Base excision repair proteins are required for integrin-mediated suppression of bleomycin-induced DNA breakage in murine lung endothelial cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 321, Issue 1, 2007, Pages 318-326

  Rose, Jane L ^a,c   Reeves, Kevin C ^a   Likhotvorik, Rostislav I ^a   Hoyt, Dale G ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE EXCISION REPAIR PROTEIN; BETA1 INTEGRIN ANTIBODY; BLEOMYCIN; DNA LIGASE 3 ALPHA; HISTONE; INTEGRIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NUCLEIC ACID BINDING PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN ANTIBODY; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHINESE HAMSTER; CONTROLLED STUDY; DNA STRAND BREAKAGE; ENDOTHELIUM CELL; EXCISION REPAIR; LUNG ENDOTHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BLEOMYCIN; BLOTTING, WESTERN; CELL SURVIVAL; DNA DAMAGE; DNA LIGASES; DNA REPAIR; DNA-BINDING PROTEINS; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GREEN FLUORESCENT PROTEINS; HISTONES; IN SITU NICK-END LABELING; INTEGRINS; LUNG; MICE; POLY(ADP-RIBOSE) POLYMERASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING;

EID: 33947416923     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.106.113498     Document Type: Article

References (40)

1. Audebert M, Salles B, and Calsou P (2004) Involvement of PARP-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 279:55117-55126.
2. Audebert M, Salles B, Weinfeld M, and Calsou P (2006) Involvement of polynucleotide kinase in a poly(ADP-ribose) polymerase-1-dependent DNA double-strand breaks rejoining pathway. J Mol Biol 356:257-265.
3. Banath JP and Olive PL (2003) Expression of phosphorylated histone H2AX as a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res 63:4347-4350.
4. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, and Christman MF (2002) Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature (Lond) 419:411-415.
5. Caldecott KW (2003) XRCC1 and DNA strand break repair. DNA Repair (Amst) 2:955-969.
6. Caldecott KW, McKeown CK, Tucker JD, Ljungquist S, and Thompson LH (1994) An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol Cell Biol 14:68-76.
7. Chen J and Stubbe J (2005) Bleomycins: towards better therapeutics. Nat Rev Cancer 5:102-112.
8. Dianova II, Sleeth KM, Allinson SL, Parsons JL, Breslin C, Caldecott KW, and Dianov GL (2004) XRCC1-DNA polymerase beta interaction is required for efficient base excision repair. Nucleic Acids Res 32:2550-2555.
9. Drouet J, Delteil C, Lefrancois J, Concannon P, Salles B, and Calsou P (2005) DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J Biol Chem 280:7060-7069.
10. Fan J and Wilson DM, 3rd (2005) Protein-protein interactions and posttranslational modifications in mammalian base excision repair. Free Radic Biol Med 38:1121-1138.
11. Fernandes N, Sun Y, Chen S, Paul P, Shaw RJ, Cantley LC, and Price BD (2005) DNA damage-induced association of ATM with its target proteins requires a protein interaction domain in the N terminus of ATM. J Biol Chem 280:15158-15164.
12. Fernandez-Capetillo O, Lee A, Nussenzweig M, and Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair (Amst) 3:959-967.
13. Gerritsen ME, Shen CP, McHugh MC, Atkinson WJ, Kiely JM, Milstone DS, Luscinskas FW, and Gimbrone MA Jr (1995) Activation-dependent isolation and culture of murine pulmonary microvascular endothelium. Microcirculation 2:151-163.
14. Gorczyca W, Gong J, and Darzynkiewicz Z (1993) Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res 53:1945-1951.
15. Hoyt DG, Rizzo M, Gerritsen ME, Pitt BR, and Lazo JS (1997) Integrin activation protects pulmonary endothelial cells from the genotoxic effects of bleomycin. Am J Physiol 273:L612-L617.
16. Hoyt DG, Rusnak JM, Mannix RJ, Modzelewski RA, Johnson CS, and Lazo JS (1996) Integrin activation suppresses etoposide-induced DNA strand breakage in cultured murine tumor-derived endothelial cells. Cancer Res 56:4146-4149.
17. Huang H, McIntosh JL, Fang L, Szabo C, and Hoyt DG (2003) Integrin-mediated suppression of endotoxin-induced DNA damage in lung endothelial cells is sensitive to poly(ADP-ribose) polymerase-1 gene deletion. Int J Mol Med 12:533-540.
18. Iliakis G, Wang H, Perrault AR, Boecker W, Rosidi B, Windhofer F, Wu W, Guan J, Terzoudi G, and Pantelias G (2004) Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res 104:14-20.
19. Jones CB, McIntosh J, Huang H, Graytock A, and Hoyt DG (2001) Regulation of bleomycin-induced DNA breakage and chromatin structure in lung endothelial cells by integrins and poly(ADP-ribose) polymerase. Mol Pharmacol 59:69-75.
20. Juliano RL (2002) Signal transduction by cell adhesion receptors and the cytoskeleton: functions of integrins, cadherins, selectins, and immunoglobulin-superfamily members. Annu Rev Pharmacol Toxicol 42:283-323.
21. Leppard JB, Dong Z, Mackey ZB, and Tomkinson AE (2003) Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol Cell Biol 23:5919-5927.
22. Levy N, Martz A, Bresson A, Spenlehauer C, de Murcia G, and Menissier-de Murcia J (2006) XRCC1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res 34:32-41.
23. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, and de Murcia G (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 18:3563-3571.
24. Meredith JE Jr, Fazeli B, and Schwartz MA (1993) The extracellular matrix as a cell survival factor. Mol Biol Cell 4:953-961.
25. Mortusewicz O, Rothbauer U, Cardoso MC, and Leonhardt H (2006) Differential recruitment of DNA Ligase I and III to DNA repair sites. Nucleic Acids Res 34:3523-3532.
26. Nazarov IB, Smirnova AN, Krutilina RI, Svetlova MP, Solovjeva LV, Nikiforov AA, Oei SL, Zalenskaya IA, Yau PM, Bradbury EM, et al. (2003) Dephosphorylation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its inhibition by calyculin A. Radiat Res 160:309-317.
27. Nocentini S (1999) Rejoining kinetics of DNA single- and double-strand breaks in normal and DNA ligase-deficient cells after exposure to ultraviolet C and gamma radiation: an evaluation of ligating activities involved in different DNA repair processes. Radiat Res 151:423-432.
28. Oei SL and Ziegler M (2000) ATP for the DNA ligation step in base excision repair is generated from poly(ADP-ribose). J Biol Chem 275:23234-23239.
29. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, and Bonner WM (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10:886-895.
30. Petermann E, Keil C, and Oei SL (2006) Roles of DNA ligase III and XRCC1 in regulating the switch between short patch and long patch BER. DNA Repair (Amst) 5:544-555.
31. Peterson CL and Cote J (2004) Cellular machineries for chromosomal DNA repair. Genes Dev 18:602-616.
32. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, and Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868.
33. Rose J, Huang H, Wray S, and Hoyt D (2005) Integrin engagement increases histone H3 acetylation and reduces histone H1 association with DNA in murine lung endothelial cells. Mol Pharmacol 68:439-446.
34. Schwartz JL, Giovanazzi S, and Weichselbaum RR (1987) Recovery from sublethal and potentially lethal damage in an X-ray-sensitive CHO cell. Radiat Res 111:58-67.
35. Snedecor G and Cochran W (1980) Statistical Methods, Iowa State University Press, Ames, IA.
36. Stupack DG, Puente XS, Boutsaboualoy S, Storgard CM, and Cheresh DA (2001) Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J Cell Biol 155:459-470.
37. Valerie K and Povirk LF (2003) Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22:5792-5812.
38. Verger A and Crossley M (2004) Chromatin modifiers in transcription and DNA repair. Cell Mol Life Sci 61:2154-2162.
39. Wang H, Rosidi B, Perrault R, Wang M, Zhang L, Windhofer F, and Iliakis G (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res 65:4020-4030.
40. Weterings E and van Gent DC (2004) The mechanism of non-homologous endjoining: a synopsis of synapsis. DNA Repair (Amst) 3:1425-1435.