulin heavy chain class switch in a human lymphoblastoid cell line. Nature 306:189–190

    Google Scholar 

  • Sachs L (1978) Control of normal cell differentiation and the phenotypic reversion of malignancy in myeloid leukaemia. Nature 274:535–539

    Google Scholar 

  • Sachs L, Lotem J (1979) Regulation of normal differentiation in mouse and human myeloid leukemic cells by phorbol esters and the mechanism of tumor promotion. Proc Natl Acad Sci USA 76:5158–5162

    Google Scholar 

  • Sarasin A, Benoit A (1980) Induction of an error-prone mode of DNA repair in UV-irradiated monkey kidney cells. Mutat Res 70:71–81

    Google Scholar 

  • Sarasin AR, Hanawalt PC (1978) Carcinogens enhance survival of UV-irradiated simian virus 40 in treated monkey kidney cells: induction of a recovery pathway? Proc Natl Acad Sci USA 75:346–350

    Google Scholar 

  • Sarasin A, Bourre F, Benoit A (1982) Error-prone replication of ultraviolet-irradiated Simian Virus 40 in carcinogen-treated monkey kidney cells. Biochemie 64:815–821

    Google Scholar 

  • Scher W, Friend C (1978) Breakage of DNA and alterations in folded genomes by inducers of differentiation in Friend erythroleukemic cells. Cancer Res 38:841–849

    Google Scholar 

  • Schiestl R, Wintersberger U (1983) Induction of mating type interconversion in a heterothallic strain of Saccharomyces cerevisiae by DNA damaging agents. Mol Gen Genet 191:59–65

    Google Scholar 

  • Schimke RT (1982) Studies on gene duplications and amplifications —an historical perspective. In: Schimke RT (ed) Gene amplification. Cold Spring Harbor Laboratory, pp 1–6

  • Schorpp M, Mallick U, Rahmsdorf HJ, Herrlich P (to be published) UV-induced extracellular factor from human fibroblasts communicates the UV-response to non-irradiated cells. Cell 37:861–868

  • Schwab M, Alitalo K, Varmus HE, Bishop JM, George D (1983) A cellular oncogene (c-ki-ras) is amplified, overexpressed, and located within karyotypic abnormalities in mouse adrenocortical tumor cells. Nature 303:497–501

    Google Scholar 

  • Sonenshein GE, Brawermann G (1976) Regulation of immunoglobulin synthesis in mouse myeloma cells. Biochemistry 15:5497–5500

    Google Scholar 

  • Sukumar S, Notario V, Martin-Zanca D, Barbacid M (1983) Induction of mammary carcinomas in rats by nitrosomethylurea involves malignant activation of H-ras-1 locus by single point mutations. Nature 306:658–661

    Google Scholar 

  • Surowy CS, Berger NA (1983) Diadenosine 5′,5‴-P1,P4-tetraphosphate stimulates processing of ADP-ribosylated poly (ADP-ribose) polymerase. J Biol Chem 258:579–583

    Google Scholar 

  • Terada M, Nudel U, Fibach E, Rifkind RA, Marks PA (1978) Changes in DNA associated with induction of erythroid differentiation by dimethyl sulfoxide in murine erythroleukemia cells. Cancer Res 38:835–840

    Google Scholar 

  • Tlsty T, Brown PC, Johnston R, Schimke RT (1982) Enhanced frequency of generation of methotrexate resistance and gene amplification in cultured mouse and hamster cell lines. In: Schimke RT (ed) Gene amplification. Cold Spring Harbor Laboratory, pp 231–238

  • Todd RF, Griffin JD, Ritz J, Nadler LM, Abrams T, Schlossman SF (1981) Expression of normal monocyte-macrophage differentiation antigen on HL60 promyelocytes undergoing differentiation induced by leucocyte-conditioned medium or phorbol diester. Leuk Res 5:491–495

    Google Scholar 

  • Topp WC, Lane D, Pollack R (1980) Transformation by SV40 and polyoma virus. In: Tooze J (ed) DNA tumor viruses. Cold Spring Harbor Laboratories, pp 266–269

  • Troll W, Klassen A, Janoff A (1970) Tumorigenesis in mouse skin: inhibition by synthetic inhibitors of proteases. Science 169:1211–1213

    Google Scholar 

  • Varshavsky A (1983) Diadenosine 5′,5‴-P1,P4-tetraphosphate: pleiotropically acting alarmone? Cell 34:711–712

    Google Scholar 

  • Vijayalaxmi, Evans HJ, Ray JH, German J (1983) Bloom's syndrome: evidence for an increased mutation frequency in vivo. Science 221:851–853

    Google Scholar 

  • Warren ST, Schultz RA, Chang CC, Wade MH (1981) Elevated spontaneous mutation rate in Bloom syndrome fibroblasts. Proc Natl Acad Sci USA 78:3133–3137

    Google Scholar 

  • Weimann BJ (1976) Induction of immunoglobulin synthesis in Abelson murine leukemia virus-transformed mouse lymphoma cells in culture. Cold Spring Harbor Symp Quant Biol XLI:163–164

    Google Scholar 

  • Wielckens K, Bredehorst R, Adamietz P, Hilz H (1982) Mono ADP ribosylation and poly ADP-ribosylation of proteins in normal and malignant tissue. Adv Enzyme Regul 20:20–37

    Google Scholar 

  • Witkin EM (1976) Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev 40:869–907

    Google Scholar 

  • Wong GHW, Clark-Lewis I, McKimm-Breschkin JL, Harris AW, Schrader JW (1983) Interferon-γ induces enhanced expression of Ia and H-2 antigens on B lymphoid, macrophage, and myeloid cell lines. J Immunol 131:788–793

    Google Scholar 

  • Zur Hausen H, O'Neill FJ, Freese UK (1978) Persisting oncogenic herpes virus induced by the tumour promoter TPA. Nature 272:373–375

    Google Scholar 

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  1. Kernforschungszentrum Karlsruhe, Institute of Genetics and Toxicology, University of Karlsruhe, Postfach 3640, D-7500, Karlsruhe, Germany

    P. Herrlich, H. Ponta & H. J. Rahmsdorf

  2. Institute of Genetics, University of Karlsruhe, Postfach 3640, D-7500, Karlsruhe, Germany

    P. Herrlich & U. Mallick

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  1. P. Herrlich
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Herrlich, P., Mallick, U., Ponta, H. et al. Genetic changes in mammalian cells reminiscent of an SOS response. Hum Genet 67, 360–368 (1984). https://doi.org/10.1007/BF00291392

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