Chromosome position determines the success of double-strand break repair

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 2, 2016, Pages E146-E154

  Lee, Cheng Sheng ^a,e   Wang, Ruoxi W ^a   Chang, Hsiao Han ^b   Capurso, Daniel ^c   Segal, Mark R ^d   Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Chromosome conformation; Donor location; Double strand break repair; Homologous recombination; Homology search

Indexed keywords

DOUBLE STRANDED DNA; FUNGAL DNA; GENOMIC DNA; REPLICATION FACTOR A; SINGLE STRANDED DNA; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL VIABILITY; CHROMOSOME ANALYSIS; CHROMOSOME POSITIONING; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; ENHANCER REGION; FREQUENCY ANALYSIS; FUNGAL CELL CULTURE; FUNGAL GENETICS; FUNGAL STRAIN; GENE CONVERSION; GENETIC ASSOCIATION; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; YEAST; CHROMOSOME; DNA REPLICATION; GENE LOCUS; GENETIC RECOMBINATION; GENETICS; KINETICS; METABOLISM; MICROBIAL VIABILITY; SACCHAROMYCES CEREVISIAE; SOUTHERN BLOTTING;

BLOTTING, SOUTHERN; CHROMOSOME POSITIONING; CHROMOSOMES, FUNGAL; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPLICATION; GENETIC LOCI; KINETICS; MICROBIAL VIABILITY; RECOMBINATION, GENETIC; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84954477354     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1523660113     Document Type: Article

References (47)

1. Hicks WM, Yamaguchi M, Haber JE (2011) Real-time analysis of double-strand DNA break repair by homologous recombination. Proc Natl Acad Sci USA 108(8): 3108-3115.
2. Jin QW, Fuchs J, Loidl J (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J Cell Sci 113(Pt 11):1903-1912.
3. Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295(5558):1306-1311.
4. Duan Z, et al. (2010) A three-dimensional model of the yeast genome. Nature 465(7296):363-367.
5. Agmon N, Liefshitz B, Zimmer C, Fabre E, Kupiec M (2013) Effect of nuclear architecture on the efficiency of double-strand break repair. Nat Cell Biol 15(6):694-699.
6. Therizols P, et al. (2006) Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region. J Cell Biol 172(2): 189-199.
7. Wong H, Arbona JM, Zimmer C (2013) How to build a yeast nucleus. Nucleus 4(5): 361-366.
8. Chiarle R, et al. (2011) Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 147(1):107-119.
9. Roukos V, et al. (2013) Spatial dynamics of chromosome translocations in living cells. Science 341(6146):660-664.
10. Hartwell LH, Weinert TA (1989) Checkpoints: Controls that ensure the order of cell cycle events. Science 246(4930):629-634.
11. Sandell LL, Zakian VA (1993) Loss of a yeast telomere: Arrest, recovery, and chromosome loss. Cell 75(4):729-739.
12. Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE (2001) Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol Cell 7(2):293-300.
13. Avşaroʇ lu B, et al. (2014) Effect of chromosome tethering on nuclear organization in yeast. PLoS One 9(7):e102474.
14. Zhang Z, Li G, Toh KC, Sung WK (2013) 3D chromosome modeling with semi-definite programming and Hi-C data. J Comput Biol 20(11):831-846.
15. Varoquaux N, Ay F, Noble WS, Vert JP (2014) A statistical approach for inferring the 3D structure of the genome. Bioinformatics 30(12):i26-i33.
16. Lesne A, Riposo J, Roger P, Cournac A, Mozziconacci J (2014) 3D genome reconstruction from chromosomal contacts. Nat Methods 11(11):1141-1143.
17. Segal MR, Xiong H, Capurso D, Vazquez M, Arsuaga J (2014) Reproducibility of 3D chromatin configuration reconstructions. Biostatistics 15(3):442-456.
18. Connolly B, White CI, Haber JE (1988) Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol Cell Biol 8(6):2342-2349.
19. Keogh MC, et al. (2006) A phosphatase complex that dephosphorylates gamma H2AX regulates DNA damage checkpoint recovery. Nature 439(7075):497-501.
20. Naumova N, et al. (2013) Organization of the mitotic chromosome. Science 342(6161): 948-953.
21. Guacci V, Hogan E, Koshland D (1994) Chromosome condensation and sister chromatid pairing in budding yeast. J Cell Biol 125(3):517-530.
22. Coïc E, et al. (2011) Dynamics of homology searching during gene conversion in Saccharomyces cerevisiae revealed by donor competition. Genetics 189(4):1225-1233.
23. Inbar O, Kupiec M (1999) Homology search and choice of homologous partner during mitotic recombination. Mol Cell Biol 19(6):4134-4142.
24. Wu X, Haber JE (1996) A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell 87(2):277-285.
25. Li J, et al. (2012) Regulation of budding yeast mating-type switching donor preference by the FHA domain of Fkh1. PLoS Genet 8(4):e1002630.
26. Fishman-Lobell J, Rudin N, Haber JE (1992) Two alternative pathways of doublestrand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12(3):1292-1303.
27. Eapen VV, Sugawara N, Tsabar M, Wu WH, Haber JE (2012) The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol Cell Biol 32(22):4727-4740.
28. White CI, Haber JE (1990) Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J 9(3):663-673.
29. Jain S, et al. (2009) A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev 23(3):291-303.
30. Vaze MB, et al. (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10(2):373-385.
31. Lee SE, et al. (1998) Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94(3):399-409.
32. Van Hulle K, et al. (2007) Inverted DNA repeats channel repair of distant doublestrand breaks into chromatid fusions and chromosomal rearrangements. Mol Cell Biol 27(7):2601-2614.
33. Downing B, Morgan R, Van Hulle K, Deem A, Malkova A (2008) Large inverted repeats in the vicinity of a single double-strand break strongly affect repair in yeast diploids lacking Rad51. Mutat Res 645(1-2):9-18.
34. Miné-Hattab J, Rothstein R (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14(5):510-517.
35. Clerici M, Mantiero D, Lucchini G, Longhese MP (2005) The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J Biol Chem 280(46):38631-38638.
36. Costelloe T, et al. (2012) The yeast Fun30 and human SMARCAD1 chromatin remodellers promote DNA end resection. Nature 489(7417):581-584.
37. Horigome C, et al. (2014) SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol Cell 55(4):626-639.
38. Sugawara N, Wang X, Haber JE (2003) In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol Cell 12(1):209-219.
39. Chen H, Lisby M, Symington LS (2013) RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol Cell 50(4):589-600.
40. Nagano T, et al. (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502(7469):59-64.
41. Aylon Y, Kupiec M (2004) New insights into the mechanism of homologous recombination in yeast. Mutat Res 566(3):231-248.
42. Amin NS, Nguyen MN, Oh S, Kolodner RD (2001) exo1-Dependent mutator mutations: Model system for studying functional interactions in mismatch repair. Mol Cell Biol 21(15):5142-5155.
43. Tan FJ, Hoang ML, Koshland D (2012) DNA resection at chromosome breaks promotes genome stability by constraining non-allelic homologous recombination. PLoS Genet 8(3):e1002633.
44. Renkawitz J, Lademann CA, Kalocsay M, Jentsch S (2013) Monitoring homology search during DNA double-strand break repair in vivo. Mol Cell 50(2):261-272.
45. Qi Z, et al. (2015) DNA sequence alignment by microhomology sampling during homologous recombination. Cell 160(5):856-869.
46. Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE (2010) Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromeredependent mechanism. Curr Biol 20(4):328-332.
47. Roukos V, Misteli T (2014) The biogenesis of chromosome translocations. Nat Cell Biol 16(4):293-300.