Parp1 activation in mouse embryonic fibroblasts promotes Pol β-dependent cellular hypersensitivity to alkylation damage

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 686, Issue 1-2, 2010, Pages 57-67

  Jelezcova, Elena ^a   Trivedi, Ram N ^a   Wang, Xiao hong ^a   Tang, Jiang bo ^a,b   Brown, Ashley R ^a   Goellner, Eva M ^a   Schamus, Sandy ^a   Fornsaglio, Jamie L ^a   Sobol, Robert W ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Alkylating agents; Base excision repair; DNA glycosylase; DNA polymerase beta; Parp1; RNAi

Indexed keywords

ALKYLATING AGENT; DNA DIRECTED DNA POLYMERASE BETA; MESYLIC ACID METHYL ESTER; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SHORT HAIRPIN RNA;

ALKYLATION; ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL LINE; CELL SURVIVAL; CHROMOSOME DAMAGE; CONTROLLED STUDY; CYTOTOXICITY; EXCISION REPAIR; FIBROBLAST; IMMUNOBLOTTING; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ALKYLATION; ANIMALS; CELL DEATH; CELL LINE; DNA DAMAGE; DNA POLYMERASE BETA; DNA REPAIR; EMBRYO, MAMMALIAN; FIBROBLASTS; MICE; MICE, KNOCKOUT; POLY(ADP-RIBOSE) POLYMERASES; UP-REGULATION;

EID: 77649184203     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2010.01.016     Document Type: Article

References (75)

1. Almeida K.H., and Sobol R.W. A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair 6 (2007) 695-711
2. 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-β in base-excision repair. Nature 379 (1996) 183-186
3. Beard W.A., and Wilson S.H. Structure and mechanism of DNA polymerase Beta. Chem. Rev. 106 (2006) 361-382
4. Horton J.K., Prasad R., Hou E., and Wilson S.H. Protection against methylation-induced cytotoxicity by DNA polymerase β-dependent long patch base excision repair. J. Biol. Chem. 275 (2000) 2211-2218
5. Fortini P., Pascucci B., Parlanti E., Sobol R.W., Wilson S.H., and Dogliotti E. Different DNA polymerases are involved in the short- and long-patch base excision repair in mammalian cells. Biochemistry 37 (1998) 3575-3580
6. Matsumoto Y., and Kim K. Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair. Science 269 (1995) 699-702
7. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.P., Horton J.K., and Wilson S.H. The lyase activity of the DNA repair protein β-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405 (2000) 807-810
8. Trivedi R.N., Wang X.H., Jelezcova E., Goellner E.M., Tang J., and Sobol R.W. Human methyl purine DNA glycosylase and DNA polymerase β expression collectively predict sensitivity to temozolomide. Mol. Pharmacol. 74 (2008) 505-516
9. Horton J.K., Joyce-Gray D.F., Pachkowski B.F., Swenberg J.A., and Wilson S.H. Hypersensitivity of DNA polymerase beta null mouse fibroblasts reflects accumulation of cytotoxic repair intermediates from site-specific alkyl DNA lesions. DNA Repair (Amst.) 2 (2003) 27-48
10. Price A., and Lindahl T. Enzymatic release of 5′-terminal deoxyribose phosphate residues from damaged DNA in human cells. Biochemistry 30 (1991) 8631-8637
11. Bebenek K., Tissier A., Frank E.G., McDonald J.P., Prasad R., Wilson S.H., Woodgate R., and Kunkel T.A. 5′-Deoxyribose phosphate lyase activity of human DNA polymerase iota in vitro. Science 291 (2001) 2156-2159
12. Prasad R., Bebenek K., Hou E., Shock D.D., Beard W.A., Woodgate R., Kunkel T.A., and Wilson S.H. Localization of the deoxyribose phosphate lyase active site in human DNA polymerase iota by controlled proteolysis. J. Biol. Chem. 278 (2003) 29649-29654
13. Braithwaite E.K., Prasad R., Shock D.D., Hou E.W., Beard W.A., and Wilson S.H. DNA polymerase lambda mediates a back-up base excision repair activity in extracts of mouse embryonic fibroblasts. J. Biol. Chem. 280 (2005) 18469-18475
14. Braithwaite E.K., Kedar P.S., Lan L., Polosina Y.Y., Asagoshi K., Poltoratsky V.P., Horton J.K., Miller H., Teebor G.W., Yasui A., and Wilson S.H. DNA polymerase lambda protects mouse fibroblasts against oxidative DNA damage and is recruited to sites of DNA damage/repair. J. Biol. Chem. 280 (2005) 31641-31647
15. Garcia-Diaz M., Bebenek K., Gao G., Pedersen L.C., London R.E., and Kunkel T.A. Structure-function studies of DNA polymerase lambda. DNA Repair (Amst.) 4 (2005) 1358-1367
16. Garcia-Diaz M., Bebenek K., Kunkel T.A., and Blanco L. Identification of an intrinsic 5′-deoxyribose-5-phosphate lyase activity in human DNA polymerase lambda: a possible role in base excision repair. J. Biol. Chem. 276 (2001) 34659-34663
17. Grin I.R., Khodyreva S.N., Nevinsky G.A., and Zharkov D.O. Deoxyribophosphate lyase activity of mammalian endonuclease VIII-like proteins. FEBS Lett. 580 (2006) 4916-4922
18. Sobol R.W., Kartalou M., Almeida K.H., Joyce D.F., Engelward B.P., Horton J.K., Prasad R., Samson L.D., and Wilson S.H. Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses. J. Biol. Chem. 278 (2003) 39951-39959
19. Ochs K., Sobol R.W., Wilson S.H., and Kaina B. Cells deficient in DNA polymerase β are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res. 59 (1999) 1544-1551
20. Ochs K., Lips J., Profittlich S., and Kaina B. Deficiency in DNA polymerase β provokes replication-dependent apoptosis via DNA breakage, Bcl-2 decline and caspase-3/9 activation. Cancer Res. 62 (2002) 1524-1530
21. Srivastava D.K., Berg B.J., Prasad R., Molina J.T., Beard W.A., Tomkinson A.E., and Wilson S.H. Mammalian abasic site base excision repair. Identification of the reaction sequence and rate-determining steps. J. Biol. Chem. 273 (1998) 21203-21209
22. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis. 2nd ed. (2006), ASM Press, Washington, DC
23. 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
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. Almeida K.H., and Sobol R.W. Increased specificity and efficiency of base excision repair through complex formation. In: Siede W., Doetsch P.W., and Kow Y.W. (Eds). DNA Damage Recognition (2005), Marcel Dekker Inc., New York 33-64
26. Parsons J.L., and Dianov G.L. Monitoring base excision repair proteins on damaged DNA using human cell extracts. Biochem. Soc. Trans. 32 (2004) 962-963
27. 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
28. Lavrik O.I., Prasad R., Sobol R.W., Horton J.K., Ackerman E.J., and Wilson S.H. Photoaffinity labeling of mouse fibroblast enzymes by a base excision repair intermediate. Evidence for the role of poly(ADP-ribose) polymerase-1 in DNA repair. J. Biol. Chem. 276 (2001) 25541-25548
29. 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
30. Dantzer F., Ame J.C., Schreiber V., Nakamura J., Menissier-de Murcia J., and de Murcia G. Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol. 409 (2006) 493-510
31. Zong W.X., Ditsworth D., Bauer D.E., Wang Z.Q., and Thompson C.B. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18 (2004) 1272-1282
32. Trivedi R.N., Almeida K.H., Fornsaglio J.L., Schamus S., and Sobol R.W. The role of base excision repair in the sensitivity and resistance to temozolomide mediated cell death. Cancer Res. 65 (2005) 6394-6400
33. Rubinson D.A., Dillon C.P., Kwiatkowski A.V., Sievers C., Yang L., Kopinja J., Zhang M., McManus M.T., Gertler F.B., Scott M.L., and Van Parijs L. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33 (2003) 401-406
34. Poeschla E.M., Wong-Staal F., and Looney D.J. Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors. Nat. Med. 4 (1998) 354-357
35. Kataoka N., and Dreyfuss G. A simple whole cell lysate system for in vitro splicing reveals a stepwise assembly of the exon-exon junction complex. J. Biol. Chem. 279 (2004) 7009-7013
36. Berridge M.V., and Tan A.S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303 (1993) 474-482
37. Wood R.D., Mitchell M., Sgouros J., and Lindahl T. Human DNA repair genes. Science 291 (2001) 1284-1289
38. Woodhouse B.C., and Dianov G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst.) 7 (2008) 1077-1086
39. 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
40. Ethier C., Labelle Y., and Poirier G.G. PARP-1-induced cell death through inhibition of the MEK/ERK pathway in MNNG-treated HeLa cells. Apoptosis 12 (2007) 2037-2049
41. Paquet-Durand F., Silva J., Talukdar T., Johnson L.E., Azadi S., van Veen T., Ueffing M., Hauck S.M., and Ekstrom P.A. Excessive activation of poly(ADP-ribose) polymerase contributes to inherited photoreceptor degeneration in the retinal degeneration 1 mouse. J. Neurosci. 27 (2007) 10311-10319
42. Iwashita A., Yamazaki S., Mihara K., Hattori K., Yamamoto H., Ishida J., Matsuoka N., and Mutoh S. Neuroprotective effects of a novel poly(ADP-ribose) polymerase-1 inhibitor, 2-[3-[4-(4-chlorophenyl)-1-piperazinyl] propyl]-4(3H)-quinazolinone (FR255595), in an in vitro model of cell death and in mouse 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Pharmacol. Exp. Ther. 309 (2004) 1067-1078
43. Tentori L., and Graziani G. Chemopotentiation by PARP inhibitors in cancer therapy. Pharmacol. Res. 52 (2005) 25-33
44. Horton J.K., Stefanick D.F., Naron J.M., Kedar P.S., and Wilson S.H. Poly(ADP-ribose) polymerase activity prevents signaling pathways for cell cycle arrest following DNA methylating agent exposure. J. Biol. Chem. 280 (2005) 15773-15785
45. Horton J.K., Stefanick D.F., and Wilson S.H. Involvement of poly(ADP-ribose) polymerase activity in regulating Chk1-dependent apoptotic cell death. DNA Repair (Amst.) 4 (2005) 1111-1120
46. Polosina Y.Y., Rosenquist T.A., Grollman A.P., and Miller H. 'Knock down' of DNA polymerase β by RNA interference: recapitulation of null phenotype. DNA Repair (Amst.) 3 (2004) 1469-1474
47. Hassa P.O., Haenni S.S., Elser M., and Hottiger M.O. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going?. Microbiol. Mol. Biol. Rev. 70 (2006) 789-829
48. Beranek D.T. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231 (1990) 11-30
49. Gu H., Marth J.D., Orban P.C., Mossmann H., and Rajewsky K. Deletion of a DNA polymerase β gene segment in T cells using cell type-specific gene targeting. Science 265 (1994) 103-106
50. Casorelli I., Pelosi E., Biffoni M., Cerio A.M., Peschle C., Testa U., and Bignami M. Methylation damage response in hematopoietic progenitor cells. DNA Repair (Amst.) 6 (2007) 1170-1178
51. Kaina B., Christmann M., Naumann S., and Roos W.P. MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst.) 6 (2007) 1079-1099
52. Cohausz O., Blenn C., Malanga M., and Althaus F.R. The roles of poly(ADP-ribose)-metabolizing enzymes in alkylation-induced cell death. Cell. Mol. Life Sci. 65 (2008) 644-655
53. Moubarak R.S., Yuste V.J., Artus C., Bouharrour A., Greer P.A., Menissier-de Murcia J., and Susin S.A. Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol. Cell. Biol. 27 (2007) 4844-4862
54. Kanzawa T., Germano I.M., Komata T., Ito H., Kondo Y., and Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11 (2004) 448-457
55. Meador J.A., Zhao M., Su Y., Narayan G., Geard C.R., and Balajee A.S. Histone H2AX is a critical factor for cellular protection against DNA alkylating agents. Oncogene 27 (2008) 5662-5671
56. Affar el B., Shah R.G., Dallaire A.K., Castonguay V., and Shah G.M. Role of poly(ADP-ribose) polymerase in rapid intracellular acidification induced by alkylating DNA damage. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 245-250
57. Ha H.C., and Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 13978-13982
58. 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
59. Kauppinen T.M., Chan W.Y., Suh S.W., Wiggins A.K., Huang E.J., and Swanson R.A. Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 7136-7141
60. Cohen-Armon M., Visochek L., Rozensal D., Kalal A., Geistrikh I., Klein R., Bendetz-Nezer S., Yao Z., and Seger R. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell 25 (2007) 297-308
61. Russo A.L., Kwon H.C., Burgan W.E., Carter D., Beam K., Weizheng X., Zhang J., Slusher B.S., Chakravarti A., Tofilon P.J., and Camphausen K. In vitro and in vivo radiosensitization of glioblastoma cells by the poly (ADP-ribose) polymerase inhibitor E7016. Clin. Cancer Res. 15 (2009) 607-612
62. Andrabi S.A., Kim N.S., Yu S.W., Wang H., Koh D.W., Sasaki M., Klaus J.A., Otsuka T., Zhang Z., Koehler R.C., Hurn P.D., Poirier G.G., Dawson V.L., and Dawson T.M. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 18308-18313
63. 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
64. Endres M., Wang Z.Q., Namura S., Waeber C., and Moskowitz M.A. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J. Cereb. Blood Flow Metab. 17 (1997) 1143-1151
65. Fiorillo C., Ponziani V., Giannini L., Cecchi C., Celli A., Nassi N., Lanzilao L., Caporale R., and Nassi P. Protective effects of the PARP-1 inhibitor PJ34 in hypoxic-reoxygenated cardiomyoblasts. Cell. Mol. Life Sci. 63 (2006) 3061-3071
66. Oh K.S., Lee S., Yi K.Y., Seo H.W., Koo H.N., and Lee B.H. A novel and orally active poly (ADP-ribose) polymerase-1 inhibitor, 2-[methoxycarbonyl(4-methoxyphenyl)methyl sulfanyl]-1H-benzimidazole-4-carboxylic acid amide (KR-33889), attenuates injury in in vitro model of cell death and in vivo model of cardiac ischemia. J. Pharmacol. Exp. Ther. (2008)
67. Pillai J.B., Gupta M., Rajamohan S.B., Lang R., Raman J., and Gupta M.P. Poly(ADP-ribose) polymerase-1-deficient mice are protected from angiotensin II-induced cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 291 (2006) H1545-1553
68. Pillai J.B., Isbatan A., Imai S., and Gupta M.P. Poly(ADP-ribose) polymerase-1-dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced Sir2alpha deacetylase activity. J. Biol. Chem. 280 (2005) 43121-43130
69. Yang K.T., Chang W.L., Yang P.C., Chien C.L., Lai M.S., Su M.J., and Wu M.L. Activation of the transient receptor potential M2 channel and poly(ADP-ribose) polymerase is involved in oxidative stress-induced cardiomyocyte death. Cell Death Differ. 13 (2006) 1815-1826
70. Liu X., Shi Y., Guan R., Donawho C., Luo Y., Palma J., Zhu G.D., Johnson E.F., Rodriguez L.E., Ghoreishi-Haack N., Jarvis K., Hradil V.P., Colon-Lopez M., Cox B.F., Klinghofer V., Penning T., Rosenberg S.H., Frost D., Giranda V.L., and Luo Y. Potentiation of temozolomide cytotoxicity by poly(ADP)ribose polymerase inhibitor ABT-888 requires a conversion of single-stranded DNA damages to double-stranded DNA breaks. Mol. Cancer Res. 6 (2008) 1621-1629
71. Haince J.F., Rouleau M., Hendzel M.J., Masson J.Y., and Poirier G.G. Targeting poly(ADP-ribosyl)ation: a promising approach in cancer therapy. Trends Mol. Med. 11 (2005) 456-463
72. Miknyoczki S.J., Jones-Bolin S., Pritchard S., Hunter K., Zhao H., Wan W., Ator M., Bihovsky R., Hudkins R., Chatterjee S., Klein-Szanto A., Dionne C., and Ruggeri B. Chemopotentiation of temozolomide, irinotecan, and cisplatin activity by CEP-6800, a poly(ADP-ribose) polymerase inhibitor. Mol. Cancer Ther. 2 (2003) 371-382
73. El-Khamisy S.F., Masutani M., Suzuki H., and Caldecott K.W. A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucl. Acids Res. 31 (2003) 5526-5533
74. Mortusewicz O., Ame J.C., Schreiber V., and Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucl. Acids Res. 35 (2007) 7665-7675
75. Helleday T., Petermann E., Lundin C., Hodgson B., and Sharma R.A. DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8 (2008) 193-204