Decreased PARP-1 levels accelerate embryonic lethality but attenuate neuronal apoptosis in DNA polymerase β-deficient mice

Biochemical and Biophysical Research Communications

Volumn 354, Issue 3, 2007, Pages 656-661

  Sugo, Noriyuki ^a   Niimi, Naoko ^a   Aratani, Yasuaki ^a   Masutani, Mitsuko ^b   Suzuki, Hiroshi ^c   Koyama, Hideki ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

Author keywords

Development; DNA polymerase ; Knockout mouse; Neuronal apoptosis; PARP 1

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN P53; SERINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG HYPERSENSITIVITY; EMBRYO; EMBRYO DEVELOPMENT; GENOTOXICITY; HETEROZYGOSITY; KNOCKOUT MOUSE; LETHALITY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NULL ALLELE; PREGNANCY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; APOPTOSIS; DNA POLYMERASE BETA; EMBRYO; FEMALE; MICE; MICE, KNOCKOUT; MUTAGENS; MUTATION; NERVOUS SYSTEM; POLY(ADP-RIBOSE) POLYMERASES; SERINE; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; MAMMALIA; MUS;

EID: 33846626455     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2006.12.230     Document Type: Article

References (36)

1. Lindahl T., and Wood R.D. Quality control by DNA repair. Science 286 (1999) 1897-1905
2. Barnes D.E., and Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38 (2004) 445-476
3. Wilson S.H. Mammalian base excision repair and DNA polymerase beta. Mutat. Res. 407 (1998) 203-215
4. Parsons J.L., Dianova I.I., Allinson S.L., and Dianov G.L. DNA polymerase beta promotes recruitment of DNA ligase IIIalpha-XRCC1 to sites of base excision repair. Biochemistry 44 (2005) 10613-10619
5. Klungland A., and Lindahl T. Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 16 (1997) 3341-3348
6. Gu H., Marth J.D., Orban P.C., Mossmann H., and Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265 (1994) 103-106
7. Sugo N., Aratani Y., Nagashima Y., Kubota Y., and Koyama H. Neonatal lethality with abnormal neurogenesis in mice deficient in DNA polymerase beta. EMBO J. 19 (2000) 1397-1404
8. Sugo N., Niimi N., Aratani Y., Takiguchi-Hayashi K., and Koyama H. p53 deficiency rescues neuronal apoptosis but not differentiation in DNA polymerase beta-deficient mice. Mol. Cell. Biol. 24 (2004) 9470-9477
9. Sobol R.W., Horton J.K., Kuhn R., Gu H., Singhal R.K., Prasad R., Rajewsky K., and Wilson S.H. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 379 (1996) 183-186 published errata appear in Nature 379(6568) (1996) 848; 383(6599) (1996) 457
10. Biade S., Sobol R.W., Wilson S.H., and Matsumoto Y. Impairment of proliferating cell nuclear antigen-dependent apurinic/apyrimidinic site repair on linear DNA. J. Biol. Chem. 273 (1998) 898-902
11. Schreiber V., Dantzer F., Ame J.C., and de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell. Biol. 7 (2006) 517-528
12. Masutani M., Nakagama H., and Sugimura T. Poly(ADP-ribose) and carcinogenesis. Genes Chromosomes Cancer 38 (2003) 339-348
13. Pirrotta V. Transcription puffing with PARP. Science 299 (2003) 528-529
14. Dantzer F., de La Rubia G., Menissier-De Murcia J., Hostomsky Z., de Murcia G., and Schreiber V. Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry 39 (2000) 7559-7569
15. Parsons J.L., Dianova I.I., Allinson S.L., and Dianov G.L. Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J. 272 (2005) 2012-2021
16. Prasad R., Lavrik O.I., Kim S.J., Kedar P., Yang X.P., Vande Berg B.J., and Wilson S.H. DNA polymerase beta -mediated long patch base excision repair. Poly(ADP-ribose)polymerase-1 stimulates strand displacement DNA synthesis. J. Biol. Chem. 276 (2001) 32411-32414
17. Trucco C., Oliver F.J., de Murcia G., and Menissier-de Murcia J. DNA repair defect in poly(ADP-ribose) polymerase-deficient cell lines. Nucleic Acids Res. 26 (1998) 2644-2649
18. Okano S., Lan L., Caldecott K.W., Mori T., and Yasui A. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell. Biol. 23 (2003) 3974-3981
19. Caldecott K.W., Aoufouchi S., Johnson P., and 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. 24 (1996) 4387-4394
20. Leppard J.B., Dong Z., Mackey Z.B., and Tomkinson A.E. Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell. Biol. 23 (2003) 5919-5927
21. de Murcia J.M., Niedergang C., Trucco C., Ricoul M., Dutrillaux B., Mark M., Oliver F.J., Masson M., Dierich A., LeMeur M., Walztinger C., Chambon P., and de Murcia G. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl. Acad. Sci. USA 94 (1997) 7303-7307
22. Masutani M., Suzuki H., Kamada N., Watanabe M., Ueda O., Nozaki T., Jishage K., Watanabe T., Sugimoto T., Nakagama H., Ochiya T., and Sugimura T. Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. Proc. Natl. Acad. Sci. USA 96 (1999) 2301-2304
23. Wang Z.Q., Auer B., Stingl L., Berghammer H., Haidacher D., Schweiger M., and Wagner E.F. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9 (1995) 509-520
24. Vodenicharov M.D., Sallmann F.R., Satoh M.S., and Poirier G.G. Base excision repair is efficient in cells lacking poly(ADP-ribose) polymerase 1. Nucleic Acids Res. 28 (2000) 3887-3896
25. Virag L. Structure and function of poly(ADP-ribose) polymerase-1: role in oxidative stress-related pathologies. Curr. Vasc. Pharmacol. 3 (2005) 209-214
26. Eliasson M.J., Sampei K., Mandir A.S., Hurn P.D., Traystman R.J., Bao J., Pieper A., Wang Z.Q., Dawson T.M., Snyder S.H., and Dawson V.L. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat. Med. 3 (1997) 1089-1095
27. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., and Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297 (2002) 259-263
28. Shieh W.M., Ame J.C., Wilson M.V., Wang Z.Q., Koh D.W., Jacobson M.K., and Jacobson E.L. Poly(ADP-ribose) polymerase null mouse cells synthesize ADP-ribose polymers. J. Biol. Chem. 273 (1998) 30069-30072
29. Simbulan-Rosenthal C.M., Rosenthal D.S., Luo R., and Smulson M.E. Poly(ADP-ribosyl)ation of p53 during apoptosis in human osteosarcoma cells. Cancer Res. 59 (1999) 2190-2194
30. Wieler S., Gagne J.P., Vaziri H., Poirier G.G., and Benchimol S. Poly(ADP-ribose) polymerase-1 is a positive regulator of the p53-mediated G1 arrest response following ionizing radiation. J. Biol. Chem. 278 (2003) 18914-18921
31. Cistulli C., Lavrik O.I., Prasad R., Hou E., and Wilson S.H. AP endonuclease and poly(ADP-ribose) polymerase-1 interact with the same base excision repair intermediate. DNA Repair (Amst) 3 (2004) 581-591
32. Niimi N., Sugo N., Aratani Y., and Koyama H. Genetic interaction between DNA polymerase beta and DNA-PKcs in embryogenesis and neurogenesis. Cell Death Differ. 12 (2005) 184-191
33. Saleh-Gohari N., Bryant H.E., Schultz N., Parker K.M., Cassel T.N., and Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 25 (2005) 7158-7169
34. Heyer B.S., MacAuley A., Behrendtsen O., and Werb Z. Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev. 14 (2000) 2072-2084
35. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
36. Watanabe F., Fukazawa H., Masutani M., Suzuki H., Teraoka H., Mizutani S., and Uehara Y. Poly(ADP-ribose) polymerase-1 inhibits ATM kinase activity in DNA damage response. Biochem. Biophys. Res. Commun. 319 (2004) 596-602