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. 1995 Jun;15(6):3154–3163. doi: 10.1128/mcb.15.6.3154

trans-dominant inhibition of poly(ADP-ribosyl)ation sensitizes cells against gamma-irradiation and N-methyl-N'-nitro-N-nitrosoguanidine but does not limit DNA replication of a polyomavirus replicon.

J H Küpper 1, M Müller 1, M K Jacobson 1, J Tatsumi-Miyajima 1, D L Coyle 1, E L Jacobson 1, A Bürkle 1
PMCID: PMC230547  PMID: 7760811

Abstract

Poly(ADP-ribosyl)ation is a posttranslational modification of nuclear proteins catalyzed by poly(ADP-ribose) polymerase (PARP; EC 2.4.2.30), with NAD+ serving as the substrate. PARP is strongly activated upon recognition of DNA strand breaks by its DNA-binding domain. Experiments with low-molecular-weight inhibitors of PARP have led to the view that PARP activity plays a role in DNA repair and possibly also in DNA replication, cell proliferation, and differentiation. Accumulating evidence for nonspecific inhibitor effects prompted us to develop a molecular genetic system to inhibit PARP in living cells, i.e., to overexpress selectively the DNA-binding domain of PARP as a dominant negative mutant. Here we report on a cell culture system which allows inducible, high-level expression of the DNA-binding domain. Induction of this domain leads to about 90% reduction of poly(ADP-ribose) accumulation after gamma-irradiation and sensitizes cells to the cytotoxic effect of gamma-irradiation and of N-methyl-N'-nitro-N-nitrosoguanidine. In contrast, induction does not affect normal cellular proliferation or the replication of a transfected polyomavirus replicon. Thus, trans-dominant inhibition of the poly(ADP-ribose) accumulation occurring after gamma-irradiation or N-methyl-N'-nitro-N-nitrosoguanidine is specifically associated with a disturbance of the cellular recovery from the inflicted damage.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aboul-Ela N., Jacobson E. L., Jacobson M. K. Labeling methods for the study of poly- and mono(ADP-ribose) metabolism in cultured cells. Anal Biochem. 1988 Oct;174(1):239–250. doi: 10.1016/0003-2697(88)90541-6. [DOI] [PubMed] [Google Scholar]
  2. Alksnis M., Barkhem T., Strömstedt P. E., Ahola H., Kutoh E., Gustafsson J. A., Poellinger L., Nilsson S. High level expression of functional full length and truncated glucocorticoid receptor in Chinese hamster ovary cells. Demonstration of ligand-induced down-regulation of expressed receptor mRNA and protein. J Biol Chem. 1991 Jun 5;266(16):10078–10085. [PubMed] [Google Scholar]
  3. Althaus F. R. Poly ADP-ribosylation: a histone shuttle mechanism in DNA excision repair. J Cell Sci. 1992 Aug;102(Pt 4):663–670. doi: 10.1242/jcs.102.4.663. [DOI] [PubMed] [Google Scholar]
  4. Althaus F. R., Richter C. ADP-ribosylation of proteins. Enzymology and biological significance. Mol Biol Biochem Biophys. 1987;37:1–237. [PubMed] [Google Scholar]
  5. Alvarez-Gonzalez R., Althaus F. R. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat Res. 1989 Sep;218(2):67–74. doi: 10.1016/0921-8777(89)90012-8. [DOI] [PubMed] [Google Scholar]
  6. Bellingham D. L., Cidlowski J. A. Stable overproduction of intact glucocorticoid receptors in mammalian cells using a selectable glucocorticoid responsive dihydrofolate reductase gene. Mol Endocrinol. 1989 Nov;3(11):1733–1747. doi: 10.1210/mend-3-11-1733. [DOI] [PubMed] [Google Scholar]
  7. Berger N. A., Berger S. J. Metabolic consequences of DNA damage: the role of poly (ADP-ribose) polymerase as mediator of the suicide response. Basic Life Sci. 1986;38:357–363. doi: 10.1007/978-1-4615-9462-8_39. [DOI] [PubMed] [Google Scholar]
  8. Borek C., Morgan W. F., Ong A., Cleaver J. E. Inhibition of malignant transformation in vitro by inhibitors of poly(ADP-ribose) synthesis. Proc Natl Acad Sci U S A. 1984 Jan;81(1):243–247. doi: 10.1073/pnas.81.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Boulikas T. Poly(ADP-ribosyl)ation, DNA strand breaks, chromatin and cancer. Toxicol Lett. 1993 Apr;67(1-3):129–150. doi: 10.1016/0378-4274(93)90051-x. [DOI] [PubMed] [Google Scholar]
  10. Boulikas T. Relation between carcinogenesis, chromatin structure and poly(ADP-ribosylation) (review). Anticancer Res. 1991 Mar-Apr;11(2):489–527. [PubMed] [Google Scholar]
  11. Breathnach R., Harris B. A. Plasmids for the cloning and expression of full-length double-stranded cDNAs under control of the SV40 early or late gene promoter. Nucleic Acids Res. 1983 Oct 25;11(20):7119–7136. doi: 10.1093/nar/11.20.7119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Burnstein K. L., Bellingham D. L., Jewell C. M., Powell-Oliver F. E., Cidlowski J. A. Autoregulation of glucocorticoid receptor gene expression. Steroids. 1991 Feb;56(2):52–58. doi: 10.1016/0039-128x(91)90124-e. [DOI] [PubMed] [Google Scholar]
  13. Burnstein K. L., Jewell C. M., Cidlowski J. A. Human glucocorticoid receptor cDNA contains sequences sufficient for receptor down-regulation. J Biol Chem. 1990 May 5;265(13):7284–7291. [PubMed] [Google Scholar]
  14. Bürkle A., Chen G., Küpper J. H., Grube K., Zeller W. J. Increased poly(ADP-ribosyl)ation in intact cells by cisplatin treatment. Carcinogenesis. 1993 Apr;14(4):559–561. doi: 10.1093/carcin/14.4.559. [DOI] [PubMed] [Google Scholar]
  15. Bürkle A., Grube K., Küpper J. H. Poly(ADP-ribosyl)ation: its role in inducible DNA amplification, and its correlation with the longevity of mammalian species. Exp Clin Immunogenet. 1992;9(4):230–240. [PubMed] [Google Scholar]
  16. Bürkle A., Heilbronn R., zur Hausen H. Potentiation of carcinogen-induced methotrexate resistance and dihydrofolate reductase gene amplification by inhibitors of poly(adenosine diphosphate-ribose) polymerase. Cancer Res. 1990 Sep 15;50(18):5756–5760. [PubMed] [Google Scholar]
  17. Bürkle A., Meyer T., Hilz H., zur Hausen H. Enhancement of N-methyl-N'-nitro-N-nitrosoguanidine-induced DNA amplification in a Simian virus 40-transformed Chinese hamster cell line by 3-aminobenzamide. Cancer Res. 1987 Jul 15;47(14):3632–3636. [PubMed] [Google Scholar]
  18. Chatterjee S., Cheng M. F., Berger S. J., Berger N. A. Alkylating agent hypersensitivity in poly(adenosine diphosphate-ribose) polymerase deficient cell lines. Cancer Commun. 1991 Mar;3(3):71–75. doi: 10.3727/095535491820873551. [DOI] [PubMed] [Google Scholar]
  19. Cherney B. W., McBride O. W., Chen D. F., Alkhatib H., Bhatia K., Hensley P., Smulson M. E. cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8370–8374. doi: 10.1073/pnas.84.23.8370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Desmarais Y., Ménard L., Lagueux J., Poirier G. G. Enzymological properties of poly(ADP-ribose)polymerase: characterization of automodification sites and NADase activity. Biochim Biophys Acta. 1991 Jun 24;1078(2):179–186. doi: 10.1016/0167-4838(91)99007-f. [DOI] [PubMed] [Google Scholar]
  21. Ding R., Pommier Y., Kang V. H., Smulson M. Depletion of poly(ADP-ribose) polymerase by antisense RNA expression results in a delay in DNA strand break rejoining. J Biol Chem. 1992 Jun 25;267(18):12804–12812. [PubMed] [Google Scholar]
  22. Ding R., Smulson M. Depletion of nuclear poly(ADP-ribose) polymerase by antisense RNA expression: influences on genomic stability, chromatin organization, and carcinogen cytotoxicity. Cancer Res. 1994 Sep 1;54(17):4627–4634. [PubMed] [Google Scholar]
  23. Durkacz B. W., Omidiji O., Gray D. A., Shall S. (ADP-ribose)n participates in DNA excision repair. Nature. 1980 Feb 7;283(5747):593–596. doi: 10.1038/283593a0. [DOI] [PubMed] [Google Scholar]
  24. Eki T., Hurwitz J. Influence of poly(ADP-ribose) polymerase on the enzymatic synthesis of SV40 DNA. J Biol Chem. 1991 Feb 15;266(5):3087–3100. [PubMed] [Google Scholar]
  25. Fasel N., Pearson K., Buetti E., Diggelmann H. The region of mouse mammary tumor virus DNA containing the long terminal repeat includes a long coding sequence and signals for hormonally regulated transcription. EMBO J. 1982;1(1):3–7. doi: 10.1002/j.1460-2075.1982.tb01115.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Giguère V., Hollenberg S. M., Rosenfeld M. G., Evans R. M. Functional domains of the human glucocorticoid receptor. Cell. 1986 Aug 29;46(5):645–652. doi: 10.1016/0092-8674(86)90339-9. [DOI] [PubMed] [Google Scholar]
  27. Hahn P., Nevaldine B., Morgan W. F. X-ray induction of methotrexate resistance due to dhfr gene amplification. Somat Cell Mol Genet. 1990 Sep;16(5):413–423. doi: 10.1007/BF01233191. [DOI] [PubMed] [Google Scholar]
  28. Hunting D. J., Gowans B. J., Henderson J. F. Specificity of inhibitors of poly(ADP-ribose) synthesis. Effects on nucleotide metabolism in cultured cells. Mol Pharmacol. 1985 Aug;28(2):200–206. [PubMed] [Google Scholar]
  29. Huppi K., Bhatia K., Siwarski D., Klinman D., Cherney B., Smulson M. Sequence and organization of the mouse poly (ADP-ribose) polymerase gene. Nucleic Acids Res. 1989 May 11;17(9):3387–3401. doi: 10.1093/nar/17.9.3387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Imschenetzky M., Montecino M., Puchi M. Poly(ADP-ribosylation) of atypical CS histone variants is required for the progression of S phase in early embryos of sea urchins. J Cell Biochem. 1991 Jul;46(3):234–241. doi: 10.1002/jcb.240460306. [DOI] [PubMed] [Google Scholar]
  31. Imschenetzky M., Montecino M., Puchi M. Temporally different poly(adenosine diphosphate-ribosylation) signals are required for DNA replication and cell division in early embryos of sea urchins. J Cell Biochem. 1993 Feb;51(2):198–205. doi: 10.1002/jcb.240510212. [DOI] [PubMed] [Google Scholar]
  32. Jacobson E. L., Jacobson M. K. Pyridine nucleotide levels as a function of growth in normal and transformed 3T3 cells. Arch Biochem Biophys. 1976 Aug;175(2):627–634. doi: 10.1016/0003-9861(76)90553-1. [DOI] [PubMed] [Google Scholar]
  33. Jacobson E. L., Meadows R., Measel J. Cell cycle perturbations following DNA damage in the presence of ADP-ribosylation inhibitors. Carcinogenesis. 1985 May;6(5):711–714. doi: 10.1093/carcin/6.5.711. [DOI] [PubMed] [Google Scholar]
  34. Jacobson E. L., Smith J. Y., Wielckens K., Hilz H., Jacobson M. K. Cellular recovery of dividing and confluent C3H10T1/2 cells from N-methyl-N'-nitro-N-nitrosoguanidine in the presence of ADP-ribosylation inhibitors. Carcinogenesis. 1985 May;6(5):715–718. doi: 10.1093/carcin/6.5.715. [DOI] [PubMed] [Google Scholar]
  35. Juarez-Salinas H., Sims J. L., Jacobson M. K. Poly(ADP-ribose) levels in carcinogen-treated cells. Nature. 1979 Dec 13;282(5740):740–741. doi: 10.1038/282740a0. [DOI] [PubMed] [Google Scholar]
  36. Kasid U. N., Stefanik D. F., Lubet R. A., Dritschilo A., Smulson M. E. Relationship between DNA strand breaks and inhibition of poly (ADP-ribosylation): enhancement of carcinogen-induced transformation. Carcinogenesis. 1986 Feb;7(2):327–330. doi: 10.1093/carcin/7.2.327. [DOI] [PubMed] [Google Scholar]
  37. Kawamitsu H., Hoshino H., Okada H., Miwa M., Momoi H., Sugimura T. Monoclonal antibodies to poly(adenosine diphosphate ribose) recognize different structures. Biochemistry. 1984 Jul 31;23(16):3771–3777. doi: 10.1021/bi00311a032. [DOI] [PubMed] [Google Scholar]
  38. Klehr D., Maass K., Bode J. Scaffold-attached regions from the human interferon beta domain can be used to enhance the stable expression of genes under the control of various promoters. Biochemistry. 1991 Feb 5;30(5):1264–1270. doi: 10.1021/bi00219a015. [DOI] [PubMed] [Google Scholar]
  39. Ko M. S., Takano T. A highly inducible system of gene expression by positive feedback production of glucocorticoid receptors. DNA. 1989 Mar;8(2):127–133. doi: 10.1089/dna.1.1989.8.127. [DOI] [PubMed] [Google Scholar]
  40. Krupitza G., Cerutti P. ADP-ribosylation of ADPR-transferase and topoisomerase I in intact mouse epidermal cells JB6. Biochemistry. 1989 Mar 7;28(5):2034–2040. doi: 10.1021/bi00431a011. [DOI] [PubMed] [Google Scholar]
  41. Krupitza G., Cerutti P. Poly(ADP-ribosylation) of histones in intact human keratinocytes. Biochemistry. 1989 May 2;28(9):4054–4060. doi: 10.1021/bi00435a063. [DOI] [PubMed] [Google Scholar]
  42. Kurosaki T., Ushiro H., Mitsuuchi Y., Suzuki S., Matsuda M., Matsuda Y., Katunuma N., Kangawa K., Matsuo H., Hirose T. Primary structure of human poly(ADP-ribose) synthetase as deduced from cDNA sequence. J Biol Chem. 1987 Nov 25;262(33):15990–15997. [PubMed] [Google Scholar]
  43. Küpper J. H., de Murcia G., Bürkle A. Inhibition of poly(ADP-ribosyl)ation by overexpressing the poly(ADP-ribose) polymerase DNA-binding domain in mammalian cells. J Biol Chem. 1990 Nov 5;265(31):18721–18724. [PubMed] [Google Scholar]
  44. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  45. Lavi S. Carcinogen-mediated amplification of viral DNA sequences in simian virus 40-transformed Chinese hamster embryo cells. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6144–6148. doi: 10.1073/pnas.78.10.6144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Lee S. H., Kwong A. D., Ishimi Y., Hurwitz J. Studies on the DNA elongation inhibitor and its proliferating cell nuclear antigen-dependent control in simian virus 40 DNA replication in vitro. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4877–4881. doi: 10.1073/pnas.86.13.4877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lönn U., Lönn S. Accumulation of 10-kilobase DNA replication intermediates in cells treated with 3-aminobenzamide. Proc Natl Acad Sci U S A. 1985 Jan;82(1):104–108. doi: 10.1073/pnas.82.1.104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lönn U., Lönn S., Nylen U., Winblad G. Altered formation of DNA replication intermediates in human 46 BR fibroblast cells hypersensitive to 3-aminobenzamide. Carcinogenesis. 1989 Jun;10(6):981–985. doi: 10.1093/carcin/10.6.981. [DOI] [PubMed] [Google Scholar]
  49. Lönn U., Lönn S. Step-wise progression of mammalian 10-kb DNA replication intermediates to mature chromatin. Eur J Biochem. 1988 Dec 1;178(1):47–51. doi: 10.1111/j.1432-1033.1988.tb14427.x. [DOI] [PubMed] [Google Scholar]
  50. Mendoza-Alvarez H., Alvarez-Gonzalez R. Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem. 1993 Oct 25;268(30):22575–22580. [PubMed] [Google Scholar]
  51. Milam K. M., Cleaver J. E. Inhibitors of poly(adenosine diphosphate-ribose) synthesis: effect on other metabolic processes. Science. 1984 Feb 10;223(4636):589–591. doi: 10.1126/science.6420886. [DOI] [PubMed] [Google Scholar]
  52. Milam K. M., Thomas G. H., Cleaver J. E. Disturbances in DNA precursor metabolism associated with exposure to an inhibitor of poly(ADP-ribose) synthetase. Exp Cell Res. 1986 Jul;165(1):260–268. doi: 10.1016/0014-4827(86)90550-1. [DOI] [PubMed] [Google Scholar]
  53. Molinete M., Vermeulen W., Bürkle A., Ménissier-de Murcia J., Küpper J. H., Hoeijmakers J. H., de Murcia G. Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J. 1993 May;12(5):2109–2117. doi: 10.1002/j.1460-2075.1993.tb05859.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Moriwaki S., Yagi T., Nishigori C., Imamura S., Takebe H. Analysis of N-methyl-N-nitrosourea-induced mutations in a shuttle vector plasmid propagated in mouse O6-methylguanine-DNA methyltransferase-deficient cells in comparison with proficient cells. Cancer Res. 1991 Dec 1;51(23 Pt 1):6219–6223. [PubMed] [Google Scholar]
  55. Moses K., Harris A. L., Durkacz B. W. Synergistic enhancement of 6-thioguanine cytotoxicity by ADP-ribosyltransferase inhibitors. Cancer Res. 1988 Oct 15;48(20):5650–5654. [PubMed] [Google Scholar]
  56. Okret S., Poellinger L., Dong Y., Gustafsson J. A. Down-regulation of glucocorticoid receptor mRNA by glucocorticoid hormones and recognition by the receptor of a specific binding sequence within a receptor cDNA clone. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5899–5903. doi: 10.1073/pnas.83.16.5899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ozawa Y., Uchida K., Uchida M., Ami Y., Kushida S., Okada N., Miwa M. Isolation of cDNAs encoding the catalytic domain of poly(ADP-ribose) polymerase from Xenopus laevis and cherry salmon using heterologous oligonucleotide consensus sequences. Biochem Biophys Res Commun. 1993 May 28;193(1):119–125. doi: 10.1006/bbrc.1993.1598. [DOI] [PubMed] [Google Scholar]
  58. Phi-Van L., von Kries J. P., Ostertag W., Strätling W. H. The chicken lysozyme 5' matrix attachment region increases transcription from a heterologous promoter in heterologous cells and dampens position effects on the expression of transfected genes. Mol Cell Biol. 1990 May;10(5):2302–2307. doi: 10.1128/mcb.10.5.2302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Radons J., Heller B., Bürkle A., Hartmann B., Rodriguez M. L., Kröncke K. D., Burkart V., Kolb H. Nitric oxide toxicity in islet cells involves poly(ADP-ribose) polymerase activation and concomitant NAD+ depletion. Biochem Biophys Res Commun. 1994 Mar 30;199(3):1270–1277. doi: 10.1006/bbrc.1994.1368. [DOI] [PubMed] [Google Scholar]
  60. Rankin P. W., Jacobson E. L., Benjamin R. C., Moss J., Jacobson M. K. Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo. J Biol Chem. 1989 Mar 15;264(8):4312–4317. [PubMed] [Google Scholar]
  61. Rosewicz S., McDonald A. R., Maddux B. A., Goldfine I. D., Miesfeld R. L., Logsdon C. D. Mechanism of glucocorticoid receptor down-regulation by glucocorticoids. J Biol Chem. 1988 Feb 25;263(6):2581–2584. [PubMed] [Google Scholar]
  62. 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. 1990 Jun 15;90(2):249–254. doi: 10.1016/0378-1119(90)90187-v. [DOI] [PubMed] [Google Scholar]
  63. Satoh M. S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 1992 Mar 26;356(6367):356–358. doi: 10.1038/356356a0. [DOI] [PubMed] [Google Scholar]
  64. Satoh M. S., Poirier G. G., Lindahl T. NAD(+)-dependent repair of damaged DNA by human cell extracts. J Biol Chem. 1993 Mar 15;268(8):5480–5487. [PubMed] [Google Scholar]
  65. Scovassi A. I., Mariani C., Negroni M., Negri C., Bertazzoni U. ADP-ribosylation of nonhistone proteins in HeLa cells: modification of DNA topoisomerase II. Exp Cell Res. 1993 May;206(1):177–181. doi: 10.1006/excr.1993.1135. [DOI] [PubMed] [Google Scholar]
  66. Simonin F., Briand J. P., Muller S., de Murcia G. Detection of poly(ADP ribose) polymerase in crude extracts by activity-blot. Anal Biochem. 1991 Jun;195(2):226–231. doi: 10.1016/0003-2697(91)90321-j. [DOI] [PubMed] [Google Scholar]
  67. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  68. Takahashi S., Nakae D., Yokose Y., Emi Y., Denda A., Mikami S., Ohnishi T., Konishi Y. Enhancement of DEN initiation of liver carcinogenesis by inhibitors of NAD+ ADP ribosyl transferase in rats. Carcinogenesis. 1984 Jul;5(7):901–906. doi: 10.1093/carcin/5.7.901. [DOI] [PubMed] [Google Scholar]
  69. Thibodeau J., Gradwohl G., Dumas C., Clairoux-Moreau S., Brunet G., Penning C., Poirier G. G., Moreau P. Cloning of rodent cDNA coding the poly(ADP-ribose) polymerase catalytic domain and analysis of mRNA levels during the cell cycle. Biochem Cell Biol. 1989 Sep;67(9):653–660. doi: 10.1139/o89-097. [DOI] [PubMed] [Google Scholar]
  70. Tsurimoto T., Melendy T., Stillman B. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature. 1990 Aug 9;346(6284):534–539. doi: 10.1038/346534a0. [DOI] [PubMed] [Google Scholar]
  71. Uchida K., Hanai S., Ishikawa K., Ozawa Y., Uchida M., Sugimura T., Miwa M. Cloning of cDNA encoding Drosophila poly(ADP-ribose) polymerase: leucine zipper in the auto-modification domain. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3481–3485. doi: 10.1073/pnas.90.8.3481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. 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. 1987 Oct 29;148(2):617–622. doi: 10.1016/0006-291x(87)90921-1. [DOI] [PubMed] [Google Scholar]
  73. Wigler M., Pellicer A., Silverstein S., Axel R., Urlaub G., Chasin L. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1373–1376. doi: 10.1073/pnas.76.3.1373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Witmer M. V., Aboul-Ela N., Jacobson M. K., Stamato T. D. Increased sensitivity to DNA-alkylating agents in CHO mutants with decreased poly(ADP-ribose) polymerase activity. Mutat Res. 1994 May;314(3):249–260. doi: 10.1016/0921-8777(94)90069-8. [DOI] [PubMed] [Google Scholar]
  75. Zhang J., Dawson V. L., Dawson T. M., Snyder S. H. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science. 1994 Feb 4;263(5147):687–689. doi: 10.1126/science.8080500. [DOI] [PubMed] [Google Scholar]
  76. de Murcia G., Ménissier de Murcia J. Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem Sci. 1994 Apr;19(4):172–176. doi: 10.1016/0968-0004(94)90280-1. [DOI] [PubMed] [Google Scholar]

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