Targeting of Rad51-dependent homologous recombination: Implications for the radiation sensitivity of human lung cancer cell lines

British Journal of Cancer

Volumn 92, Issue 6, 2005, Pages 1089-1097

  Sak, A ^a   Stueben, G ^a   Groneberg, M ^a   Bocker W ^a   Stuschke, M ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

DNA double strand break repair apoptosis; H2AX; Lung cancer; p53; Rad51

Indexed keywords

DOUBLE STRANDED DNA; GENE PRODUCT; PROTEIN GAMMA H2AX; RAD51 PROTEIN; UNCLASSIFIED DRUG; ANTISENSE OLIGONUCLEOTIDE; DNA BINDING PROTEIN; PROTEIN P53; RAD51 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DNA STRAND BREAKAGE; DOSE TIME EFFECT RELATION; DOWN REGULATION; GENE TARGETING; GENETIC TRANSFECTION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; LUNG NON SMALL CELL CANCER; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RADIATION DOSE; RADIOSENSITIVITY; DNA REPAIR; GENETIC RECOMBINATION; GENETICS; LUNG TUMOR; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; LUNG NEOPLASMS; OLIGONUCLEOTIDES, ANTISENSE; RAD51 RECOMBINASE; RADIATION TOLERANCE; RECOMBINATION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 17444402057     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjc.6602457     Document Type: Article

References (48)

1. Allen C, Halbrook J, Nickoloff JA (2003) Interactive competition between homologous recombination and non-homologous end joining. Mol Cancer Res 1: 913-920
2. Banath JP, MacPhail SH, Olive PL (2004) Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res 64: 7144-7149
3. Bertrand P, Lambert S, Joubert C, Lopez BS (2003) Overexpression of mammalian Rad51 does not stimulate tumorigenesis while a dominant-negative Rad51 affects centrosome fragmentation, ploidy and stimulates tumorigenesis, in p53-defective CHO cells. Oncogene 22: 7587-7592
4. Bishop DK, Ear U, Bhattacharyya A, Calderone C, Beckett M, Weichselbaum RR, Shinohara A (1998) Xrcc3 is required for assembly of Rad51 complexes in vivo. J Biol Chem 273: 21482-21488
5. Burgess TL, Fisher EF, Ross SL, Bready JV, Qian YX, Bayewitch LA, Cohen AM, Herrera CJ, Hu SS, Kramer TB, Lott FD, Martin FH, Pierce GF, Simonet L, Farrell CL (1995) The antiproliferative activity of c-myb and c-myc antisense oligonucleotides in smooth muscle cells is caused by a nonantisense mechanism. Proc Natl Acad Sci USA 92: 4051-4055
6. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1674-1677
7. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5: 675-679
8. Chen G, Yuan SS, Liu W, Xu Y, Trujillo K, Song B, Cong F, Goff SP, Wu Y, Arlinghaus R, Baltimore D, Gasser PJ, Park MS, Sung P, Lee EY (1999) Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J Biol Chem 274: 12748-12752
9. Collis SJ, Tighe A, Scott SD, Roberts SA, Hendry JH, Margison GP (2001) Ribozyme minigene-mediated RAD51 down-regulation increases radiosensitivity of human prostate cancer cells. Nucleic Acids Res 29: 1534-1538
10. Cortez D, Wang Y, Qin J, Elledge SJ (1999) Requirement of ATM-dependent phosphorylation of brca 1 in the DNA damage response to double-strand breaks. Science 286: 1162-1166
11. Delacote F, Han M, Stamato TD, Jasin M, Lopez BS (2002) An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res 30: 3454-3463
12. Flygare J, Benson F, Hellgren D (1996) Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes. Biochim Biophys Acta 1312: 231-236
13. Golub EI, Gupta RC, Haaf T, Wold MS, Radding CM (1998) Interaction of human rad51 recombination protein with single-stranded DNA binding protein, RPA. Nucleic Acids Res 26: 5388-5393
14. Grandy I, Hardt T, Schmid M, Haaf T (2002) Effects of higher-order nuclear structure and Rad51 overexpression on radiation-induced chromosome rearrangements. Cytogenet Genome Res 98: 265-269
15. Gupta RC, Golub EI, Wold MS, Radding CM (1998) Polarity of DNA strand exchange promoted by recombination proteins of the RecA family. Proc Natl Acad Sci USA 95: 9843-9848
16. Haaf T, Golub EI, Reddy G, Radding CM, Ward DC (1995) Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 92: 2298-2302
17. Iotsova V, Stehelin D (1995) Antisense p53 provokes changes in HeLa cell growth and morphology. Eur J Cell Biol 68: 122-132
18. Izzard RA, Jackson SP, Smith GC (1999) Competitive and noncompetitive inhibition of the DNA-dependent protein kinase. Cancer Res 59: 2581-2586
19. Johnson RD, Jasin M (2001) Double-strand-break-induced homologous recombination in mammalian cells. Biochem Soc Trans 29: 196-201
20. Kanaar R, Hoeijmakers JHJ, vanGent DC (1998) Molecular mechanism of DNA double-strand break repair. Trends Cell Biol 8: 483-489
21. Kumari A, Schultz N, Helleday T (2004) p53 protects from replication-associated DNA double-strand breaks in mammalian cells. Oncogene 23: 2324-2329
22. Lambert S, Lopez BS (2001) Role of RAD51 in sister-chromatid exchanges in mammalian cells. Oncogene 20: 6627-6631
23. Leuther KK, Hammersten O, Kornberg RD, Chu G (1999) Structure of DNA-dependent protein kinase: implications for its regulation by DNA. EMBO J 18: 1114-1123
24. Linke SP, Sengupta S, Khabie N, Jeffries BA, Buchhop S, Miska S, Henning W, Pedeux R, Wang XW, Hofseth LJ, Yang Q, Garfield SH, Sturzbecher HW, Harris CC (2003) p53 interacts with hRAD51 and hRAD54, and directly modulates homologous recombination. Cancer Res 63: 2596-2605
25. Liu Y, Li M, Lee EY, Maizels N (1999) Localization and dynamic relocalization of mammalian Rad52 during the cell cycle and in response to DNA damage. Curr Biol 9: 975-978
26. Ohnishi T, Taki T, Hiraga S, Arita N, Morita T (1998) In vitro and in vivo potentiation of radiosensitivity of malignant gliomas by antisense inhibition of the RAD51 gene. Biochem Biophys Res Commun 245: 319-324
27. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, 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
28. Raderschall E, Bazarov A, Cao J, Lurz R, Smith A, Mann W, Ropers HH, Sedivy JM, Golub EI, Fritz E, Haaf T (2002a) Formation of higher-order nuclear Rad51 structures is functionally linked to p21 expression and protection from DNA damage-induced apoptosis. J Cell Sci 115: 153-164
29. Raderschall E, Stout K, Freier S, Suckow V, Schweiger S, Haaf T (2002b) Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res 62: 219-225
30. Russell JS, Brady K, Burgan WE, Cerra MA, Oswald KA, Camphausen K, Tofilon PJ (2003) Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity. Cancer Res 63: 7377-7383
31. Sak A, Stuschke M, Wurm R, Schroeder G, Sinn B, Wolf G, Budach V (2002) Selective inactivation of DNA-dependent protein kinase with antisense oligodeoxynucleotides: consequences for the rejoining of radiation-induced DNA double-strand breaks and radiosensitivity of human cancer cell lines. Cancer Res 62: 6621-6624
32. Sak A, Wurm R, Elo B, Grehl S, Pottgen C, Stuben G, Sinn B, Wolf G, Budach V, Stuschke M (2003) Increased radiation-induced apoptosis and altered cell cycle progression of human lung cancer cell lines by antisense oligodeoxynucleotides targeting p53 and p21(WAF1/CIP1). Cancer Gene Ther 10: 926-934
33. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, Abraham RT (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 58: 4375-4382
34. Shinohara A, Ogawa H, Matsuda Y, Ushio N, Ikeo K, Ogawa T (1993) Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat Genet 3: 239-243
35. Smith GCM, Jackson SP (1999) The DNA-dependent protein kinase. Genes Dev 13: 916-934
36. Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A, Ogawa H, Takata M, Yamaguchi-Iwai Y, Takeda S (1998) Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 17: 598-608
37. Sonoda E, Takata M, Yamashita YM, Morrison C, Takeda S (2001) Homologous DNA recombination in vertebrate cells. Proc Natl Acad Sci USA 98: 8388-8394
38. Stuschke M, Sak A, Wurm R, Sinn B, Wolf G, Stuben G, Budach V (2002) Radiation induced apoptosis in human non-small-cell lung cancer cell lines is secondary to cell-cycle progression beyond the G2-phase checkpoint. Int J Radiat Biol 78: 807-819
39. Taki T, Ohnishi T, Yamamoto A, Hiraga S, Arita N, Izumoto S, Hayakawa T, Morita T (1996) Antisense inhibition of the RAD51 enhances radiosensitivity. Biochem Biophys Res Commun 223: 434-438
40. Tan TL, Essers J, Citterio E, Swagemakers SM, de Wit J, Benson FE, Hoeijmakers JH, Kanaar R (1999) Mouse Rad54 affects DNA conformation and DNA-damage-induced Rad51 foci formation. Curr Biol 9: 325-328
41. Tashiro S, Kotomura N, Shinohara A, Tanaka K, Ueda K, Kamada N (1996) S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12: 2165-2170
42. Tsuzuki T, Fujii Y, Sakumi K, Tominaga Y, Nakao K, Sekiguchi M, Matsushiro A, Yoshimura Y, Morita T (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc Natl Acad Sci USA 93: 6236-6240
43. van Gent DC, Hoeijmakers JH, Kanaar R (2001) Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet 2: 196-206
44. Vispe S, Cazaux C, Lesca C, Defais M (1998) Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res 26: 2859-2864
45. Wang H, Zeng ZC, Bui TA, Sonoda E, Takata M, Takeda S, Iliakis G (2001) Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group. Oncogene 20: 2212-2224
46. Xia SJ, Shammas MA, Shmookler Reis RJ (1997) Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol Cell Biol 17: 7151-7158
47. Yamamoto A, Taki T, Yagi H, Habu T, Yoshida K, Yoshimura Y, Yamamoto K, Matsushiro A, Nishimune Y, Morita T (1996) Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol Gen Genet 251: 1-12
48. Yuan SS, Chang HL, Lee EY (2003) Ionizing radiation-induced Rad51 nuclear focus formation is cell cycle-regulated and defective in both ATM(-/-) and c-Abl(-/-) cells. Mutat Res 525: 85-92