Molecular and biochemical features of poly (ADP-ribose) metabolism

Althaus FR, Richter CR: ADP-ribosylation of proteins: Enzymology and biological significance. Part I, Molecular biology, biochemistry and biophysics, vol. 37. Springer-Verlag, Berlin, 1987, pp 1–125 de Murcia G, Huletsky A, Poirier GG: Review: Modulation of chromatin structure by poly(ADP-ribosyl)ation. Biochem Cell Biol 66:626–635, 1988 Boulikas T: Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation) (Review). Anticancer Res 11: 489–528, 1991 Cherney BW, McBride WO, Chen D, Alkhatib H, Bhatia K, Hensely P, Smulson ME: cDNA sequence, proteins structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci (USA) 84:8370–8374, 1987 Kurosaki T, Ushiro H, Mitsuuchi Y, Suzuki S, Matsuda M, Matsuda Y, Katanuma N, Kangawa K, Matsuo H, Hirose T, Inayama A, Shizuta Y: Primary structure of human poly(ADP-ribose) synthetase as deduced from cDNA sequence. J Biol Chem 262: 15990–15997, 1987 Suzuki H, Uchida K, Shima H, Sato T, Okamoto T, Kimura T, Miwa M: Molecular cloning of cDNA for human poly(ADP-ribose) polymerase and expression of its gene during HL-60 cell differentiation. Biochem Biophys Res Commun 146:403–409, 1987 Gradwohl G, Ménissier-de Murcia J, Molinete M, Simonin F, Koken M, Hoeijmakers JHJ, de Murcia G: The second zinc finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc Natl Acad Sci USA 87:2990–2994, 1990 Ikejima M, Noguchi S, Yamashita R, Ogura T, Sugimura T, Gill DM, Miwa M: The zine fingers of human poly(ADP-ribose) polymerase are differentially required for the recognition of DNA breaks and nicks and the consequent enzyme activation other structures recognize intact DNA. J Biol Chem 265:21907–21913, 1990 Simonin F, Ménissier-de Murcia J, Poch O, Muller S, Gradwohl G, Molinete M, Penning C, Keith G, de Murcia G: Expression and site-directed mutagenesis of the catalytic domain of human poly(ADP-ribose) polymerase in E. coli. J Biol Chem 265: 19249–19256, 1990 Hatakeyama K, Nemoto Y, Ueda K, Hayaishi O: Purification and characterization of poly(ADP-ribose) glycohydrolase. Different modes of action on large and small poly(ADP-ribose). J Biol Chem 261:14902–14911, 1986 Tanuma S, Kawashima K, Endo H: Identification of two activities of poly(ADP-ribose)n glycohydrolase in HeLa S3 cells. Biochem Biophys Res Commun 135:979–986, 1986 Thomassin H, Jacobson MK, Guay J, Verreault A, Aboul-Ela N, Ménard L, Poirier GG: An affinity matrix for the purification of poly(ADP-ribose) glycohydrolase. Nucl Acid Res 18:4691–4694, 1990 Chambon P, Doly JD, Strosser MT, Mandel P: On the formation of a novel adenylic compound by enzymatic extracts of liver nuclei. Biochem Biophys Commun 25:638–643, 1966 Doly JD, Petek F: Étude de la structure d'un composé ‘poly (ADP-ribose)’ synthétisé par des extraits nucléaires de foie de poulet. CR Hebd Acad Sci Ser D Sci Nat 263:1341–1344, 1966 Minaga T, Kun E: Probable helical conformation of poly(ADP-ribose). J Biol Chem 258:5726–5730, 1983 Minaga T, Kun E: Spectral analysis of the conformation of poly (adenosine diphosphoribose). J Biol Chem 258:725–730, 1983 Kanai Y, Fujiwara M: Naturally occuring antibodies to poly (ADP-ribose) in autoimmune MRL Mp-Ipr Ipr mice. Clin Exp Immunol 59:132–138, 1985 Sibley JT, Braun RP, Lee JS: The production of antibodies to DNA in normal mice following immunization with poly(ADP-ribose). Clin Exp Immunol 64:563–569, 1986 Alvarez-Gonzalez R, Jacobson MK: Characterization of polymer of ADP-ribose generatedin vitro andin vivo. Biochemistry 26:3218–3224, 1987 Kanai Y, Miwa M, Kuchina Y, Sugimura T: Presence of branched portion in poly(adenosine diphosphate ribose)in vivo. J Biol Chem 257:6217–6223, 1982 Miwa M, Saikawa N, Yamaizumi Z, Nishimura S, Sugimura T: Structure of poly(adenosine diphosphate ribose): Identification of 2′-(1″-ribosyl-2″-(or3″) (1″'-ribosyl)) adenosine-5′, 5″, 5″'-tri (phosphate) as a branch linkage. Proc Natl Acad Sci (USA) 76: 595–599, 1979 Miwa M, Ishihara M, Takishima S, Takasuka N, Maeda M, Yamaizumi Z, Sugimura T: The branched and linear portions of poly(adenosine diphosphate ribose) have the same α (1–2) ribose-ribose linkage. J Biol Chem 256:2916–2921, 1981 Aboul-Ela N, Jacobson EL, Jacobson MK: Labelling methods for the study of poly(ADP-ribose) and mono (ADP-ribose) metabolism in cultured cells. Anal Biochem 174:239–250, 1988 Juarez-Salinas H, Levi V, Jacobson EL, Jacobson MK: Poly (ADP-ribose) has a branched structurein vivo. J Biol Chem 257: 607–609, 1982 Juarez-Salinas H, Mendoza-Alvarez H, Levi V, Jacobson MK, Jacobson EL: Simultaneous determination of linear and branched residues in poly (ADP-ribose). Anal Biochem 131:410–418, 1983 Lautier D, Poirier D, Boudreau A, Jamali MA, Castonguay A, Poirier GG: Stimulation of poly(ADP-ribose) synthesis by free radicals in C3H10T1/2 cells: Relationship, with NAD metabolism and DNA breakage. Biochem Cell Biol 68:602–608, 1990 Hayashi K, Tanaka M, Shimada T, Miwa M, Sugimura T: Size and shape of poly(ADP-ribose): Examination by gel filtration, gel electrophoresis and electron microscopy. Biochem Biophys Res Commun 112:102–107, 1983 Alvarez-Gonzalez R, Althaus FR: Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA damaging agents. Mutation Res 218:67–74, 1989 Berger NA: Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res 101:4–15, 1985 Jonsson GG, Jacobson EL, Jacobson MK: The effect of hyperthermia on poly(ADP-ribose) metabolism. Cancer Res 48: 4233–4239, 1988 Ueda K, Okayama H, Fukushima M, Hayaishi O: Purification and analysis of the poly(ADP-ribose) synthetase system. J Biochem 77:1–11, 1975 Ueda K, Zhang J, Hayaishi O Immobilized poly(ADP-ribose) synthetase: Preparation and properties. In: FR Althaus, H Hilz, S Shall (eds.) ADP-ribosylation of Proteins, Springer-Verlag, Berlin, Heidelberg, New York, 1985, pp 47–51 Desmarais Y, Ménard L, Lagueux J, Poirier GG: Enzymological properties of poly(ADP-ribose) polymerase: Characterization of automodification sites and of its NADase activity. Biochim Biophys Acta 1078:179–186, 1991 Ueda K, Kawaichi M, Okayama H, Hayaishi O: Poly(ADP-ribosyl)ation of nuclear proteins. J Biol Chem 254:679–687, 1979 Yoshihara K, Hashida T, Tanaka Y, Matsunami N, Yamaguchi A, Kamiya T: Mode of enzyme-bound poly(ADP-ribose) synthesis and histone modification by reconstituted poly(ADP-ribose) polymerase-DNA cellulose complex. J Biol Chem 256:3471–3478, 1981 Ikejima M, Marsischky G, Gill DM: Direction of elongation of poly(ADP-ribose) chains. Addition of residues at the polymerase-proximal terminus. J Biol Chem 262:17641–17650, 1987 Naegeli H, Althaus FR: Regulation of poly(ADP-ribose) polymerase. Histone-specific adaptations of reaction products. J Biol Chem 266:10596–10601, 1991 Hatakeyama K, Nemoto Y, Ueda K, Hayaishi O: Poly(ADP-ribose) glycohydrolase and ADP-ribosyl group turnover. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions. Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 47–52 Miwa M, Sugimura T: Splitting of the ribose-ribose linkage of poly(adenosine diphosphate-ribose) by calf thymus extract. J Biol Chem 246:6362–6364, 1971 Miwa M, Tanaka M, Matsushima T, Sugimura T: Purification and properties of a glycohydrolase from calf thymus splitting the ribose-ribose linkage of poly(adenosine diphosphate ribose). J Biol Chem 249:3475–3482, 1974 Ikejima M, Gill DM: Poly(ADP-ribose) degradation by glycohydrolase starts with an endonucleotytic incision. J Biol Chem 263:11037–11040, 1988 Jonsson GG, Ménard L, Jacobson EL, Poirier GG, Jacobson MK: Effect of hyperthermia on poly(adenosine diphosphate-ribose) glycohydrolase. Cancer Res 48:4240–4243, 1988 Burzio LO, Riquelme PT, Ohtsuka E, Koide SS: Evidence for two variants of poly(adenosine diphosphate ribose) glycohydrolase in rat testis. Arch Biochem Biophys 173:306–319, 1976 Tanuma S: Purification and properties of two forms of poly (ADP-ribose) glycohydrolase. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions. Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 119–124 Tanuma S, Endo H: Purification and characterization of an (ADP-ribose)n glycohydrolase from human erythrocytes. Eur J Biochem 191:57–63, 1990 Weinberg DH, Collins KL, Simaneh P, Russo A, Wold MS, Virshys DM, Kelly TJ: Reconstitution of simian virus 40 DNA replication with purified proteins. Proc Natl Acad Sci (USA) 87; 8692–8696, 1990 Yamanaka H, Penning CA, Willis EH, Wasson B, Carson DA: Characterization of human poly(ADP-ribose) polymerase with autoantibodies. J Biol Chem 263:3879–3883, 1988 Futai M, Mizuno D: A new phosphodiesterase forming nucleoside 5′-monophosphate from rat liver. J Biol Chem 242:5301–5307, 1967 Okayama H, Honda M, Hayaishi O: Novel enzyme from rat liver that cleaves an ADP-ribosyl histone linkage. Proc Natl Acad Sci (USA) 75:2254–2257, 1978 Oka J, Ueda K, Hayaishi O, Komura H, Nakanishi K: ADP-ribosyl protein lyase. Purification, properties and identification of the product. J Biol Chem 259:986–993, 1984 Adamietz P, Rudolph A: ADP-ribosylation of nuclear proteinsin vivo. J Biol Chem 259:6841–6846, 1984 Baker JC, Smale ST, Tijan R, Ames BN: Inhibition of simian virus SV40 DNA replicationin vitro by poly(ADP-ribosyl)ated diadenosine tetraphosphate. J Biol Chem 262:14955–14959, 1987 Yoshihara K, Tanaka Y: ADP-ribosylation of diadenosine 5′,5″',-P1,P4-tetraphosphate by poly(ADP-ribose) polymerasein vitro. J Biol Chem 256:6756–6761, 1981 Rapaport E, Zamecnick PC, Baril EF: Association of diadenosine 5′,5″'-P1,P4-tetraphosphate binding protein with HeLa cell DNA polymerase alpha. J Biol Chem 256:12148–12151, 1981 Kun E, Zimber PH, Chang AC, Puschendorf B, Grunicke H: Macromolecular enzymatic product of NAD in liver mitochondria. Proc Natl Acad Sci (USA) 72:1436–1440, 1975 Thomassin H, Niedergang C, Mandel P: Characterization of the poly(ADP-ribose) polymerase associated with free cytoplasmic mRNA protein particles. Biochem Biophys Res Commun 133: 654–661, 1985 Thomassin H, Mandel P: Poly(ADP-ribosyl)ation in free cytoplasmic mRNA-protein complexes. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions. Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 125–129 Ferro AM, Olivera BM: Poly-ADP-ribosylation of DNA topoisomerase I from calf thymus. J Biol Chem 259:547–554, 1984 Kasid UN, Halligan B, Liu LF, Dritschilo A, Smulson ME: Poly (ADP-ribose)-mediated post-translational modification of chromatin-associated human topoisomerase. I. Inhibitory effects on catalytic activity. J Biol Chem 264:18687–18692, 1989 Schröder HC, Steffen R, Wenger R, Ugarkovi D, Müller WEG: Age-dependent increase of DNA topoisomerase II activity in quail oviduct: Modulation of the nuclear matrix-associated enzyme activity by protein phosphorylation and poly(ADP-ribosyl)ation. Mutation Res 219:283–294, 1989 Yoshihara K, Itaya A, Tanaka Y, Ohashi Y, Ito K, Teraoka H, Tsukada K, Matsukage A, Kamiya T: Inhibition of DNA polymerase α, DNA polymerase β, terminal deoxynucleotidyl transferase and DNA ligase II by poly(ADP-ribosyl)ation reactionin vitro. Biochem Biophys Res Comm 128:61–67, 1985 Krupitza G, Cerutti P: ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6. Biochemistry 28:2034–2040, 1989 Tanuma S, Johnson LD, Johnson GS: ADP-ribosylation of chromosomal proteins and mouse mammary tumour virus gene expression. J Biol Chem 258:15371–15375, 1983 Alvarez-Gonzalez R: 3′-Deoxy NAD as a substrate for poly (ADP-ribose) polymerase and the reaction mechanism of poly (ADP-ribose) elongation. J Biol Chem 263:17690–17696, 1988 Taniguchi T: Reaction mechanism for automodification of poly (ADP-ribose) synthetase. Biochem Biophys Res Commun 147: 1008–1012, 1987 Ménard L, Thibault L, Poirier GG: Reconstitution of anin vitro poly(ADP-ribose) turnover system. Biochim Biophys Acta 1049:45–58, 1990 Huletsky A, de Murcia G, Muller S, Hengartner M, Ménard L, Lamarre D, Poirier GG: The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. J Biol Chem 264:8878–8886, 1989 Mathis G, Althaus FR: Release of core DNA from nucleosomal core particles following (ADP-ribose)n modificationin vitro. Biochem Biophys Res Commun 143:1049–1054, 1987 Sauermann G, Wesierka-Gadek J: Poly(ADP-ribose) effectively competes with DNA for histone H4 binding. Biochem Biophys Res Commun 139:523–529, 1986 Fréchette A, Huletsky A, Aubin RJ, de Murcia G, Mandel P, Lord A, Grondin G, Poirier GG: Poly(ADP-ribosyl)ation of chromatin: Kinetics of relaxation and its effect on chromatin solubility. Can J Biochem Cell Biol 63:764–773, 1985 Huletsky A, Niedergang C, Fréchette A, Aubin R, Gaudreau A, Poirier GG: Sequentiel ADP-ribosylation pattern of nucleosomal histones. Eur J Biochem 146:277–285, 1985 Niedergang C, de Murcia G, Ittel ME, Pouyet J, Mandel P: Time course of polynucleosome relaxation and ADP-ribosylation. Eur J Biochem 146:185–191, 1985 Huletsky A: Modulation de la structure de la chromatine par la poly(ADP-ribosyl)ation). Thèse de doctorat Université de Sherbrooke, Québec, Canada, 1988 de Murcia G, Huletsky A, Lamarre D, Gaudreau A, Pouyet J, Daune M, Poirier GG: Modulation of chromatin superstructure by poly(ADP-ribose) synthesis and degradation. J Biol Chem 261:7011–7017, 1986 Cardenas-Corona ME, Jacobson EL, Jacobson MK: Endogenous-polymers of ADP-ribose are associated with the nuclear matrix. J Biol Chem 262:14863–14866, 1987 Ferro AM, Olivera BM: Poly(ADP-ribosylation)in vitro. Reaction parameters and enzyme mechanism. J Biol Chem 257:7808–7813, 1982 Ueda K, Hayaishi O: ADP-ribosylation. Annu Rev Biochem 54: 73–100, 1985 Petzold SJ, Booth BA, Leimbach GA, Berger NA: Purification and properties of poly(ADP-ribose) polymerase from lamb thymus. Biochemistry 20:7075–7081, 1981 Zahradka P, Ebisuzaki K: A shuttle mechanism for DNA-protein interactions. Eur J Biochem 127:579–585, 1982 Jacobson EL, Meadows R, Measel J: Cell cycle perturbations following DNA damage in the presence of ADP-ribosylation inhibitors. Carcinogenesis 6:711–714, 1985 Kameshita I, Yamamoto H, Fugimoto S, Shizuta Y: Antigenic determinant and interspecies cross-reactivity of a monoclonal antibody to poly(ADP-ribose) synthetase FEBS Letters 182: 393–397, 1985 Lamarre D, Talbot B, de Murcia G, Laplante C, Ledue Y, Poirier GG: Monoclonal antibodies against poly(ADP-ribose) polymerase. Epitope mapping, inhibition of activity, inter-species immunoreactivity and cellular distribution of enzyme. Biochim Biophys Acta 950:147–160, 1988 Ludwig A, Behnke B, Holtlund J, Hilz H: Immunoquantitation and size determination of intrinsic poly(ADP-ribose) polymerase from acid precipitates. An analysis of thein vivo status in mammalian species and in lower eurkaryotes. J Biol Chem 263: 6993–6999, 1988 Scovassi AI, Izzo R, Franchi E, Bertazzoni U: Structural analysis of poly(ADP-ribose) polymerase in higher and lower cucaryotes. Eur J Biochem 159:77–84, 1986 Hayaishi O, Ueda K: ADP-ribosylation reactions Biology and Medecine. Academic Press, New York, 1982, pp 1–700 Yamanaka H, Willis EH, Penning CA, Peebles CL, Tan EM, Carson DA: Human autoantibodies to poly(adenosine diphosphateribose) polymerase. J Clin Invest 80:900–904, 1987 Kameshita I, Mitsuruchi Y, Matsuda M, Shizuta Y: Biosynthesis and degradation of poly(ADP-ribose) synthetase. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 71–75 Kaufmann SH, Brunet G, Talbot B, Lamarre D, Dumas C, Shaper JH, Poirier GG: Association of poly(ADP-ribose) polymerase with nuclear matrix. The role of intermolecular disulfide bond formation, RNA retention and cell type. Exp Cell Res 192: 524–535, 1991 Adolph KW, Song MH: Cell cycle variations in ADP-ribosylation of HeLa nuclear proteins. Arch Biochem Biophys 243:427–438, 1985 Adolph KW, Song MH: Decrease in ADP-ribosylation of HeLa non-histone proteins from interphase to metaphase. Biochemistry 24:345–352, 1985 Adolph KW, Song MH: ADP-ribosylation of metaphase and interphase non histones using [3H] adenosine as a radioactive label. FEBS Letters 182:158–162, 1985 Alvarez-Gonzalez R, Ringer DP: Nuclear matrix associated poly (ADP-ribose) metabolism in regenerating rat liver. FEBS Letters 236:362–366, 1988 Wesierka-Gadek J, Sauermann G: Modification of nuclear matrix proteins by ADP-ribosylation. Association of nuclear ADP-ribosyltransferase with the nuclear matrix. Eur J Biochem 153: 421–428, 1985 Burzio LO, Saez L, Cornejo R: Poly(ADP-ribose) synthethase activity in rat testis mitochondria. Biochem Biophys Res Commun 103:369–375, 1981 Chatterjee S, Petzold SJ, Berger SJ, Berger NA: Strategy for selection of cell variants deficient in poly(ADP-ribose) polymerase. Exp Cell Res 172:245–257, 1987 Hunting DJ, Gowans BJ, Henderson JF: Specificity of inhibitors of poly(ADP-ribose) synthesis. Effects of nucleotide metabolism in cultured cells. Mol Pharmacol 28:200–206, 1985 Milam KM, Cleaver JE: Inhibitors of poly(adenosine diphosphate ribose) synthesis: Effect on other metabolic processes. Science 223:589–591, 1984 Purnell MR, Whish WJD: Novel inhibitors of poly(ADP-ribose) synthetase. Biochem J 185:775–777, 1980 Rankin PW, Jacobson EL, Benjamin RC, Moss J, Jacobson MK: Quantitative studies of inhibitors of ADP-ribosylationin vitro andin vivo. J Biol Chem 264: 4312–4317, 1989 Banasik M, Komura H, Shimoyama M, Ueda K: Specific inhibitors of poly(ADP-ribose) synthetase and mono (ADP-ribosyl) transferase. J Biol Chem 267:1569–1575, 1992 Banasik M, Komura H, Ueda K: Inhibition of poly(ADP-ribose) synthetase by unsaturated fatty acids, vitamins and vitamin-like substances. FEBS Letters 263:222–224, 1990 Hakam A, McLick J, Buki K, Kun E: Catalytic activities of synthetic octadeoxyribonucleotides as coenzymes of poly(ADP-ribose) polymerase and the identification of a new enzyme inhibitory site. FEBS Letters 212:73–78, 1987 Kupper JH, de Murcia G, Burkle A: Inhibition of poly(ADP-ribosyl)ation by overexpressing the poly(ADP-ribose) polymerase DNA-binding domain in mammalian cells. J Biol Chem 265: 18721–18724, 1990 Kameshita I, Matsuda Z, Taniguchi T, Shizuta Y: Poly(ADP-ribose) synthetase. Separation and identification of three proteolytic fragments as the substrate binding domain, the DNA binding domain and the automodification domain. J Biol Chem 259: 4770–4776, 1984 Nishikimi M, Ogasawara K, Kameshita I, Taniguchi T, Shizuta Y: Poly(ADP-ribose) synthetase. The DNA binding domain and the automodification domain. J Biol Chem 257:6102–6105, 1982 Taniguchi T, Yamauchi K, Yamamoto T, Toyoshima K, Harada N, Tanaka H, Takahashi S, Yamamoto H, Fujimoto S: Depression in gene experssion for poly(ADP-ribose) synthetase during the interferon-gamma-induced activation process of murine macrophage tumor cells. Eur J Biochem 171:571–575, 1988 Alkhatib HM, Chen D, Cherney B, Bhatia K, Notario V, Giri C, Stein G, Slattery E, Roeder RG, Smulson ME: Cloning and expression of cDNA for human poly (ADP-ribose) polymerase. Proc Natl Acad Sci (USA) 84:1224–1228, 1987 Schneider R, Auer B, Kuhne C, Herzog H, Klocker H, Burtscher HJ, Hirsch-Kauffmann M, Wintersberger U, Schweigher M: Isolation of a cDNA clone for human NAD+: Protein ADP-ribosyltransferase. Eur J Cell Biol 44:302–307, 1987 Saito I, Hatakeyama K, Kido T, Ohkubo H, Nakanishi S, Ueda K: Cloning of a full-length cDNA encoding bovine thymus poly (ADP-ribose) synthetase: Evolutionarily conserved segments and their potential functions. Gene 90:249–254, 1990 Thibodeau J, Gradwohl G, Dumas C, Clairoux-Moreau S, Brunet G, Penning C, Poirier GG, Moreau P: Cloning of rodent cDNA encoding the poly(ADP-ribose) polymerase catalytic domain and analysis of mRNA levels during the cell cycle. Biochem Cell Biol 67:653–660, 1989 Huppi K, Bhatia K, Siwarski D, Klinman D, Cherney B, Smulson ME: Sequence and organization of the mouse poly(ADP-ribose) polymerase gene. Nucl Acid Res 17:3387–3401, 1989 Ittel ME, Garnier JM, Jeltsh JM, Niedergang C: Chicken poly (ADP-ribose)synthetase: Complete deduced amino acid sequence and comparison with mammalian enzyme sequences. Gene 102:157–164, 1991 Brawerman G: Determinants of messenger RNA stability. Cell 48:5–6, 1987 Shaw G, Kamen R: A conserved AV sequence from 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:649–667, 1986 Kozak M: Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev 47:1–40, 1983 Mazen A, Ménissier-de Murcia J, Molinete M, Simonin F, Gradwohl G, Poirier GG, de Murcia G: Poly(ADP-ribose) polymerase: A novel finger protein. Nucl Acid Res 17:4689–4698, 1989 Lamarre D, Talbot B, Leduc Y, Muller S, Poirier GG: Production and characterization of monoclonal antibodies specific for the functional domains of poly(ADP-ribose) polymerase. Biochem Cell Biol 64:368–376, 1986 Zahradka P, Ebisuzaki K: Poly(ADP-ribose) polymerase is a zine metalloenzyme. Eur J Biochem 142:503–509, 1984 Uchida K, Morita T, Sato T, Ogura T, Yamashita R, Noguchi S, Suzuki H, Nyunoya H, Miwa M, Sugimura T: Nucleotide sequence of a full-length cDNA for human fibroblast poly(ADP-ribose) polymerase. Biochem Biophys Res Commun 148:617–622, 1987 Miller J, McLachlan AD, Klug A: Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4:1609–1614, 1985 Berg JM: Zinc fingers and other metal-binding domains. Elments for interaction between macromolecules. J Biol Chem 265:6513–6516, 1990 Brown RS, Sander C, Argos P: The primary structure of transcription factor TFIIIA has 12 consecutive repeats. FEBS Letters 186:271–274, 1985 Johnson PF, McKnight SL: Eukaryotic transcriptional regulatory proteins. Ann Rev Biochem 58:799–839, 1989 Gradwohl G, Ménissier-de Murcia J, Molinete M, Simonin F, de Murcia G: Expression of functional zinc finger domain of human poly(ADP-ribose) polymerase in E. coli. Nucl Acad Res 17:7112, 1989 Ménissier-de Murcia J, Molinete M, Gradwohl G, Simonin F, de Murcia G: Zine binding domain of poly(ADP-ribose) polymerase participates in the recognition of single strand breaks on DNA. J Mol Biol 210:229–234, 1989 Gradwohl G, Mazen A, De Murcia G: Poly(ADP-ribose) polymerase froms loops with DNA. Biochem Biophys Res Commun 148:913–919, 1987 Gradwohl G, Mazen A, Poirier GG, De Murcia G: Les réactions de poly(ADP-ribosyl)ation. Regard sur la biochimie 2:19–26, 1988 Ittel ME, Jeltsch JM, Niedergang C: Sequence analysis of the DNA associated to poly(ADP-ribose) molecules. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 505–510 Kalderon D, Richardson WD, Markham AF, Smith AE: Sequence requirements for nuclear location of Simian virus 40 large-T antigen. Nature 311:33–38, 1984 Schreiber V, Molinete M, Boeuf M, de Murcia G, Ménissier-de Murcia J: The human poly(ADP-ribose) polymerase nuclear localization signal is a bipartite element functionally separate from DNA binding and catalytic activity. EMBO J 11:3263–3269, 1992 Molinete M, Schreiber V, Simonin F, Gradwohl G, Ménissier-de Murcia J, de Murcia G: Structure and function of the human poly (ADP-ribose) polymerase. In: GG Poirier, P Moreau (eds.) ADP-ribosylation Reactions. Springer-Verlag, New York, 1992, pp 3–14 Kawaichi M, Ueda K, Hayaishi O: Multiple autopoly(ADP-ribosyl)ation of rat liver poly(ADP-ribose) synthetase. Mode of modification and properties of automodified synthetase. J Biol Chem 256:9483–9489, 1981 Walker EJ, Saraste M, Runswick MJ, Gay NJ: Distantly related sequences in the a-and b-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951, 1982 Herzog H, Zabel BU, Schneider R, Auer B, Hirsch-Kauffmann M, Schweiger M: Human nuclear NAD+ ADP-ribosyltransferase: Localization of the gene on chromosome 1q41-q42 and expression of an active human enzyme in Escherichia coli. Proc Natl Acad Sci USA 86:3514–3518, 1989 Thibodeau J, Simonin F, Favazza M, Gradwohl G, Poirier GG, de Murcia G: Experession in E. coli of the catalytic domain of rat poly(ADP-ribose) polymerase. FEBS Letters 264:81–83, 1990 Yamanaka H, Willis EH, Carson DA: Human antibodies to poly (adenosine diphosphate-ribose) polymerase recognize cross-reactive epitopes associated with the catalytic site of the enzyme. J Clin Invest 83:180–186, 1989 Buki KG, Kun E: Polypeptide domains of ADP-ribosyltransferase obtained by digestion with plasmin. Biochemistry 27:5990–5995, 1988 Sastry SS, Buki KG, Kun E: Binding of adenosine diphosphoribosyltransferase to the termini and internal regions of linear DNAs. Biochemistry 28:5670–5680, 1989 Brennan RG, Matthews BW: The helix-turn-helix DNA binding motif. J Biol Chem 264:1903–1906, 1989 Auer B, Nagl U, Herzog H, Schneider R, Schweiger M: Human nuclear NAD+ ADP-ribosyltransferase (polymerizing): Organization of the gene. DNA 8:575–580, 1989 Ogura T, Nyunoya H, Takahashi-Masutani M, Miwa M, Sugimura T, Esumi H: Characterization of a putative promoter region of the human poly(ADP-ribose) polymerase gene: Structural similarity to that of the DNA polymerase β gene. Biochem Biophys Res Commun 167:701–710, 1990 Pugh BF, Tijan R: Mechanism of transcriptional activation by SP1: Evidence for coactivators., Cell 61:1187–1197, 1990 Yokoyama Y, Kawamoto T, Mitsuuchi Y, Kurosaki T, Toda K, Ushiro H, Terashima M, Suminoto H, Kuribayashi I, Yamamoto Y, Maeda T, Ikeda H, Sagara Y, Shizuta Y: Human poly(ADP-ribose) polymerase gene. Cloning of the promoter region. Eur J Biochem 194:521–526, 1990 Carson DA, Seto S, Wasson DB: Lymphocyte dysfunction after DNA damage by toxic oxygen species. A model of immunodeficiency. J Exp Med 163:746–751, 1986 Bhatia K, Pommier Y, Giri C, Fornace AJ, Imaizumi M, Breitman TR, Cherney BW, Smulson ME: Expression of the poly (ADP-ribose) polymerase gene following natural and induced DNA strand breakage and effect of hyperexpression of DNA repair. Carcinogenesis 11:123–128, 1990 Ruby SW, Szostak JW: Specific Saccharomyces cerevisiae genes are expressed in response to DNA damaging agents. Mol Cell Biol 5:75–84, 1985 Fornace AJ, Zmudka B, Hollander MC, Wilson SH: Induction of ßpolymerase mRNA by DNA damaging agents in Chinese hamster ovary cells. Mol Cell Biol 9:851–853, 1989 Leduc Y, Lawrence JJ, de Murcia G, Poirier GG: Cell cycle regulation of poly(ADP-ribose) synthetase in FR3T3 cells. Biochim Biophys Acta 968:275–282, 1988 McNerney R, Tavassoli M, Shall S, Brazinski A, Johnstone A: Changes in mRNA levels of poly(ADP-ribose) polymerase during activation of human lymphocytes. Biochim Biophys Acta 1009:185–187, 1989 Menegazzi M, Gelosa F, Tommasi M, Uchida K, Miwa M, Sugimura T, Suzuki H: Induction of poly(ADP-ribose) polymerase gene expression in lectin-stimulated human T lymphocytes is dependent on protein synthesis. Biochem Biophys Res Commun 156:995–999, 1988 Bhatia K, Kang VH, Stein GS, Bustin M, Cherney BW, Notario V, Haque SJ, Huppi M, Smulson ME: Cell cycle regulation of an exogenous human poly(ADP-ribose) polymerase cDNA introduced into murine cells. J Cell Physiol 144:345–353, 1990 Smulson M, Alkhatib H, Bhatia K, Chen D, Cherney B, Notario V, Tahourdin C, Dritschilo A, Hensley P, Breitman T, Stein G, Pommier Y, McBride W, Bustin M, Giri, C: The cloning of the cDNA and gene for human poly(ADP-ribose) polymerase: Status on the biological function(s) using recombinant probes. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions. Mechanisms and Biological Significance. Springer Verlag, New York, 1989, pp 463–477 Jacobson MK, Levi V, Juares-Salinas H, Barton RA, Jacobson EL: Effect of carcinogenic N-alkyl-N-nitroso compounds on nicotinamide adenine dinucleotide metabolism. Cancer Res 40: 1797–1802, 1980 Skidmore CJ, Davies MI, Goodwin PM, Halldorsson H, Lewis PJ, Shall S, Zia'ce A: The involvement of poly(ADP-ribose) polymerase in the degradation of NAD caused by gamma-radiation and N-methyl-N-nitrosourea. Eur J Biochem 101:135–142, 1979 Miller EG: Effect of deoxyribonuclease I on the number and length of chains of poly(ADP-ribose) synthesizedin vitro. Biochem Biophys Res Commun 66:280–286, 1975 Benjamin RC, Gill DM: Poly(ADP-ribose) synthesisin vitro programmed by damaged DNA: A comparison of DNA molecules containing different types of strand breaks. J Biol Chem 255:10502–10508, 1980 Cohen JJ, Berger NA: Activation of poly(ADP-ribose) polymerase with irradiated and UV endonuclease treated SV 40 minichromosome. Biochem Biophys Res Commun 98:268–274, 1981 Cohen JJ, Catino DM, Petzold SJ, Berger NA: Activation of poly (ADP-ribose) polymerase by SV 40 minichromosomes: Effects of deoxyribonucleic acid damage and histone H1. Biochemistry 21:4931–4940, 1982 Smulson ME, Schein P, Mullins DW, Sudhakar S: A putative role for nicotinamide adenine dinucleotide-promoted nuclear protein modification in the antitumor activity of N-methyl-N-nitrosourea. Cancer Res 37:3006–3012, 1977 Berger NA, Sikorski GW: Poly(adenosine diphosphoribose) synthesis in ultraviolet-irradiated xeroderma pigmentosum cells reconstituted with micrococcus luteus UV endonuclease. Biochemistry 20:3610–3614, 1981 Tanaka K, Sekiguchi M, Okada Y: Restoration of ultraviolet-in-duced unscheduled DNA synthesis of xeroderma pigmentosum cells by the concomitant treatment with bacteriophage T4 endonuclease V and HVJ (Sendai virus). Proc Natl Acad Sci (USA) 72:4071–4075, 1975 Shall S: ADP-ribose in DNA repair: A new component of DNA excision repair. Adv Radiat Biol II:1–69, 1984 Mathis G, Althaus FR: Uncoupling of DNA excision repair and nucleosomal unfolding in poly(ADP-ribose)-depleted mammalian cells. Carcinogenesis 11:1237–1239, 1999 Satoh MS, Lindahl T: Role of poly(ADP-ribose) formation in DNA repair. Nature 356:356–358, 1992 Satoh MS, Poirier GG, Lindahl T: NAD+-dependent repair of damaged DNA by human cell extracts. J Biol Chem 268:5480–5587, 1993 Creissen D, Shall S: Regulation of DNA ligase activity by poly (ADP-ribose). Nature (London) 296:271–272, 1982 Creissen D, Shall S: DNA ligase II of mammalian cells. In: FR Althaus, H Hilz, S Shall (eds.) ADP-ribosylation of Proteins. Springer Verlag, Heidelberg, Berlin, New York, 1985, pp 284–287 Cleaver JE, Milam KM, Morgan WF: Do inhibitor studies demonstrate a role for poly(ADP-ribose) in DNA repair? Radiat Res 101:16–28, 1985 Morgan WF, Cleaver JE, Shadley JD, Wiencke JK, Wolff S: The cytogenetic effects of an inhibition of poly(ADP-ribose) polymerase. In: MK Jacobson, EL Jacobson (eds.) ADP-ribose Transfer Reactions: Mechanisms and Biological Significance. Springer-Verlag, New York, 1989, pp 235–241 Wieckens K, George E, Pless T, Hilz H: Stimulation of poly (ADP-ribosyl)ation during Ehrlich Ascites tumor cell starvation and suppression of concomitant DNA fragmentation. J Biol Chem 258:4098–4104, 1983 Nomura H, Kitamura A, Tanigawa Y, Tsuchiya M, Ueki M, Sugimoto O, Shimoyama M: Possible participation of Ca++, Mg++-dependent endonuclease in liver DNA fragmentation after N-methyl-N-nitrosourea treatment. Biochim Biophys Acta 781:112–122, 1984 Tanaka Y, Yoshihara K, Itaya A, Kamiya T, Koide SS: Mechanism of the inhibition of Ca++, Mg++-dependent endonuclease of bull seminal plasma induced by ADP-ribosylation. J Biol Chem 259:6579–6585, 1984 Yoshihara K, Tanigawa Y, Burzio L, Koide SS: Evidence for adenosine diphosphate ribosylation of Ca+, Mg+-dependent endonuclease. Proc Natl Acad Sci (USA) 72:289–293, 1975 Sims JL, Berger SJ, Berger NA: Poly(ADP-ribose) polymerase inhibitors preserve nicotinamide adenine dinucleotide and adenosine 5′-triphosphate pools in DNA-damaged cells: Mechanism of stimulation of unscheduled DNA synthesis. Biochemistry 22:5188–5194, 1983 Stark GR, Wahl GM: Gene amplification. Ann Rev Biochem 53: 447–491, 1984 Tyler-Smith C, Alderson T: Gene amplification in methotrexateresistant mouse cells. I. DNA rearrangement accompanies dihydrofolate reductase gene amplification in a T-cell lymphoma. J Mol Biol 153:203–218, 1981 Bürkle A: Inhibition of carcinogen-inducible DNA amplification in a simian virus 40 transformed hamster cell line by ethacridine or ethanol. Cancer Res 49:2854–2857, 1989 Bürkle A, Meyer T, Hilz H, Zur Hausen H: Enhancement of Nmethyl-nitro-N-nitrosoguanidine — induced DNA amplification in a Simian virus 40 — transformed Chinese Hamster cell line by 3-aminobenzamide. Cancer Res 47:3632–3636, 1987 Lambert ME, Pelligrini S, Gattoni-Celli S, Weinstein IB: Carcinogen induced asynchronous replication of polyoma DNA is mediated by a trans-acting factor. Carcinogenesis 7:1011–1017, 1986 Hough CJ, Smulson ME: Association of poly(adenosine diphosphate ribosylated) nucleosomes with transcriptionally active and inactive regions of chromatin. Biochemistry 23:5016–5023, 1984 Fakan S, Leduc Y, Lamarre D, Brunet G, Poirier GG: Immunoelectron microscopical distribution of poly(ADP-ribose) polymerase in the mammalian cell nucleus. Exp Cell Res 179:517–526, 1988 Muller WEG, Zahn RW: Poly ADP-ribosylation of DNA-dependent RNA polymerase I from quail oviduct. Dependence on progesterone stimulation. Mol Cell Biochem 12:147–159, 1976 Jacob ST: Transcription of eukaryotic ribosomal RNA gene. Mol Cell Biochem 70:11–20, 1986 Kurl RN, Jacob ST: Characterization of a factor that can prevent random transcription of cloned cDNA and its probable relationship to poly(ADP-ribose) polymerase. Nucl Acid Res 13:89–101, 1985 Slattery E, Dignam JD, Matsui T, Roeder RG: Purification and analysis of a factor which suppresses nick-induced transcription by RNA polymerase II and its identity with poly(ADP-ribose) polymerase. J Biol Chem 258:5955–5959, 1983 Ohtsuki M, Sekimizu K, Agemori M, Shizuta Y, Natori S: Effect of the DNA-binding domain of poly(ADP-ribose) synthetase on accurate transcription initiation in HeLa cell lysate. FEBS Letters 168:275–277, 1984 Reeves R: Transcriptionally active chromatin. Biochim Biophys Acta 782:343–393, 1984 Sastry SS, Kun E: The interaction of adenosine diphosphoribosyl transferase (ADPRT) with a cruciform DNA. Biochem Biophys Res Comm 167:842–847, 1990 Koo HS, Wuek HM, Crothers DM: DNA bending at adenine thymine tracts. Nature 320:501–506, 1986 Bossi L, Smith DM: Conformational change in the DNA associated with an usual promoter mutation in a tRNA operon of salmonella. Cell 39:643–652, 1984 Struhl K: Molecular mechanisms of transcriptional regulation in yeast. Ann Rev Biochem 58:1051–1077, 1989 Zahn K, Blattner FR: Direct evidence for DNA bending at the lambda replication origin. Science 236:416–422, 1987 Lillie JW, Green MR: Transcription activation by the adenovirus Ela protein. Nature 338:39–44, 1989 Herendeen DR, Kassavetis GA, Barry J, Alberts BM, Geiduschek EP: Enhancement of bacteriophage T4 late transcription by components of the T4 DNA replication apparatus. Science 245:952–958, 1989 Taniguchi T, Takahashi S, Yamamoto H, Fujimoto S, Okoyama H: Requirement of down-regulation of NAD+ ADP-ribosyltransferase for the interferon-γ-induced activation process of murine macrophage tumor cells. Eur J Biochem 195:557–562, 1991 Yamagoe S, Kohda T, Oishi M: Poly(ADP-ribose) polymerase inhibitors suppress UV-induced human immunodeficiency virus type 1 gene expression at the posttranscriptional level. Mol Cell Biol 11:3522–3527, 1991 Althaus FR, Lawrence SD, He YZ, Sattler GL, Tsukada Y, Pitot HC: Effects of altered (ADP-ribose)n metabolism on expression of fetal functions by adult hepatocytes. Nature 300:366–368, 1982 Caplan AI: Poly(ADP-ribose) synthetase and cell differentiation. In: FR Althaus, H Hilz, S Shall (eds.) ADP-ribosylation of Proteins. Springer Verlag, Berlin, Heidelberg, New York, 1985, pp 388–396 Ebisuzaki K, Casley WL, Griffiths A, Wheaton L: Temporal mapping of the differentiation pathway of the murine erythroleukemia cell. Cancer Res 51:1668–1673, 1991 Taniguchi T, Morisawa K, Ogawa M, Yamamoto H, Fugimoto S: Decrease in the level of poly(ADP-ribose) synthetase during nerve growth factor-promoted nevrite outgrowth in rat phenochromocytoma PC12 cells. Biochem Biophys Res Commun 154: 1034–1040, 1988 Nakayasu M, Shima H, Aonuma S, Nakagama H, Nagao M, Sugimura T: Deletion of transfected oncogenes from NIH 3T3 transformants by inhibitors of poly(ADP-ribose) polymerase. Proc Natl Acad Sci (USA) 85:9066–9070, 1988 Milo GE, Kurian P, Kirsten E, Kun E: Inhibition of carcinogen induced cellular transformation of human fibroblasts by drugs that interact with the poly(ADP-ribose) polymerase system. FEBS Letters 179:332–336, 1985 Tseng A, Lee WMF, Kirsten E, Hakam A, McLick J, Buki K, Kun E: Prevention of tumorigenesis of oncogene transformed rat fibroblasts with DNA site inhibitors of poly(ADP-ribose) polymerase. Proc Natl Acad Sci (USA) 84:1107–1111, 1987 Kun E, Kirsten E, Milo GE, Kurian P, Kumari HL: Cell-cycle dependent intervention by benzamide of carcinogen-induced neoplastic transformation andin vitro poly(ADP-ribosyl)ation of nuclear proteins in human fibroblasts. Proc Natl Acad Sci (USA) 80:7219–7223, 1983 Borek C, Morgan WF, Ong A, Cleaver JE: Inhibition of malignant transformationin vitro by inhibitors of poly(ADP-ribose) synthesis. Proc Natl Acad Sci (USA) 81:243–247, 1984 Borek C, Cleaver JE: Antagonistic action of a tumor promotion and a poly (adenosine diphosphoribose) synthesis inhibitor in radiation-induced transformationin vitro. Biochem Biophys Res Commun 134:1334–1341, 1986 Wasserman K, Newman RA, Mclaughlin JD, Sacks PG, Zwelling LA: A possible role for altered poly(adenosine diphosphoribose) synthesis in the sensitivity of human head and neck squamous carcinoma cells to ionizing radiation. Biochem Biophys Res Commun 154:1041–1046, 1988 Weitzman SG, Weitberg AB, Clark EP, Stossel TP: Phagocytes as carcinogens: Malignant transformation produced by human neutrophils. Science 227:1231–1233, 1985 Tanuma S, Kanai Y: Poly(ADP-ribosyl)ation of chromosomal proteins in the HeLa S3 cell cycle. J Biol Chem 257:6565–6570, 1982 Boorstein RJ, Pardee AB: Factors modifying 3-aminobenzamide cytotoxicity in normal and repair-deficient human fibroblasts. J Cell Physiol 120:335–344, 1984 Boorstein RJ, Pardee AB: 3-Aminobenzamide is lethal to MMS-damaged human fibroblasts primarily during G-phase. J Cell Physiol 120:345–353, 1984 Ittel ME, Jongstra-Bilen J, Rochette-Egly C, Mandel P: Involvement of poly(ADP-ribose) polymerase in the initiation of phytohemagglutinin induced human lymphocyte proliferation. Biochem Biophys Res Commun 166:428–432, 1983 Dai Y, Yu Y, Chen X: The cell-cycle dependent and the DNA-damaging agent-induced changes of cellular NAD content and their significance. Mutation Res 191:29–35, 1987 Romano F, Menapack L, Ubaldo I: Inhibitors of ADP-ribosyl transferase suppress the mitogenic actions execred by tumor promoters, but not those evoked by peptide mitogens in primary neonatal rat hepatocytes. Carcinogenesis 9:2147–2151, 1988 Cantoni O, Cattabeni F, Stocchi V, Meyn RE, Cerutti P, Murray D: Hydrogen peroxide insult in cultured mammalian cells: Relationships between DNA single-strand breakage, poly(ADP-ribose) metabolisms and cell killing. Biochim Biophys Acta 1014: 1–7, 1989 Boulikas T, Bastin B, Boulikas P, Dupuis G: Increase in histone poly(ADP-ribosylation) in mitogen-activated lymphoïd cells. Exp Cell Res 187:77–86, 1990 Burzio L, Koide SS: A functional role of poly(ADP-R) in DNA synthesis. Biochem Biophys Res Commun 40:1013–1020, 1970 Savard P, Aubin R, Whish WJD, Lord A, Poirier GG: Poly(adenosine diphosphoribose) polymerase activity and adenosine diphosphate ribosylation of proteins during pancreatic degeneration and regeneration. Cancer Res 41:1417–1421, 1981 Menegazzi M, Carcereri de Prati A, Ledda-Columbano GM, Columbano A, Uchida K, Miwa M, Suzuki H: Regulation of poly (ADP-ribose) polymerase mRNA levels during compensatory and mitogen-induced growth of rat liver. Arch Biochem Biophys 279:232–236, 1990 De Murcia G, Jonstra-Bilen J, Ittel M, Mandel P, Delain E: Poly (ADP-ribose) polymerase automodification and interaction with DNA: Electron microscopic visualisation. EMBO J 2:543–548, 1983 Baksi K, Alkhatib H, Smulson ME:In vivo characterization of the poly(ADP-ribosyl)ation of SV 40 chromatin and large T antigen by immunofractionation. Exp Cell Res 172:110–123, 1987 Eki T, Hurwitz J: Influence of poly(ADP-ribose) polymerase on the enzymatic synthesis of SV 40 DNA. J Biol Chem 266:3087–3100, 1991 Lee SH, Kwong AD, Tshimi Y, Hurwitz J: Studies on the DNA elongation inhibitor and its proliferating cell nuclear antigen-dependant control in Simian virus 40 DNA replicationin vitro. Proc Natl Acad Sci USA 86:4877–4881, 1989 Lönn U, Lönn S: Accumulation of 10-kilobase DNA replication intermediates in cells treated with 3-aminobenzamide. Proc Natl Acad Sci (USA) 82:104–108, 1985 Poirier GG, de Murcia G, Niedergang C, Jongstra-Bilen J, Mandel P: Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of the chromatin structure. Proc Natl Acad Sci 79:3423–3427, 1982 Nobori T, Yamanaka H, Carson DA: Poly(ADP-ribose) polymerase inhibits DNA synthesis initiation in the absence of NAD+. Biochem Biophys Res Comm 163:1113–1118, 1989 Anachkova B, Russev G, Poirier GG: DNA replication and poly (ADP-ribosy)ation of chromatin. Cytobios 58:19–28, 1989 Loetscher P, Alvarez-Gonzalez R, Althaus FR: Poly ADPR may signal changing metabolic conditions to the chromatin of mammalian cells. Proc Natl Acad Sci (USA) 84:1286–1289, 1987