Skip to main content
Log in

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

  • Review
  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

In the past five years, poly(ADP-ribosyl)ation has developed greatly with the help of molecular biology and the improvement of biochemical techniques. In this article, we describe the physico-chemical properties of the enzymes responsible for the synthesis and degradation of poly(ADP-ribose), respectively poly(ADP-ribose) polymerase and poly(ADP-ribose) glycohydrolase. We then discuss the possible roles of this polymer in DNA repair and replication as well as in cellular differentiation and transformation. Finally, we put forward various hypotheses in order to better define the function of this polymer found only in eucaryotes. (Mol Cell Biochem122: 171–193, 1993)

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

3-AB:

3-Aminobenzamide

3-MBA:

3-Methoxybenzamide

AADH:

Amino Acid Dehydrogenase

CAT:

Chloramphenicol Acetyl Transferase

DHFR:

Dihydrofolate Reductase

DMS:

Dimethylsulfate

DMSO:

Dimethylsulfoxide

DNase:

Deoxyribonuclease

HMG:

High Mobility Group

kb:

Kilobase

kDa:

Kilodalton

LMG:

Low Mobility Group

MNNG:

Methylnitroso Nitroguanidine

MNU:

Methylnitrosourea

NAD:

Nicotinamide Adenine Dinucleotide

NLS:

Nuclear Localization System

NTP:

Nucleotide Triphosphate

pADPR:

Poly (ADP-ribose)

PARP:

Poly(ADP-ribose) Polymerase

PHA:

Phytohemaglutinin

PMA:

Phorbol Myristate Acetate

PRAMP:

Phosphoribosyl AMP

(PR)2AMP:

Diphosphoribosyl AMP

RNase:

Ribonuclease

SCE:

Sister Chromatid Exchange

TPA:

Tetradecanoyl Phorbol-13-Acetate

UV:

Ultra-Violet

References

  1. 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

    Google Scholar 

  2. de Murcia G, Huletsky A, Poirier GG: Review: Modulation of chromatin structure by poly(ADP-ribosyl)ation. Biochem Cell Biol 66:626–635, 1988

    Google Scholar 

  3. Boulikas T: Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation) (Review). Anticancer Res 11: 489–528, 1991

    Google Scholar 

  4. 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

    Google Scholar 

  5. 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

    Google Scholar 

  6. 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

    Google Scholar 

  7. 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

    Google Scholar 

  8. 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

    Google Scholar 

  9. 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

    Google Scholar 

  10. 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

    Google Scholar 

  11. 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

    Google Scholar 

  12. 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

    Google Scholar 

  13. 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

    Google Scholar 

  14. 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

    Google Scholar 

  15. Minaga T, Kun E: Probable helical conformation of poly(ADP-ribose). J Biol Chem 258:5726–5730, 1983

    Google Scholar 

  16. Minaga T, Kun E: Spectral analysis of the conformation of poly (adenosine diphosphoribose). J Biol Chem 258:725–730, 1983

    Google Scholar 

  17. 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

    Google Scholar 

  18. 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

    Google Scholar 

  19. Alvarez-Gonzalez R, Jacobson MK: Characterization of polymer of ADP-ribose generatedin vitro andin vivo. Biochemistry 26:3218–3224, 1987

    Google Scholar 

  20. 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

    Google Scholar 

  21. 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

    Google Scholar 

  22. 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

    Google Scholar 

  23. 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

    Google Scholar 

  24. Juarez-Salinas H, Levi V, Jacobson EL, Jacobson MK: Poly (ADP-ribose) has a branched structurein vivo. J Biol Chem 257: 607–609, 1982

    Google Scholar 

  25. 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

    Google Scholar 

  26. 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

    Google Scholar 

  27. 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

    Google Scholar 

  28. Alvarez-Gonzalez R, Althaus FR: Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA damaging agents. Mutation Res 218:67–74, 1989

    Google Scholar 

  29. Berger NA: Poly(ADP-ribose) in the cellular response to DNA damage. Radiat Res 101:4–15, 1985

    Google Scholar 

  30. Jonsson GG, Jacobson EL, Jacobson MK: The effect of hyperthermia on poly(ADP-ribose) metabolism. Cancer Res 48: 4233–4239, 1988

    Google Scholar 

  31. Ueda K, Okayama H, Fukushima M, Hayaishi O: Purification and analysis of the poly(ADP-ribose) synthetase system. J Biochem 77:1–11, 1975

    Google Scholar 

  32. 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

    Google Scholar 

  33. 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

    Google Scholar 

  34. Ueda K, Kawaichi M, Okayama H, Hayaishi O: Poly(ADP-ribosyl)ation of nuclear proteins. J Biol Chem 254:679–687, 1979

    Google Scholar 

  35. 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

    Google Scholar 

  36. 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

    Google Scholar 

  37. Naegeli H, Althaus FR: Regulation of poly(ADP-ribose) polymerase. Histone-specific adaptations of reaction products. J Biol Chem 266:10596–10601, 1991

    Google Scholar 

  38. 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

    Google Scholar 

  39. 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

    Google Scholar 

  40. 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

    Google Scholar 

  41. Ikejima M, Gill DM: Poly(ADP-ribose) degradation by glycohydrolase starts with an endonucleotytic incision. J Biol Chem 263:11037–11040, 1988

    Google Scholar 

  42. 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

    Google Scholar 

  43. 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

    Google Scholar 

  44. 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

    Google Scholar 

  45. Tanuma S, Endo H: Purification and characterization of an (ADP-ribose)n glycohydrolase from human erythrocytes. Eur J Biochem 191:57–63, 1990

    Google Scholar 

  46. 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

    Google Scholar 

  47. 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

    Google Scholar 

  48. Futai M, Mizuno D: A new phosphodiesterase forming nucleoside 5′-monophosphate from rat liver. J Biol Chem 242:5301–5307, 1967

    Google Scholar 

  49. 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

    Google Scholar 

  50. 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

    Google Scholar 

  51. Adamietz P, Rudolph A: ADP-ribosylation of nuclear proteinsin vivo. J Biol Chem 259:6841–6846, 1984

    Google Scholar 

  52. 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

    Google Scholar 

  53. 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

    Google Scholar 

  54. 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

    Google Scholar 

  55. 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

    Google Scholar 

  56. 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

    Google Scholar 

  57. 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

    Google Scholar 

  58. Ferro AM, Olivera BM: Poly-ADP-ribosylation of DNA topoisomerase I from calf thymus. J Biol Chem 259:547–554, 1984

    Google Scholar 

  59. 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

    Google Scholar 

  60. 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

    Google Scholar 

  61. 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

    Google Scholar 

  62. Krupitza G, Cerutti P: ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6. Biochemistry 28:2034–2040, 1989

    Google Scholar 

  63. 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

    Google Scholar 

  64. 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

    Google Scholar 

  65. Taniguchi T: Reaction mechanism for automodification of poly (ADP-ribose) synthetase. Biochem Biophys Res Commun 147: 1008–1012, 1987

    Google Scholar 

  66. Ménard L, Thibault L, Poirier GG: Reconstitution of anin vitro poly(ADP-ribose) turnover system. Biochim Biophys Acta 1049:45–58, 1990

    Google Scholar 

  67. 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

    Google Scholar 

  68. 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

    Google Scholar 

  69. Sauermann G, Wesierka-Gadek J: Poly(ADP-ribose) effectively competes with DNA for histone H4 binding. Biochem Biophys Res Commun 139:523–529, 1986

    Google Scholar 

  70. 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

    Google Scholar 

  71. 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

    Google Scholar 

  72. 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

    Google Scholar 

  73. Huletsky A: Modulation de la structure de la chromatine par la poly(ADP-ribosyl)ation). Thèse de doctorat Université de Sherbrooke, Québec, Canada, 1988

    Google Scholar 

  74. 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

    Google Scholar 

  75. 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

    Google Scholar 

  76. Ferro AM, Olivera BM: Poly(ADP-ribosylation)in vitro. Reaction parameters and enzyme mechanism. J Biol Chem 257:7808–7813, 1982

    Google Scholar 

  77. Ueda K, Hayaishi O: ADP-ribosylation. Annu Rev Biochem 54: 73–100, 1985

    Google Scholar 

  78. Petzold SJ, Booth BA, Leimbach GA, Berger NA: Purification and properties of poly(ADP-ribose) polymerase from lamb thymus. Biochemistry 20:7075–7081, 1981

    Google Scholar 

  79. Zahradka P, Ebisuzaki K: A shuttle mechanism for DNA-protein interactions. Eur J Biochem 127:579–585, 1982

    Google Scholar 

  80. Jacobson EL, Meadows R, Measel J: Cell cycle perturbations following DNA damage in the presence of ADP-ribosylation inhibitors. Carcinogenesis 6:711–714, 1985

    Google Scholar 

  81. 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

    Google Scholar 

  82. 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

    Google Scholar 

  83. 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

    Google Scholar 

  84. 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

    Google Scholar 

  85. Hayaishi O, Ueda K: ADP-ribosylation reactions Biology and Medecine. Academic Press, New York, 1982, pp 1–700

    Google Scholar 

  86. 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

    Google Scholar 

  87. 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

    Google Scholar 

  88. 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

    Google Scholar 

  89. Adolph KW, Song MH: Cell cycle variations in ADP-ribosylation of HeLa nuclear proteins. Arch Biochem Biophys 243:427–438, 1985

    Google Scholar 

  90. Adolph KW, Song MH: Decrease in ADP-ribosylation of HeLa non-histone proteins from interphase to metaphase. Biochemistry 24:345–352, 1985

    Google Scholar 

  91. 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

    Google Scholar 

  92. Alvarez-Gonzalez R, Ringer DP: Nuclear matrix associated poly (ADP-ribose) metabolism in regenerating rat liver. FEBS Letters 236:362–366, 1988

    Google Scholar 

  93. 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

    Google Scholar 

  94. Burzio LO, Saez L, Cornejo R: Poly(ADP-ribose) synthethase activity in rat testis mitochondria. Biochem Biophys Res Commun 103:369–375, 1981

    Google Scholar 

  95. 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

    Google Scholar 

  96. 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

    Google Scholar 

  97. Milam KM, Cleaver JE: Inhibitors of poly(adenosine diphosphate ribose) synthesis: Effect on other metabolic processes. Science 223:589–591, 1984

    Google Scholar 

  98. Purnell MR, Whish WJD: Novel inhibitors of poly(ADP-ribose) synthetase. Biochem J 185:775–777, 1980

    Google Scholar 

  99. 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

    Google Scholar 

  100. 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

    Google Scholar 

  101. 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

    Google Scholar 

  102. 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

    Google Scholar 

  103. 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

    Google Scholar 

  104. 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

    Google Scholar 

  105. 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

    Google Scholar 

  106. 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

    Google Scholar 

  107. 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

    Google Scholar 

  108. 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

    Google Scholar 

  109. 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

    Google Scholar 

  110. 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

    Google Scholar 

  111. 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

    Google Scholar 

  112. 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

    Google Scholar 

  113. Brawerman G: Determinants of messenger RNA stability. Cell 48:5–6, 1987

    Google Scholar 

  114. 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

    Google Scholar 

  115. Kozak M: Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev 47:1–40, 1983

    Google Scholar 

  116. 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

    Google Scholar 

  117. 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

    Google Scholar 

  118. Zahradka P, Ebisuzaki K: Poly(ADP-ribose) polymerase is a zine metalloenzyme. Eur J Biochem 142:503–509, 1984

    Google Scholar 

  119. 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

    Google Scholar 

  120. 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

    Google Scholar 

  121. Berg JM: Zinc fingers and other metal-binding domains. Elments for interaction between macromolecules. J Biol Chem 265:6513–6516, 1990

    Google Scholar 

  122. Brown RS, Sander C, Argos P: The primary structure of transcription factor TFIIIA has 12 consecutive repeats. FEBS Letters 186:271–274, 1985

    Google Scholar 

  123. Johnson PF, McKnight SL: Eukaryotic transcriptional regulatory proteins. Ann Rev Biochem 58:799–839, 1989

    Google Scholar 

  124. 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

    Google Scholar 

  125. 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

    Google Scholar 

  126. Gradwohl G, Mazen A, De Murcia G: Poly(ADP-ribose) polymerase froms loops with DNA. Biochem Biophys Res Commun 148:913–919, 1987

    Google Scholar 

  127. Gradwohl G, Mazen A, Poirier GG, De Murcia G: Les réactions de poly(ADP-ribosyl)ation. Regard sur la biochimie 2:19–26, 1988

    Google Scholar 

  128. 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

    Google Scholar 

  129. 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

    Google Scholar 

  130. 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

    Google Scholar 

  131. 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

    Google Scholar 

  132. 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

    Google Scholar 

  133. 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

    Google Scholar 

  134. 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

    Google Scholar 

  135. 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

    Google Scholar 

  136. 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

    Google Scholar 

  137. Buki KG, Kun E: Polypeptide domains of ADP-ribosyltransferase obtained by digestion with plasmin. Biochemistry 27:5990–5995, 1988

    Google Scholar 

  138. Sastry SS, Buki KG, Kun E: Binding of adenosine diphosphoribosyltransferase to the termini and internal regions of linear DNAs. Biochemistry 28:5670–5680, 1989

    Google Scholar 

  139. Brennan RG, Matthews BW: The helix-turn-helix DNA binding motif. J Biol Chem 264:1903–1906, 1989

    Google Scholar 

  140. 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

    Google Scholar 

  141. 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

    Google Scholar 

  142. Pugh BF, Tijan R: Mechanism of transcriptional activation by SP1: Evidence for coactivators., Cell 61:1187–1197, 1990

    Google Scholar 

  143. 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

    Google Scholar 

  144. 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

    Google Scholar 

  145. 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

    Google Scholar 

  146. Ruby SW, Szostak JW: Specific Saccharomyces cerevisiae genes are expressed in response to DNA damaging agents. Mol Cell Biol 5:75–84, 1985

    Google Scholar 

  147. 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

    Google Scholar 

  148. 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

    Google Scholar 

  149. 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

    Google Scholar 

  150. 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

    Google Scholar 

  151. 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

    Google Scholar 

  152. 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

    Google Scholar 

  153. 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

    Google Scholar 

  154. 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

    Google Scholar 

  155. 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

    Google Scholar 

  156. 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

    Google Scholar 

  157. 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

    Google Scholar 

  158. 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

    Google Scholar 

  159. 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

    Google Scholar 

  160. 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

    Google Scholar 

  161. 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

    Google Scholar 

  162. Shall S: ADP-ribose in DNA repair: A new component of DNA excision repair. Adv Radiat Biol II:1–69, 1984

    Google Scholar 

  163. Mathis G, Althaus FR: Uncoupling of DNA excision repair and nucleosomal unfolding in poly(ADP-ribose)-depleted mammalian cells. Carcinogenesis 11:1237–1239, 1999

    Google Scholar 

  164. Satoh MS, Lindahl T: Role of poly(ADP-ribose) formation in DNA repair. Nature 356:356–358, 1992

    Google Scholar 

  165. Satoh MS, Poirier GG, Lindahl T: NAD+-dependent repair of damaged DNA by human cell extracts. J Biol Chem 268:5480–5587, 1993

    Google Scholar 

  166. Creissen D, Shall S: Regulation of DNA ligase activity by poly (ADP-ribose). Nature (London) 296:271–272, 1982

    Google Scholar 

  167. 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

    Google Scholar 

  168. 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

    Google Scholar 

  169. 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

    Google Scholar 

  170. 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

    Google Scholar 

  171. 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

    Google Scholar 

  172. 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

    Google Scholar 

  173. 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

    Google Scholar 

  174. 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

    Google Scholar 

  175. Stark GR, Wahl GM: Gene amplification. Ann Rev Biochem 53: 447–491, 1984

    Google Scholar 

  176. 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

    Google Scholar 

  177. 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

    Google Scholar 

  178. 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

    Google Scholar 

  179. 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

    Google Scholar 

  180. Hough CJ, Smulson ME: Association of poly(adenosine diphosphate ribosylated) nucleosomes with transcriptionally active and inactive regions of chromatin. Biochemistry 23:5016–5023, 1984

    Google Scholar 

  181. 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

    Google Scholar 

  182. 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

    Google Scholar 

  183. Jacob ST: Transcription of eukaryotic ribosomal RNA gene. Mol Cell Biochem 70:11–20, 1986

    Google Scholar 

  184. 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

    Google Scholar 

  185. 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

    Google Scholar 

  186. 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

    Google Scholar 

  187. Reeves R: Transcriptionally active chromatin. Biochim Biophys Acta 782:343–393, 1984

    Google Scholar 

  188. Sastry SS, Kun E: The interaction of adenosine diphosphoribosyl transferase (ADPRT) with a cruciform DNA. Biochem Biophys Res Comm 167:842–847, 1990

    Google Scholar 

  189. Koo HS, Wuek HM, Crothers DM: DNA bending at adenine thymine tracts. Nature 320:501–506, 1986

    Google Scholar 

  190. 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

    Google Scholar 

  191. Struhl K: Molecular mechanisms of transcriptional regulation in yeast. Ann Rev Biochem 58:1051–1077, 1989

    Google Scholar 

  192. Zahn K, Blattner FR: Direct evidence for DNA bending at the lambda replication origin. Science 236:416–422, 1987

    Google Scholar 

  193. Lillie JW, Green MR: Transcription activation by the adenovirus Ela protein. Nature 338:39–44, 1989

    Google Scholar 

  194. 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

    Google Scholar 

  195. 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

    Google Scholar 

  196. 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

    Google Scholar 

  197. 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

    Google Scholar 

  198. 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

    Google Scholar 

  199. 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

    Google Scholar 

  200. 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

    Google Scholar 

  201. 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

    Google Scholar 

  202. 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

    Google Scholar 

  203. 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

    Google Scholar 

  204. 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

    Google Scholar 

  205. 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

    Google Scholar 

  206. 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

    Google Scholar 

  207. 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

    Google Scholar 

  208. Weitzman SG, Weitberg AB, Clark EP, Stossel TP: Phagocytes as carcinogens: Malignant transformation produced by human neutrophils. Science 227:1231–1233, 1985

    Google Scholar 

  209. Tanuma S, Kanai Y: Poly(ADP-ribosyl)ation of chromosomal proteins in the HeLa S3 cell cycle. J Biol Chem 257:6565–6570, 1982

    Google Scholar 

  210. Boorstein RJ, Pardee AB: Factors modifying 3-aminobenzamide cytotoxicity in normal and repair-deficient human fibroblasts. J Cell Physiol 120:335–344, 1984

    Google Scholar 

  211. Boorstein RJ, Pardee AB: 3-Aminobenzamide is lethal to MMS-damaged human fibroblasts primarily during G-phase. J Cell Physiol 120:345–353, 1984

    Google Scholar 

  212. 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

    Google Scholar 

  213. 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

    Google Scholar 

  214. 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

    Google Scholar 

  215. 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

    Google Scholar 

  216. 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

    Google Scholar 

  217. Burzio L, Koide SS: A functional role of poly(ADP-R) in DNA synthesis. Biochem Biophys Res Commun 40:1013–1020, 1970

    Google Scholar 

  218. 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

    Google Scholar 

  219. 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

    Google Scholar 

  220. 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

    Google Scholar 

  221. 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

    Google Scholar 

  222. 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

    Google Scholar 

  223. 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

    Google Scholar 

  224. 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

    Google Scholar 

  225. 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

    Google Scholar 

  226. 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

    Google Scholar 

  227. Anachkova B, Russev G, Poirier GG: DNA replication and poly (ADP-ribosy)ation of chromatin. Cytobios 58:19–28, 1989

    Google Scholar 

  228. 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lautier, D., Lagueux, J., Thibodeau, J. et al. Molecular and biochemical features of poly (ADP-ribose) metabolism. Mol Cell Biochem 122, 171–193 (1993). https://doi.org/10.1007/BF01076101

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01076101

Key words

Navigation