Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery

Genes and Development

Volumn 23, Issue 8, 2009, Pages 912-927

  Oza, Pranav ^a   Jaspersen, Sue L ^b,c   Miele, Adriana ^a   Dekker, Job ^a   Peterson, Craig L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

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

Author keywords

3C ; Chromatin; DNA double strand break; DNA repair; Mps3p; Rad52

Indexed keywords

DOUBLE STRANDED DNA; ENVELOPE PROTEIN; MPS3P PROTEIN; NUCLEAR PROTEIN; TELOMERASE; UNCLASSIFIED DRUG; CDC13 PROTEIN, S CEREVISIAE; DNA BINDING PROTEIN; HELICASE; MEMBRANE PROTEIN; MPS3 PROTEIN, S CEREVISIAE; PIF1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SLX5 PROTEIN, S CEREVISIAE; TELOMERE BINDING PROTEIN;

ARTICLE; CELL POPULATION; CHROMATIN; CHROMOSOME; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENE LOCATION; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; YEAST CELL; CELL NUCLEUS; DOUBLE STRANDED DNA BREAK; GENETIC PROCEDURES; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

CELL NUCLEUS; CHROMATIN; CHROMOSOMES, FUNGAL; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA-BINDING PROTEINS; GENETIC TECHNIQUES; MEMBRANE PROTEINS; MICROSCOPY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE-BINDING PROTEINS;

EID: 65249150132     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1782209     Document Type: Article

References (79)

1. Antoniacci, L.M., Kenna, M.A., Uetz, P., Fields, S., and Skibbens, R.V. 2004. The spindle pole body assembly component Mps3p/Nep98p functions in sister chromatid cohesion. J. Biol. Chem. 279:49542-49550.
2. Antoniacci, L.M., Kenna, M.A., and Skibbens, R.V. 2007. The nuclear envelope and spindle pole body-associated Mps3 protein bind telomere regulators and function in telomere clustering. Cell Cycle 6:75-79.
3. Aten, J.A., Stap, J., Krawczyk, P.M., van Oven, C.H., Hoebe, R.A., Essers, J., and Kanaar, R. 2004. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303:92-95.
4. Aylon, Y., Liefshitz, B., and Kupiec, M. 2004. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23:4868-4875.
5. Bakkenist, C.J. and Kastan, M.B. 2003. DNA damage activates ATM through intermolecular autophosphorylation and di- mer dissociation. Nature 421:499-506.
6. Banerjee, S. and Myung, K. 2004. Increased genome instability and telomere length in the elg1-deficient Saccharomyces cerevisiae mutant are regulated by S-phase checkpoints. Eukaryot. Cell 3:1557-1566.
7. Bassing, C.H. and Alt, F.W. 2004. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst.) 3:781-796.
8. Belmont, A.S. and Straight, A.F. 1998. In vivo visualization of chromosomes using lac operator-repressor binding. Trends Cell Biol. 8:121-124.
9. Ben-Shahar, T.R., Heeger, S., Lehane, C., East, P., Flynn, H., Skehel, M., and Uhlmann, F. 2008. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321:563-566.
10. Bianchi, A. and Shore, D. 2008. How telomerase reaches its end: Mechanism of telomerase regulation by the telomeric complex. Mol Cell. 31:153-165.
11. Bianchi, A., Negrini, S., and Shore, D. 2004. Delivery of yeast telomerase to a DNA break depends on the recruitment functions of Cdc13 and Est1. Mol. Cell. 16:139-146.
12. Bupp, J.M., Martin, A.E., Stensrud, E.S., and Jaspersen, S.L. 2007. Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J. Cell Biol. 179:845-854.
13. Bystricky, K., Van Attikum, H., Montiel, M.-D., Dion, V., Gehlen, L., and Gasser, S.M. 2008. Regulation of nuclear positioning and dynamics of the silent mating type loci by the yeast Ku70/Ku80 complex. Mol. Cell. Biol. 29:835-848.
14. Chan, A., Boule, J.-B., and Zakian, V.A. 2008. Two pathways recruit telomerase to Saccharomyces cerevisiae telomeres. PLoS Genet. 4:e1000236. doi: 10.1371/journal.pgen.1000236.
15. Chen, C. and Kolodner, R.D. 1999. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23:81-85.
16. Conrad, M.N., Lee, C.-Y., Wilkerson, J.L., and Dresser, M.E. 2007. MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 104:8863-8868.
17. Crisp, M., Liu, Q., Roux, K., Rattner, J.B., Shanahan, C., Burke, B., Stahl, P.D., and Hodzic, D. 2006. Coupling of the nucleus and cytoplasm: Role of the LINC complex. J. Cell Biol. 172:41-53.
18. Dekker, J. 2007. GC- and AT-rich chromatin domains differ in conformation and histone modification status and are differentially modulated by Rpd3p. Genome Biol. 8:R116. doi: 10.1186/gb-2007-8-6-r116.
19. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. 2002. Capturing chromosome conformation. Science 295:1306-1311.
20. de La Roche Saint-Andre, C. 2008. Alternative ends: Telomeres and meiosis. Biochimie 90:181-189.
21. Diede, S.J. and Gottschling, D.E. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases α and δ. Cell 99:723-733.
22. Diede, S.J. and Gottschling, D.E. 2001. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11:1336-1340.
23. Ding, X., Xu, R., Yu, J., Xu, T., Zhuang, Y., and Han, M. 2007. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12:863-872.
24. Dostie, J., Richmond, T.A., Arnaout, R.A., Selzer, R.R., Lee, W.L., Honan, T.A., Rubio, E.D., Krumm, A., Lamb, J., Nusbaum, C., et al. 2006. Chromosome Conformation Capture Carbon Copy (5C): A massively parallel solution for mapping interactions between genomic elements. Genome Res. 16:1299-1309.
25. Downs, J.A., Lowndes, N.F., and Jackson, S.P. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001-1004.
26. Foster, P.L. 2006. Methods for determining spontaneous mutation rates. Methods Enzymol. 409:195-213.
27. Haque, F., Lloyd, D.J., Smallwood, D.T., Dent, C.L., Shanahan, C.M., Fry, A.M., Trembath, R.C., and Shackleton, S. 2006. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol. Cell. Biol. 26:3738-3751.
28. Hediger, F., Neumann, F.R., Van Houwe, G., Dubrana, K., and Gasser, S.M. 2002. Live imaging of telomeres: yKu and Sir proteins define redundant telomere-anchoring pathways in yeast. Curr. Biol. 12:2076-2089.
29. Hughes, T.R., Weilbaecher, R.G., Walterscheid, M., and Lundblad, V. 2000. Identification of the single-strand telo- meric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein. Proc. Natl. Acad. Sci. 97:6457-6462.
30. Ira, G., Pellicioli, A., Balijja, A., Wang, X., Fiorani, S., Carotenuto, W., Liberi, G., Bressan, D., Wan, L., Hollingsworth, N.M., et al. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011-1017.
31. Jaspersen, S.L., Giddings Jr., T.H., and Winey, M. 2002. Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J. Cell Biol. 159:945-956.
32. Jaspersen, S.L., Martin, A.E., Glazko, G., Giddings Jr., T.H., Morgan, G., Mushegian, A., and Winey, M. 2006. The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J. Cell Biol. 174:665-675.
33. Kaye, J.A., Melo, J.A., Cheung, S.K., Vaze, M.B., Haber, J.E., and Toczyski, D.P. 2004. DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr. Biol. 14:2096-2106.
34. Keeney, S. and Neale, M.J. 2006. Initiation of meiotic recombination by formation of DNA double-strand breaks: Mechanism and regulation. Biochem. Soc. Trans. 34:523-525.
35. Keogh, M.-C., Kim, J.-A., Downey, M., Fillingham, J., Chowdhury, D., Harrison, J.C., Onishi, M., Datta, N., Galicia, S., Emili, A., et al. 2006. A phosphatase complex that dephosphory- lates γH2AX regulates DNA damage checkpoint recovery. Nature439:497-501.
36. Kruhlak, M.J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Muller, W.G., McNally, J.G., Bazett-Jones, D.P., and Nussenzweig, A. 2006. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172:823-834.
37. Lee, S.E., Moore, J.K., Holmes, A., Umezu, K., Kolodner, R.D., and Haber, J.E. 1998. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399-409.
38. Lee, S.E., Pellicioli, A., Vaze, M.B., Sugawara, N., Malkova, A., Foiani, M., and Haber, J.E. 2003. Yeast Rad52 and Rad51 recombination proteins define a second pathway of DNA damage assessment in response to a single double-strand break. Mol. Cell. Biol. 23:8913-8923.
39. Lin, Y.-C., Hsu, C.-L., Shih, J.-W., and Lin, J.-J. 2001. Specific binding of single-stranded telomeric DNA by Cdc13p of Saccharomyces cerevisiae. J. Biol. Chem. 276:24588-24593.
40. Lisby, M., Mortensen, U.H., and Rothstein, R. 2003. Colocaliza- tion of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5:572-577.
41. Lobachev, K., Vitriol, E., Stemple, J., Resnick, M.A., and Bloom, K. 2004. Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr. Biol. 14:2107-2112.
42. Mangahas, J.L., Alexander, M.K., Sandell, L.L., and Zakian, V.A. 2001. Repair of chromosome ends after telomere loss in Saccharomyces. Mol. Biol. Cell 12:4078-4089.
43. Mladenov, E., Anachkov, B., and Tsaneva, I. 2006. Sub-nuclear localization of Rad51 in response to DNA damage. Genes Cells 11:513-524.
44. Moldovan, G.L., Pfander, B., and Jentsch, S. 2007. PCNA, the maestro of the replication fork. Cell 129:665-679.
45. Moore, J.K. and Haber, J.E. 1996. Capture of retrotransposon DNA at the sites of chromosomal double-strand breaks. Nature 383:644-646.
46. Myung, K. and Kolodner, R.D. 2003. Induction of genome instability by DNA damage in Saccharomyces cerevisiae. DNA Repair (Amst.) 2:243-258.
47. Myung, K., Chen, C., and Kolodner, R.D. 2001. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411:1073-1076.
48. Nagai, S., Dubrana, K., Tsai-Pflugfelder, M., Davidson, M.B., Roberts, T.M., Brown, G.W., Varela, E., Hediger, F., Gasser, S.M., and Krogan, N.J. 2008. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322:597-602.
49. Negrini, S., Ribaud, V., Bianchi, A., and Shore, D. 2007. DNA breaks are masked by multiple Rap1 binding in yeast: Implications for telomere capping and telomerase regulation. Genes & Dev. 21:292-302.
50. Nishikawa, S., Terazawa, Y., Nakayama, T., Hirata, A., Makio, T., and Endo, T. 2003. Nep98p is a component of the yeast spindle pole body and essential for nuclear division and fusion. J. Biol. Chem. 278:9938-9943.
51. Paques, F. and Haber, J.E. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349-404.
52. Pennaneach, V., Putnam, C.D., and Kolodner, R.D. 2006. Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol. Microbiol. 59:1357-1368.
53. Pennock, E., Buckley, K., and Lundblad, V. 2001. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104:387-396.
54. Pfander, B., Moldovan, G.L., Sacher, M., Hoege, C., and Jentsch, S. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428-433.
55. Riha, K., Heacock, M.L., and Shippen, D.E. 2006. The role of the nonhomologous end-joining DNA double-strand break repair pathway in telomere biology. Annu. Rev. Genet. 40:237-277.
56. Schmidt, K.H., Pennaneach, V., Putnam, C.D., Kolodner, R.D., Judith, L.C., and Paul, M. 2006. Analysis of gross chromosomal rearrangements in Saccharomyces cerevisiae. Methods Enzymol. 409:462-476.
57. Schober, H., Ferreira, H., Kalck, V., Gehlen, L.R., and Gasser, S.M. 2009. Telomerase and SUN domain protein Mps3 anchor and protect telomeres in budding yeast. Genes & Dev. (this issue). doi: 10.1101/gad.1787509.
58. Schramke, V., Luciano, P., Brevet, V., Guillot, S., Corda, Y., Longhese, M.P., Gilson, E., and Geli, V. 2004. RPA regulates telomerase action by providing Est1p access to chromosome ends. Nat. Genet. 36:46-54.
59. Seto, A.G., Zaug, A.J., Sobel, S.G., Wolin, S.L., and Cech, T.R. 1999. Saccharomyces cerevisiae telomerase is an Sm small nuclear ribonucleoprotein particle. Nature 401:177-180.
60. Shim, E.Y., Hong, S.J., Oum, J.H., Yanez, Y., Zhang, Y., and Lee, S.E. 2007. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27:1602-1613.
61. Shroff, R., Arbel-Eden, A., Pilch, D., Ira, G., Bonner, W.M., Petrini, J.H., Haber, J.E., and Lichten, M. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703-1711.
62. Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B., and de Laat, W. 2006. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38:1348-1354.
63. Stellwagen, A.E., Haimberger, Z.W., Veatch, J.R., and Gottschling, D.E. 2003. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes & Dev. 17:2384-2395.
64. Sugawara, N. and Haber, J.E. 2006. Repair of DNA double strand breaks: In vivo biochemistry. Methods Enzymol. 408:416-429.
65. Sung, P., Krejci, L., Van Komen, S., and Sehorn, M.G. 2003. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278:42729-42732.
66. Therizols, P., Fairhead, C., Cabal, G.G., Genovesio, A., Olivo- Marin, J.C., Dujon, B., and Fabre, E. 2006. Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region. J. Cell Biol. 172:189-199.
67. Tolhuis, B., Palstra, R.-J., Splinter, E., Grosveld, F., and de Laat, W. 2002. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell 10:1453-1465.
68. Tseng, S.-F., Lin, J.-J., and Teng, S.-C. 2006. The telomerase- recruitment domain of the telomere binding protein Cdc13 is regulated by Mec1p/Tel1p-dependent phosphorylation. Nucleic Acids Res. 34:6327-6336.
69. Unal, E., Heidinger-Pauli, J.M., and Koshland, D. 2007. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317:245-248.
70. Vakoc, C.R., Letting, D.L., Gheldof, N., Sawado, T., Bender, M.A., Groudine, M., Weiss, M.J., Dekker, J., and Blobel, G.A. 2005.
71. Proximity among distant regulatory elements at the β-globin locus requires GATA-1 and FOG-1. Mol. Cell 17:453-462.
72. Vaze, M.B., Pellicioli, A., Lee, S.E., Ira, G., Liberi, G., Arbel-Eden, A., Foiani, M., and Haber, J.E. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10:373-385.
73. Vilenchik, M.M. and Knudson, A.G. 2003. Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. 100:12871-12876.
74. Viscardi, V., Clerici, M., Cartagena-Lirola, H., and Longhese, M.P. 2005. Telomeres and DNA damage checkpoints. Biochimie 87:613-624.
75. Wolner, B. and Peterson, C.L. 2005. ATP-dependent and ATP- independent roles for the Rad54 chromatin remodeling enzyme during recombinational repair of a DNA double strand break. J. Biol. Chem. 280:10855-10860.
76. Wolner, B., van Komen, S., Sung, P., and Peterson, C.L. 2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12:221-232.
77. Zhang, C., Roberts, T.M., Yang, J., Desai, R., and Brown, G.W. 2006. Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amst.) 5:336-346.
78. Zhao, Z., Tavoosidana, G., Sjolinder, M., Gondor, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K.S., Singh, U., et al. 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 38:1341-1347.
79. Ziv, Y., Bielopolski, D., Galanty, Y., Lukas, C., Taya, Y., Schultz, D.C., Lukas, J., Bekker-Jensen, S., Bartek, J., and Shiloh, Y. 2006. Chromatin relaxation in response to DNA double- strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 8:870-876.