Rad50 is dispensable for the maintenance and viability of postmitotic tissues

Molecular and Cellular Biology

Volumn 29, Issue 2, 2009, Pages 483-492

  Adelman, Carrie A ^a,b   De Saurav, ^a   Petrini, John H J ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MRE11 PROTEIN; RAD50 PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL VIABILITY; CEREBELLUM; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; GENE; GENE DELETION; HOMOLOGOUS RECOMBINATION; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAD50 GENE; TELOMERE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BONE MARROW CELLS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; DNA DAMAGE; DNA-BINDING PROTEINS; GENE DELETION; GENE TARGETING; HEPATOCYTES; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICE, KNOCKOUT; MITOSIS; PURKINJE CELLS; TELOMERE;

MAMMALIA; MUS;

EID: 58249101175     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01525-08     Document Type: Article

References (63)

1. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171.
2. Barnes, D. E., G. Stamp, I. Rosewell, A. Denzel, and T. Lindahl. 1998. Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 8:1395-1398.
3. Barski, J. J., K. Dethleffsen, and M. Meyer. 2000. Cre recombinase expression in cerebellar Purkinje cells. Genesis 28:93-98.
4. Blindenbacher, A., X. Wang, I. Langer, R. Savino, L. Terracciano, and M. H. Heim. 2003. Interleukin 6 is important for survival after partial hepatectomy in mice. Hepatology 38:674-682.
5. Boulton, S. J., and S. P. Jackson. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1819-1828.
6. Bressan, D. A., B. K. Baxter, and J. H. Petrini. 1999. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7681-7687.
7. Celli, G. B., and T. de Lange. 2005. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7:712-718.
8. de Jager, M., J. van Noort, D. C. van Gent, C. Dekker, R. Kanaar, and C. Wyman. 2001. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8:1129-1135.
9. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
10. Demuth, I., P. O. Frappart, G. Hildebrand, A. Melchers, S. Lobitz, L. Stockl, R. Varon, Z. Herceg, K. Sperling, Z. Q. Wang, and M. Digweed. 2004. An inducible null mutant murine model of Nijmegen breakage syndrome proves the essential function of NBS1 in chromosomal stability and cell viability. Hum. Mol. Genet. 13:2385-2397.
11. Deng, C., J. A. Brown, D. You, and J. M. Brown. 2005. Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170:591-600.
12. Dull, T., R. Zufferey, M. Kelly, R. J. Mandel, M. Nguyen, D. Trono, and L. Naldini. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
13. El-Khamisy, S. F., G. M. Saifi, M. Weinfeld, F. Johansson, T. Helleday, J. R. Lupski, and K. W. Caldecott. 2005. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434:108-113.
14. Fausto, N., and J. S. Campbell. 2003. The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech. Dev. 120:117-130.
15. Frank, K. M., J. M. Sekiguchi, K. J. Seidl, W. Swat, G. A. Rathbun, H. L. Cheng, L. Davidson, L. Kangaloo, and F. W. Alt. 1998. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 396:173-177.
16. Frank, K. M., N. E. Sharpless, Y. Gao, J. M. Sekiguchi, D. O. Ferguson, C. Zhu, J. P. Manis, J. Horner, R. A. DePinho, and F. W. Alt. 2000. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5:993-1002.
17. Frappart, P. O., W. M. Tong, I. Demuth, I. Radovanovic, Z. Herceg, A. Aguzzi, M. Digweed, and Z. Q. Wang. 2005. An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat. Med. 11:538-544.
18. Gao, Y., Y. Sun, K. M. Frank, P. Dikkes, Y. Fujiwara, K. J. Seidl, J. M. Sekiguchi, G. A. Rathbun, W. Swat, J. Wang, R. T. Bronson, B. A. Malynn, M. Bryans, C. Zhu, J. Chaudhuri, L. Davidson, R. Ferrini, T. Stamato, S. H. Orkin, M. E. Greenberg, and F. W. Alt. 1998. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 95:891-902.
19. Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583-586.
20. Hatten, M. E., and N. Heintz. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu. Rev. Neurosci. 18:385-408.
21. Hendzel, M. J., Y. Wei, M. A. Mancini, A. Van Hooser, T. Ranalli, B. R. Brinkley, D. P. Bazett-Jones, and C. D. Allis. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric hetero-chromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360.
22. Herson, P. S., M. Virk, N. R. Rustay, C. T. Bond, J. C. Crabbe, J. P. Adelman, and J. Maylie. 2003. A mouse model of episodic ataxia type-1. Nat. Neurosci. 6:378-383.
23. Herzog, K. H., M. J. Chong, M. Kapsetaki, J. I. Morgan, and P. J. McKinnon. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280:1089-1091.
24. Hopfner, K. P., L. Craig, G. Moncalian, R. A. Zinkel, T. Usui, B. A. Owen, A. Karcher, B. Henderson, J. L. Bodmer, C. T. McMurray, J. P. Carney, J. H. Petrini, and J. A. Tainer. 2002. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562-566.
25. International Nijmegen Breakage Syndrome Study Group. 2000. Nijmegen breakage syndrome. Arch. Dis. Child. 82:400-406.
26. Ivanov, E. L., V. G. Korolev, and F. Fabre. 1992. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132:651-664.
27. Kang, J., R. T. Bronson, and Y. Xu. 2002. Targeted disruption of NBS1 reveals its roles in mouse development and DNA repair. EMBO J. 21:1447-1455.
28. Kironmai, K. M., and K. Muniyappa. 1997. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells. 2:443-455.
29. Kuhn, R., F. Schwenk, M. Aguet, and K. Rajewsky. 1995. Inducible gene targeting in mice. Science 269:1427-1429.
30. Lavin, M. F. 2007. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 26:7749-7758.
31. Lee, Y., D. E. Barnes, T. Lindahl, and P. J. McKinnon. 2000. Defective neurogenesis resulting from DNA ligase IV deficiency requires Atm. Genes Dev. 14:2576-2580.
32. Lesher, D. T., Y. Pommier, L. Stewart, and M. R. Redinbo. 2002. 8-Oxoguanine rearranges the active site of human topoisomerase I. Proc. Natl. Acad. Sci. USA 99:12102-12107.
33. 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.
34. Limoli, C. L., E. Giedzinski, W. M. Bonner, and J. E. Cleaver. 2002. UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma-H2AX formation, and Mre11 relocalization. Proc. Natl. Acad. Sci. USA 99:233-238.
35. Liu, C., J. J. Pouliot, and H. A. Nash. 2002. Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc. Natl. Acad. Sci. USA 99:14970-14975.
36. Lois, C., E. J. Hong, S. Pease, E. J. Brown, and D. Baltimore. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872.
37. Luo, G., M. S. Yao, C. F. Bender, M. Mills, A. R. Bladl, A. Bradley, and J. H. Petrini. 1999. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 96:7376-7381.
38. Maser, R. S., O. K. Mirzoeva, J. Wells, H. Olivares, B. R. Williams, R. Zinkel, P. J. Farnham, and J. H. J. Petrini. 2001. The MRE11 complexand DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21:6006-6016.
39. Mirzoeva, O. K., and J. H. Petrini. 2003. DNA replication- dependent nuclear dynamics of the Mre11 complex. Mol. Cancer Res. 1:207-218.
40. Morales, M., Y. Liu, E. C. Laiakis, W. F. Morgan, S. D. Nimer, and J. H. Petrini. 2008. DNA damage signaling in hematopoietic cells: a role for Mre11 complex repair of topoisomerase lesions. Cancer Res. 68:2186-2193.
41. Orii, K. E., Y. Lee, N. Kondo, and P. J. McKinnon. 2006. Selectiveutilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development. Proc. Natl. Acad. Sci. USA 103:10017-10022.
42. Petrini, J. H., and T. H. Stracker. 2003. The cellular response to DNA double-strand breaks: defining the sensors and mediators. Trends Cell Biol. 13:458-462.
43. Pommier, Y. 2006. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer. 6:789-802.
44. Pourquier, P., L. M. Ueng, J. Fertala, D. Wang, H. J. Park, J. M. Essigmann, M. A. Bjornsti, and Y. Pommier. 1999. Induction of reversible complexes between eukaryotic DNA topoisomerase I and DNA-containing oxidative base damages. 7, 8-dihydro-8-oxoguanine and 5-hydroxycytosine. J. Biol. Chem. 274:8516-8523.
45. Reina-San-Martin, B., M. C. Nussenzweig, A. Nussenzweig, and S. Difilippantonio. 2005. Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc. Natl. Acad. Sci. USA 102:1590-1595.
46. Soares, H. D., J. I. Morgan, and P. J. McKinnon. 1998. Atm expression patterns suggest a contribution from the peripheral nervous system to the phenotype of ataxia-telangiectasia. Neuroscience 86:1045-1054.
47. 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 J. 17:598-608.
48. Stewart, G. S., R. S. Maser, T. Stankovic, D. A. Bressan, M. I. Kaplan, N. G. Jaspers, A. Raams, P. J. Byrd, J. H. Petrini, and A. M. Taylor. 1999. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99:577-587.
49. Stohr, B. A., and K. N. Kreuzer. 2001. Repair of topoisomerase-mediated DNA damage in bacteriophage T4. Genetics 158:19-28.
50. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556.
51. Tauchi, H., J. Kobayashi, K. Morishima, D. C. van Gent, T. Shiraishi, N. S. Verkaik, D. vanHeems, E. Ito, A. Nakamura, E. Sonoda, M. Takata, S. Takeda, S. Matsuura, and K. Komatsu. 2002. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature 420: 93-98.
52. Theunissen, J. W., M. I. Kaplan, P. A. Hunt, B. R. Williams, D. O. Ferguson, F. W. Alt, and J. H. Petrini. 2003. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol. Cell 12:1511-1523.
53. 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.
54. Vance, J. R., and T. E. Wilson. 2002. Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc. Natl. Acad. Sci. USA 99:13669-13674.
55. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92:401-413.
56. Wang, Y., D. Cortez, P. Yazdi, N. Neff, S. J. Elledge, and J. Qin. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:927-939.
57. Williams, B. R., O. K. Mirzoeva, W. F. Morgan, J. Lin, W. Dunnick, and J. H. Petrini. 2002. A murine model of Nijmegen breakage syndrome. Curr. Biol. 12:648-653.
58. Wiltzius, J. J., M. Hohl, J. C. Fleming, and J. H. Petrini. 2005. The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol. 12:403-407.
59. Xiao, Y., and D. T. Weaver. 1997. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 25:2985-2991.
60. Yamada, Y., I. Kirillova, J. J. Peschon, and N. Fausto. 1997. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor. Proc. Natl. Acad. Sci. USA 94:1441-1446.
61. Yamaguchi-Iwai, Y., E. Sonoda, M. S. Sasaki, C. Morrison, T. Haraguchi, Y. Hiraoka, Y. M. Yamashita, T. Yagi, M. Takata, C. Price, N. Kakazu, and S. Takeda. 1999. Mre11 is essentialforthe maintenance ofchromosomal DNA in vertebrate cells. EMBO J. 18:6619-6629.
62. Yang, Y. G., A. Saidi, P. O. Frappart, W. Min, C. Barrucand, V. Dumon-Jones, J. Michelon, Z. Herceg, and Z. Q. Wang. 2006. Conditional deletion of Nbs1 in murine cells reveals its role in branching repair pathways of DNA double-strand breaks. EMBO J. 25:5527-5538.
63. Zhu, X. D., B. Kuster, M. Mann, J. H. Petrini, and T. Lange. 2000. Cell- cycle-regulated association ofRAD50/MRE11/NBS1 withTRF2 and human telomeres. Nat. Genet. 25:347-352.