Sequestration of mammalian Rad51-recombination protein into micronuclei

Journal of Cell Biology

Volumn 144, Issue 1, 1999, Pages 11-20

  Haaf, Thomas ^a   Raderschall, Elke ^a   Reddy, Gurucharan ^b   Ward, David C ^c   Radding, Charles M ^c   Golub, Efim I ^c  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b Pangene Inc   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA repair; Immunofluorescence; Micronuclei; Rad51; Repairosome

Indexed keywords

BROXURIDINE; DEMECOLCINE; DNA TOPOISOMERASE (ATP HYDROLYSING); GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; PROTEIN RAD 51; PROTEIN RAD 52; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RECOMBINANT DNA TECHNOLOGY;

3T3 CELLS; ANIMALS; CELL CYCLE; CELL LINE, TRANSFORMED; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; MICE; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MUTAGENS; RAD51 RECOMBINASE; RATS; RECOMBINANT FUSION PROTEINS; REPLICATION PROTEIN A;

ANIMALIA; MAMMALIA;

EID: 0033545207     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.1.11     Document Type: Article

References (61)

1. Albala, J.S., M.P. Thelen, C. Prange, W. Fan, M. Christensen, L.H. Thompson, and G.G. Lennon. 1997. Identification of a novel human RAD51 homolog, RAD51B. Genomics. 46:476-479.
2. Baumann, P., F.E. Benson, and S.C. West. 1996. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 87:757-766.
3. Benson, F.E., A. Stasiak, and S.C. West. 1994. Purification and characterisation of the human Rad51 protein, an analogue of E. coli RecA. EMBO (Eur. Mol. Biol. Organ.) J. 13:5764-5771.
4. Benson, F.E., P. Baumann, and S.C. West. 1998. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature. 391:401-404.
5. Bregman, D.B., L. Du, S. van der Zee, and S.L. Warren. 1995. Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129:287-298.
6. Cartwright, R., A.M. Dunn, P.J. Simpson, C.E. Tambini, and J. Thacker. 1998. Isolation of novel human and mouse genes of the recA/Rad51 recombination-repair gene family. Nucleic Acids Res. 26:1653-1659.
7. Dosanjh, M.K., D.W. Collins, W. Fan, G.G. Lennon, J.S. Albala, Z. Shen, and D. Schild. 1998. Isolation and characterization of RAD5IC, a new human member of the RAD51 family of related genes. Nucleic Acids Res. 5:1179-1184.
8. Flygare, J., R.C. Armstrong, A. Wennborg, S. Orsan, and D. Hellgren. 1998. Proteolytic cleavage of HsRad51 during apoptosis. FEBS (Fed. Eur. Biochem. Soc.) Lett. 427:247-251.
9. Friedberg, E.C., W. Siede, and A.J. Cooper. 1991. Cellular responses to DNA damage in yeast. In The Molecular Biology and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics. J. Pringle and E. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 147-192.
10. Game, J.C. 1993. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin. Cancer Biol. 4:73-83.
11. Gasior, S.L., A.W. Wong, Y. Kora, A. Shinohara, and D.K. Bishop. 1998. Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes. Dev. 12:2208-2221.
12. Golub, E.I., O.V. Kovalenko, R.C. Gupta, D.C. Ward, and C.M. Radding. 1997. Interaction of human recombination proteins Rad51 and Rad54. Nucleic Acids Res. 25:4106-4110.
13. Golub, E.I., R.C. Gupta, T. Haaf, M.S. Wold, and C.M. Radding. 1998. Interaction of human Rad51 recombination protein with single-stranded DNA binding protein. RPA. Nucleic Acids Res. 26:5388-5393.
14. Gupta, R.C., L.R. Bazemore, E.I. Golub, and C.M. Radding. 1997. Activities of human recombination protein Rad51. Proc. Natl. Acad. Sci. USA. 94:463-468.
15. Gupta, R.C., E.I. Golub, M.S. Wold, and C.R. Radding. 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., and M. Schmid. 1989. Centromeric association and non-random distribution of centromeres in human tumour cells. Hum. Genet. 81:137-143.
17. Haaf, T., D.L. Hayman, and M. Schmid. 1991. Quantitative determination of rDNA transcription units in vertebrate cells. Exp. Cell Res. 193:78-86.
18. Haaf, T., E.I. Golub, G. Reddy, C.M. Radding, and D.C. Ward. 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.
19. Habu, T., T. Taki, A. West, Y. Nishimune, and T. Morita. 1996. The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcripts in meiosis. Nucleic Acids Res. 24:470-477.
20. Hahnfeldt, P., and L.R. Hlatky. 1994. A Monte Carlo/Markov chain model for the association of data for chromosome aberrations and formation of micronuclei. Radiation Res. 138:239-245.
21. Heddle, J.A., M.C. Cimino, M. Hayashi, F. Romagna, M.D. Shelby, J.D. Tucker, P. Vanparys, and J.T. MacGregor. 1991. Micronuclei as an index of cytogenetic damage: past, present, and future. Environ. Mol. Mutagenesis. 18:277-291.
22. Heyer, W.D. 1994. The search for the right partner: homologous pairing and DNA strand exchange proteins in eukaryotes. Experientia. 50:223-233.
23. Jones C.J., and R.D. Wood. 1993. Preferential binding of the Xeroderma pigmentosum group A complementing protein to damaged DNA. Biochemistry. 32:12096-12104.
24. Kaufmann, S.H. 1989. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49:5870-5878.
25. Kovalenko, O.V., A.W. Plug, T. Haaf, D.K. Gonda, T. Ashley, D.C. Ward, C.M. Radding, and E.I. Golub. 1996. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptoncmal complexes. Proc. Natl. Acad. Sci. USA. 93:2958-2963.
26. Liang, F., M. Han, P.J. Romanienko, and M. Jasin, 1998. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA. 95:5172-5177.
27. Lim, D.-S., and P. Hasty. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16: 7133-7143.
28. Liu, N., J.E. Lamerdin, R.S. Tebbs, D. Schild, J.D. Tucker, M.R. Shen, K.W. Brookman, M.J. Siciliano, C.A. Walter, W. Fan, L.S. Narayana, Z.-Q. Zhou, A.W. Adamson, K.J. Sorensen, D.J. Chen, N.J. Jones, and L.H. Thompson. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell. 1:783-794.
29. Maldonado, E., R. Shiekhattar, M. Sheldon, H. Cho, R. Drapkin, P. Rickert, E. Lees, C.W. Anderson, S. Linn, and D. Reinberg. 1996. A human RNA polymerase II complex associated with SRB and DNA-repair proteins. Nature. 381:86-89.
30. Marrazzini, A., C. Betti, F. Bernacchi, I. Barrai, and R. Barale. 1994. Micronucleus test and metaphase analyses in mice exposed to known and suspected spindle poisons. Mutagenesis. 9:305-515.
31. Messam, C.A., and R.N. Pittman. 1998. Asynchrony and commitment to die during apoptosis. Exp. Cell Res. 238:389-398.
32. Milne, G., and D. Weaver. 1993. Dominant negative alleles of RAD52 reveal a DNA repair/recombination complex including Rad51 and Rad52. Genes Dev. 7:1755-1765.
33. Mizumoto, K., R.J. Rothman, and J.L. Farber. 1994. Programmed cell death (apoptosis) of mouse fibroblasts is induced by the topoisomerase II inhibitor etoposide. Mol. Pharmac. 46:890-895.
34. Morita, T., Y. Yoshimura, A. Yamamoto, K. Murata, M. Mori, H. Yamamoto, and A. Matsushiro. 1993. A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes. Proc. Natl. Acad. Sci. USA. 90: 6577-6580.
35. Norppa, H., S. Luomahaara, H. Heikanen, S. Roth, M. Sorsa, L, Renzi, and C. Lindholm. 1993. Micronucleus assay in lymphocytes as a tool to biomonitor human exposure to aneuploidogens and clastogens. Environ. Health Perspect. 101(Suppl.):139-143.
36. Ogawa, T., X. Yu, A, Shinohara, and E.H. Egelman. 1993. Similarity of the yeast rad51 filament to the bacterial RecA filament. Science. 259:1896-1899.
37. Osheroff, N., E.L. Zechiedrich, and K.C. Gale. 1991. Catalytic function of DNA topoisomerase II. Bioessays. 13:269-275.
38. Osman F., and S. Subramani. 1998. Double-strand break-induced recombination in eukaryotes. Progr. Nucleic Acids Res. Mol. Biol. 58:264-299.
39. Petes, T.D., R.E. Malone, and L.S. Symington. 1991. Recombination in yeast. In The Molecular Biology and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics. J. Pringle and E. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 407-521.
40. Pittman, D.L., L.R. Weinberg, and J.C. Schimenti. 1998. Identification, characterization, and genetic mapping of Rad51d, a new mouse and human RAD51/RecA-relaled gene. Genomics. 49:103-111.
41. Prouty, S.M., K.D. Hanson, A.L. Boyle, J.R Brown, M. Shichiri, M.R. Follansbee, W. Kang, and J.M. Sedivy. 1993. A cell culture model system for genetic analyses of the cell cycle by targeted homologous recombination. Oncogene. 8:899-907.
42. Scully, R., J. Chen, A. Plug, Y. Xiao, D. Weaver, J. Feunteun, T. Ashley, and D.M. Livingston. 1997. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 88:265-275.
43. Sharan, S.K., M. Morimatsu, U. Albrecht, D.-S. Lim, E. Regel, C. Dinh, A. Sands, G. Eichele, P. Hasty, and A. Bradley. 1997. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature. 386:804-810.
44. Shen, Z.Y., K.G. Cloud, D.J. Chen, and M.S. Park. 1996. Specific interactions between the human Rad51 and Rad52 proteins. J. Biol. Chem. 271:148-152.
45. cdc2 activation required for apoptosis. Science. 263:1143-1145.
46. Shinohara, A., and T. Ogawa. 1995. Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci. 20:387-391.
47. Shinohara, A., H. Ogawa, and T. Ogawa. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 69:457-470.
48. Shinohara, A., H. Ogawa, Y. Matsuda, N. Ushio, K. Ikeo, and T. Ogawa. 1993. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nature Genet. 4:239-243.
49. Smith, M.L., I.-T. Chen, Q. Zhan, I. Bae, C.-Y. Chen, T.M. Gilmer, M.B. Kastan, P.M. O'Connor, and A.J. Fornace, Jr. 1994. Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science. 266:1376-1380.
50. Sonoda, E., M.S. Sasaki, J.-M. Buerstedde, O. Bezzubova, A. Shinohara, H. Ogawa, M. Takata, Y. Yamaguchi-Iwai, and S. Takeda. 1998. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO (Eur. Mol. Biol. Organ.) J. 17:598-608.
51. Stopper, H., C. Korher, P. Gibis, D.L. Spencer, and W.J. Caspary. 1995. Micronuclei induced by modulators of methylation: analogs of 5-azacytidine. Carcinogenesis. 16:1647-1650.
52. Stürzbecher, H.-W., B. Donzelmann, W. Henning, U. Knippschild, and S. Buchhop. 1996. p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO (Eur. Mol. Biol. Organ.) J. 15:1992-2002.
53. Sugiyama, T., E.M. Zaitseva, and S.C. Kowalczykowski. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272:7940-7945.
54. Sung, P. 1994 Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast rad51 protein. Science. 265:1241-1243.
55. Tashiro, S., N. Kotomura, A. Shinohara, K. Tanaka, and K. Ueda. 1996. S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene. 12:2165-2170.
56. Tsuzuki, T., Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, A. Matsushiro, Y. Yoshimura, and T. Morita. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA. 93:6236-6240.
57. Ucker, D.S. 1991. Death by suicide: one way to go in mammalian cellular development. New Biologist. 3:103-109.
58. Verhaegen, F., and A. Vral. 1994. Sensitivity of micronucleus induction in human lymphocytes to low-LET radiation qualities: RBE and correlation of RBE and LET. Radiation Res. 139:208-213.
59. Vispé, S., C. Cazaux, C. Lesca, and M. Defais. 1998. Overexpression of Rad51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res. 26:2859-2864.
60. Yamamoto, A., T. Taki, H. Yagi, T. Habu, K. Yoshida, Y. Yoshimura, K. Yamamoto, A. Matsushiro, Y. Nishimune, and T. Morita. 1996. Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol. Gen. Genet. 251:1-12.
61. Yuan, Z.-M., Y. Huang, T. Ishiko, S. Nakada, T. Utsugisawa, S. Kharbanda, R. Wang, P. Sung, A. Shinohara, R. Weichselbaum, and D. Kufe. 1998. Regulation of Rad51 function by c-Abl in response to DNA damage. J. Biol. Chem. 273:3799-3802.