ASCIZ regulates lesion-specific Rad51 focus formation and apoptosis after methylating DNA damage

EMBO Journal

Volumn 24, Issue 13, 2005, Pages 2447-2457

  McNees, Carolyn J ^a,b   Conlan, Lindus A ^a   Tenis, Nora ^a   Heierhorst, Jörg ^a,b  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

FHA domain; KIAA0431; MMS; MNNG; Oxidative damage

Indexed keywords

DNA; PROTEIN ASCIZ; PROTEIN MLH1; RAD51 PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA METHYLATION; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; IONIZING RADIATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; SISTER CHROMATID;

APOPTOSIS; BASE PAIR MISMATCH; CARRIER PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; SIGNAL TRANSDUCTION;

EID: 22744456546     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600704     Document Type: Article

References (46)

1. Adamson AW, Kim WJ, Shangary S, Baskaran R, Brown KD (2002) ATM is activated in response to N-methyl-N′-nitro-N-nitrosoguanidine-induced DNA alkylation. J Biol Chem 277: 38222-38229
2. Barnes DE, Lindahl T (2004) Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu Rev Genet 38: 445-476
3. Bednarek AK, Keck-Waggoner CL, Daniel RL, Laflin KJ, Bergsagel PL, Kiguchi K, Brenner AJ, Aldaz CM (2001) WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res 61: 8068-8073
4. Bishop DK, Ear U, Bhattacharyya A, Calderone C, Beckett M, Weichselbaum RR, Shinohara A (1998) Xrcc3 is required for assembly of Rad51 complexes m vivo. J Biol Chem 273: 21482-21488
5. Chen CF, Chen PL, Zhong Q, Sharp ZD, Lee WH (1999) Expression of BRC repeats in breast cancer cells disrupts the BRCA2-Rad51 complex and leads to radiation hypersensitivity and loss of G(2)/ M checkpoint control. J Biol Chem 274: 32931-32935
6. Cline SD, Hanawalt PC (2003) Who's on first in the cellular response to DNA damage? Nat Rev Mol Cell Biol 4: 361-372
7. Conlan LA, McNees CJ, Heierhorst J (2004) Proteasome-dependent dispersal of PML nuclear bodies in response to alkylating DNA damage. Oncogene 23: 307-310
8. D'Andrea AD, Grompe M (2003) The Fanconi anaemia/BRCA pathway. Nat Rev Cancer 3: 23-34
9. Du X-J, Cole TJ, Tenis N, Gao X-M, Köntgen F, Kemp BE, Heierhorst J (2002) Impaired cardiac contractility response to hemodynamic stress in S100A1-deficient mice. Mol Cell Biol 22: 2821-2829
10. Durocher D, Jackson SP (2002) The FHA domain. FEBS Lett 513: 58-66
11. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498
12. Glaab WE, Risinger JI, Umar A, Barrett JC, Kunkel TA, Tindall KR (1998) Cellular resistance and hypermutability in mismatch repair-deficient human cancer cells following treatment with methyl methanesulfonate. Mutat Res 398: 197-207
13. Glaab WE, Tindall KR, Skopek TR (1999) Specificity of mutations induced by methyl methanesulfonate in mismatch repair-deficient human cancer cells. Mutation Res 427: 67-78
14. Hammet A, Pike BL, McNees CJ, Conlan LA, Tenis N, Heierhorst J (2003) FHA domains as phospho-threonine binding modules in cell signaling. IUBMB Life 55: 23-27
15. Hatanaka A, Yamazoe M, Sale JE, Takata M, Yamamoto K, Kitao H, Sonoda E, Kikuchi K, Yonetani Y, Takeda S (2005) Similar effects of Brca2 truncation and Rad51 paralog deficiency on immunoglubulin V gene diversification in DT40 cells support an early role for Rad51 paralogs in homologous recombination. Mol Cell Biol 25: 1124-1134
16. Henry-Mowatt J, Jackson D, Masson JY, Johnson PA, Clements PM, Benson FE, Thompson LH, Takeda S, West SC, Caldecott KW (2003) XRCC3 and Rad51 modulate replication fork progression on damaged vertebrate chromosomes. Mol Cell 11: 1109-1117
17. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, Haber JE, Foiani M (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431: 1011-1017
18. Ishikawa K, Nagase T, Nakajima D, Seki N, Ohira M, Miyajima N, Tanaka A, Kotani H, Nomura N, Ohara O (1997) Prediction of the coding sequences of unidentified human genes. VIII. 78 new cDNA clones from brain which code for large proteins in vitro. DNA Res 4: 307-313
19. Jager AC, Rasmussen M, Bisgaard HC, Singh KK, Nielsen FC, Rasmussen LJ (2001) HNPCC mutations in the human DNA mismatch repair gene hMLH1 influence assembly of hMutLalpha and hMLH1-hEXO1 complexes. Oncogene 20: 3590-3595
20. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432: 316-323
21. Li MJ, Maizels N (1997) Nuclear Rad51 foci induced by DNA damage are distinct from Rad51 foci associated with B cell activation and recombination. Exp Cell Res 237: 93-100
22. Li Z, Woo CJ, Iglesias-Ussel MD, Ronai D, Scharff MD (2004) The generation of antibody diversity through somatic hypermutation and class switch recombination. Genes Dev 18: 1-11
23. Lisby M, Barlow JH, Burgess RC, Rothstein R (2004) Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118: 699-713
24. Lisby M, Mortensen UH, Rothstein R (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572-577
25. Liu L, Yan L, Donze JR, Gerson SL (2003) Blockage of abasic site repair enhances antitumor efficacy of 1,3-bis-(2-chloroethyl)-1-nitrosourea in colon tumor xenografts. Mol Cancer Ther 2: 1061-1066
26. Matsuoka S, Huang M, Elledge SJ (1998) Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282: 1893-1897
27. Mirzoeva OK, Petrini JHJ (2001) DNA damage-dependent nuclear dynamics of the Mrell complex. Mol Cell Biol 21: 281-288
28. Morimatsu K, Kowalczykowski SC (2003) RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol Cell 11: 1337-1347
29. O'Regan P, Wilson C, Townsend S, Thacker J (2001) XRCC2 is a nuclear RAD51-like protein required for damage-dependent RAD51 focus formation without the need for ATP binding. J Biol Chem 276: 22148-22153
30. Paull TT, Rogaku EP, Yamazaki V, Kirchgessner CU, Geliert 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
31. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J (2003) Diverse but overlapping functions of the two forkhead-associated (FHA) domains in Rad53 checkpoint kinase activation. J Biol Chem 278: 30421-30424
32. Pike BL, Yongkiettrakul S, Tsai MD, Heierhorst J (2004) Mdt1, a novel Rad53 FHA1 domain-interacting protein, modulates DNA damage tolerance and G2/M cell cycle progression in Saccharomyces cerevisiae. Mol Cell Biol 24: 2779-2788
33. Rada C, Di Noia JM, Neuberger MS (2004) Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 16: 163-171
34. Raderschall E, Golub EI, Haaf T (1999) Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc Natl Acad Sci USA 96: 1921-1926
35. Richardson C, Jasin M (2000) Recombination between two chromosomes: implications for genomic integrity in mammalian cells. Cold Spring Harb Symp Quant Biol 65: 553-560
36. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, Feunteun J, Livingston DM (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90: 425-435
37. Stojic L, Mojas N, Cejka P, Di Pietro M, Ferrari S, Marra G, Jiricny J (2004) Mismatch repair-dependent G2 checkpoint induced by low doses of SN1 type methylating agents requires the ATR kinase. Genes Dev 18: 1331-1344
38. Sung P, Krejci L, Van Komen S, Sehorn MG (2003) Rad51 recombinase and recombination mediators. J Biol Chem 278: 42729-42732
39. Takata M, Sasaki MS, Tachiiri S, Fukushima T, Sonoda E, Schild D, Thompson LH, Takeda S (2001) Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol Cell Biol 21: 2858-2866
40. Tarsounas M, Davies D, West SC (2003) BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22: 1115-1123
41. Tindall KR, Glaab WE, Umar A, Risinger JI, Koi M, Barrett JC, Kunkel TA (1998) Complementation of mismatch repair gene defects by chromosome transfer. Mutat Res 402: 15-22
42. Traven A, Heierhorst J (2005) SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. BioEssays 27: 397-407
43. Wang Y, Qin J (2003) MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNA methylation. Proc Natl Acad Sci USA 100: 15387-15392
44. West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 4: 435-445
45. Yu VP, Koehler M, Steinlein C, Schmid M, Hanakahi LA, van Gool AJ, West SC, Venkitaraman AR (2000) Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev 14: 1400-1406
46. Yuan SS, Lee SY, Chen G, Song M, Tomlinson GE, Lee EY (1999) BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex m vivo. Cancer Res 59: 3547-3551