Skip to main content
NCBI home page
American Journal of Human Genetics logoLink to American Journal of Human Genetics
. 1999 May;64(5):1282–1288. doi: 10.1086/302389

Poly(ADP-ribose) polymerase in the cellular response to DNA damage, apoptosis, and disease.

F J Oliver 1, J Menissier-de Murcia 1, G de Murcia 1
PMCID: PMC1377863  PMID: 10205258

Full Text

The Full Text of this article is available as a PDF (203.0 KB).

Selected References

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

  1. Agarwal M. L., Agarwal A., Taylor W. R., Wang Z. Q., Wagner E. F., Stark G. R. Defective induction but normal activation and function of p53 in mouse cells lacking poly-ADP-ribose polymerase. Oncogene. 1997 Aug 28;15(9):1035–1041. doi: 10.1038/sj.onc.1201274. [DOI] [PubMed] [Google Scholar]
  2. Barone F. C., Arvin B., White R. F., Miller A., Webb C. L., Willette R. N., Lysko P. G., Feuerstein G. Z. Tumor necrosis factor-alpha. A mediator of focal ischemic brain injury. Stroke. 1997 Jun;28(6):1233–1244. doi: 10.1161/01.str.28.6.1233. [DOI] [PubMed] [Google Scholar]
  3. Burkart V., Wang Z. Q., Radons J., Heller B., Herceg Z., Stingl L., Wagner E. F., Kolb H. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat Med. 1999 Mar;5(3):314–319. doi: 10.1038/6535. [DOI] [PubMed] [Google Scholar]
  4. Butler A. J., Ordahl C. P. Poly(ADP-ribose) polymerase binds with transcription enhancer factor 1 to MCAT1 elements to regulate muscle-specific transcription. Mol Cell Biol. 1999 Jan;19(1):296–306. doi: 10.1128/mcb.19.1.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Caldecott K. W., Aoufouchi S., Johnson P., Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 1996 Nov 15;24(22):4387–4394. doi: 10.1093/nar/24.22.4387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casciola-Rosen L., Nicholson D. W., Chong T., Rowan K. R., Thornberry N. A., Miller D. K., Rosen A. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J Exp Med. 1996 May 1;183(5):1957–1964. doi: 10.1084/jem.183.5.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dantzer F., Nasheuer H. P., Vonesch J. L., de Murcia G., Ménissier-de Murcia J. Functional association of poly(ADP-ribose) polymerase with DNA polymerase alpha-primase complex: a link between DNA strand break detection and DNA replication. Nucleic Acids Res. 1998 Apr 15;26(8):1891–1898. doi: 10.1093/nar/26.8.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dantzer F., Schreiber V., Niedergang C., Trucco C., Flatter E., De La Rubia G., Oliver J., Rolli V., Ménissier-de Murcia J., de Murcia G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie. 1999 Jan-Feb;81(1-2):69–75. doi: 10.1016/s0300-9084(99)80040-6. [DOI] [PubMed] [Google Scholar]
  9. Duriez P. J., Shah G. M. Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biol. 1997;75(4):337–349. [PubMed] [Google Scholar]
  10. Evan G., Littlewood T. A matter of life and cell death. Science. 1998 Aug 28;281(5381):1317–1322. doi: 10.1126/science.281.5381.1317. [DOI] [PubMed] [Google Scholar]
  11. Guillouf C., Wang T. S., Liu J., Walsh C. E., Poirier G. G., Moustacchi E., Rosselli F. Fanconi anemia C protein acts at a switch between apoptosis and necrosis in mitomycin C-induced cell death. Exp Cell Res. 1999 Feb 1;246(2):384–394. doi: 10.1006/excr.1998.4316. [DOI] [PubMed] [Google Scholar]
  12. Hirsch T., Marchetti P., Susin S. A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene. 1997 Sep 25;15(13):1573–1581. doi: 10.1038/sj.onc.1201324. [DOI] [PubMed] [Google Scholar]
  13. Kaufmann S. H., Desnoyers S., Ottaviano Y., Davidson N. E., Poirier G. G. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993 Sep 1;53(17):3976–3985. [PubMed] [Google Scholar]
  14. Le Cam E., Fack F., Ménissier-de Murcia J., Cognet J. A., Barbin A., Sarantoglou V., Révet B., Delain E., de Murcia G. Conformational analysis of a 139 base-pair DNA fragment containing a single-stranded break and its interaction with human poly(ADP-ribose) polymerase. J Mol Biol. 1994 Jan 21;235(3):1062–1071. doi: 10.1006/jmbi.1994.1057. [DOI] [PubMed] [Google Scholar]
  15. Leadon S. A. Transcription-coupled repair of DNA damage: unanticipated players, unexpected complexities. Am J Hum Genet. 1999 May;64(5):1259–1263. doi: 10.1086/302390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lee J. S., Haug B. L., Sibley J. T. Decreased mRNA levels coding for poly(ADP-ribose) polymerase in lymphocytes of patients with SLE. Lupus. 1994 Apr;3(2):113–116. doi: 10.1177/096120339400300210. [DOI] [PubMed] [Google Scholar]
  17. Leist M., Single B., Castoldi A. F., Kühnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997 Apr 21;185(8):1481–1486. doi: 10.1084/jem.185.8.1481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lu X., Lane D. P. Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell. 1993 Nov 19;75(4):765–778. doi: 10.1016/0092-8674(93)90496-d. [DOI] [PubMed] [Google Scholar]
  19. Maizels N. Immunoglobulin class switch recombination: will genetics provide new clues to mechanism? Am J Hum Genet. 1999 May;64(5):1270–1275. doi: 10.1086/302393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Malanga M., Pleschke J. M., Kleczkowska H. E., Althaus F. R. Poly(ADP-ribose) binds to specific domains of p53 and alters its DNA binding functions. J Biol Chem. 1998 May 8;273(19):11839–11843. doi: 10.1074/jbc.273.19.11839. [DOI] [PubMed] [Google Scholar]
  21. Masson M., Niedergang C., Schreiber V., Muller S., Menissier-de Murcia J., de Murcia G. XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol. 1998 Jun;18(6):3563–3571. doi: 10.1128/mcb.18.6.3563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Masutani M., Suzuki H., Kamada N., Watanabe M., Ueda O., Nozaki T., Jishage K., Watanabe T., Sugimoto T., Nakagama H. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2301–2304. doi: 10.1073/pnas.96.5.2301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morrison C., Smith G. C., Stingl L., Jackson S. P., Wagner E. F., Wang Z. Q. Genetic interaction between PARP and DNA-PK in V(D)J recombination and tumorigenesis. Nat Genet. 1997 Dec;17(4):479–482. doi: 10.1038/ng1297-479. [DOI] [PubMed] [Google Scholar]
  24. Moser K. L., Neas B. R., Salmon J. E., Yu H., Gray-McGuire C., Asundi N., Bruner G. R., Fox J., Kelly J., Henshall S. Genome scan of human systemic lupus erythematosus: evidence for linkage on chromosome 1q in African-American pedigrees. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14869–14874. doi: 10.1073/pnas.95.25.14869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nie J., Sakamoto S., Song D., Qu Z., Ota K., Taniguchi T. Interaction of Oct-1 and automodification domain of poly(ADP-ribose) synthetase. FEBS Lett. 1998 Mar 6;424(1-2):27–32. doi: 10.1016/s0014-5793(98)00131-8. [DOI] [PubMed] [Google Scholar]
  26. Oei S. L., Griesenbeck J., Schweiger M. The role of poly(ADP-ribosyl)ation. Rev Physiol Biochem Pharmacol. 1997;131:127–173. doi: 10.1007/3-540-61992-5_7. [DOI] [PubMed] [Google Scholar]
  27. Oei S. L., Griesenbeck J., Schweiger M., Ziegler M. Regulation of RNA polymerase II-dependent transcription by poly(ADP-ribosyl)ation of transcription factors. J Biol Chem. 1998 Nov 27;273(48):31644–31647. doi: 10.1074/jbc.273.48.31644. [DOI] [PubMed] [Google Scholar]
  28. Oliver F. J., de la Rubia G., Rolli V., Ruiz-Ruiz M. C., de Murcia G., Murcia J. M. Importance of poly(ADP-ribose) polymerase and its cleavage in apoptosis. Lesson from an uncleavable mutant. J Biol Chem. 1998 Dec 11;273(50):33533–33539. doi: 10.1074/jbc.273.50.33533. [DOI] [PubMed] [Google Scholar]
  29. Ouchi T., Monteiro A. N., August A., Aaronson S. A., Hanafusa H. BRCA1 regulates p53-dependent gene expression. Proc Natl Acad Sci U S A. 1998 Mar 3;95(5):2302–2306. doi: 10.1073/pnas.95.5.2302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Plaza S., Aumercier M., Bailly M., Dozier C., Saule S. Involvement of poly (ADP-ribose)-polymerase in the Pax-6 gene regulation in neuroretina. Oncogene. 1999 Jan 28;18(4):1041–1051. doi: 10.1038/sj.onc.1202406. [DOI] [PubMed] [Google Scholar]
  31. Rao L., Perez D., White E. Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol. 1996 Dec;135(6 Pt 1):1441–1455. doi: 10.1083/jcb.135.6.1441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Ruscetti T., Lehnert B. E., Halbrook J., Le Trong H., Hoekstra M. F., Chen D. J., Peterson S. R. Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J Biol Chem. 1998 Jun 5;273(23):14461–14467. doi: 10.1074/jbc.273.23.14461. [DOI] [PubMed] [Google Scholar]
  33. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 1998 Jan 1;391(6662):96–99. doi: 10.1038/34214. [DOI] [PubMed] [Google Scholar]
  34. Simbulan-Rosenthal C. M., Rosenthal D. S., Ding R., Bhatia K., Smulson M. E. Prolongation of the p53 response to DNA strand breaks in cells depleted of PARP by antisense RNA expression. Biochem Biophys Res Commun. 1998 Dec 30;253(3):864–868. doi: 10.1006/bbrc.1998.9792. [DOI] [PubMed] [Google Scholar]
  35. Simbulan-Rosenthal C. M., Rosenthal D. S., Iyer S., Boulares A. H., Smulson M. E. Transient poly(ADP-ribosyl)ation of nuclear proteins and role of poly(ADP-ribose) polymerase in the early stages of apoptosis. J Biol Chem. 1998 May 29;273(22):13703–13712. doi: 10.1074/jbc.273.22.13703. [DOI] [PubMed] [Google Scholar]
  36. Smith S., Giriat I., Schmitt A., de Lange T. Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science. 1998 Nov 20;282(5393):1484–1487. doi: 10.1126/science.282.5393.1484. [DOI] [PubMed] [Google Scholar]
  37. Smulson M. E., Pang D., Jung M., Dimtchev A., Chasovskikh S., Spoonde A., Simbulan-Rosenthal C., Rosenthal D., Yakovlev A., Dritschilo A. Irreversible binding of poly(ADP)ribose polymerase cleavage product to DNA ends revealed by atomic force microscopy: possible role in apoptosis. Cancer Res. 1998 Aug 15;58(16):3495–3498. [PubMed] [Google Scholar]
  38. Szabó C., Dawson V. L. Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends Pharmacol Sci. 1998 Jul;19(7):287–298. doi: 10.1016/s0165-6147(98)01193-6. [DOI] [PubMed] [Google Scholar]
  39. Thornberry N. A., Lazebnik Y. Caspases: enemies within. Science. 1998 Aug 28;281(5381):1312–1316. doi: 10.1126/science.281.5381.1312. [DOI] [PubMed] [Google Scholar]
  40. Trucco C., Oliver F. J., de Murcia G., Ménissier-de Murcia J. DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res. 1998 Jun 1;26(11):2644–2649. doi: 10.1093/nar/26.11.2644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tsao B. P., Cantor R. M., Kalunian K. C., Chen C. J., Badsha H., Singh R., Wallace D. J., Kitridou R. C., Chen S. L., Shen N. Evidence for linkage of a candidate chromosome 1 region to human systemic lupus erythematosus. J Clin Invest. 1997 Feb 15;99(4):725–731. doi: 10.1172/JCI119217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wang X., Ohnishi K., Takahashi A., Ohnishi T. Poly(ADP-ribosyl)ation is required for p53-dependent signal transduction induced by radiation. Oncogene. 1998 Dec 3;17(22):2819–2825. doi: 10.1038/sj.onc.1202216. [DOI] [PubMed] [Google Scholar]
  43. Wang Z. Q., Stingl L., Morrison C., Jantsch M., Los M., Schulze-Osthoff K., Wagner E. F. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 1997 Sep 15;11(18):2347–2358. doi: 10.1101/gad.11.18.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Whitacre C. M., Hashimoto H., Tsai M. L., Chatterjee S., Berger S. J., Berger N. A. Involvement of NAD-poly(ADP-ribose) metabolism in p53 regulation and its consequences. Cancer Res. 1995 Sep 1;55(17):3697–3701. [PubMed] [Google Scholar]
  45. Zardo G., Caiafa P. The unmethylated state of CpG islands in mouse fibroblasts depends on the poly(ADP-ribosyl)ation process. J Biol Chem. 1998 Jun 26;273(26):16517–16520. doi: 10.1074/jbc.273.26.16517. [DOI] [PubMed] [Google Scholar]
  46. Zechiedrich E. L., Osheroff N. Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 1990 Dec;9(13):4555–4562. doi: 10.1002/j.1460-2075.1990.tb07908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. de Murcia G., Huletsky A., Lamarre D., Gaudreau A., Pouyet J., Daune M., Poirier G. G. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J Biol Chem. 1986 May 25;261(15):7011–7017. [PubMed] [Google Scholar]
  48. 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]
  49. de Murcia J. M., Niedergang C., Trucco C., Ricoul M., Dutrillaux B., Mark M., Oliver F. J., Masson M., Dierich A., LeMeur M. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7303–7307. doi: 10.1073/pnas.94.14.7303. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from American Journal of Human Genetics are provided here courtesy of American Society of Human Genetics

RESOURCES