Behavior of dicentric chromosomes in budding yeast
Autoři:
Diana Cook aff001; Sarah Long aff001; John Stanton aff001; Patrick Cusick aff001; Colleen Lawrimore aff001; Elaine Yeh aff001; Sarah Grant aff001; Kerry Bloom aff001
Působiště autorů:
Department of Biology, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
aff001
Vyšlo v časopise:
Behavior of dicentric chromosomes in budding yeast. PLoS Genet 17(3): e1009442. doi:10.1371/journal.pgen.1009442
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009442
Souhrn
DNA double-strand breaks arise in vivo when a dicentric chromosome (two centromeres on one chromosome) goes through mitosis with the two centromeres attached to opposite spindle pole bodies. Repair of the DSBs generates phenotypic diversity due to the range of monocentric derivative chromosomes that arise. To explore whether DSBs may be differentially repaired as a function of their spatial position in the chromosome, we have examined the structure of monocentric derivative chromosomes from cells containing a suite of dicentric chromosomes in which the distance between the two centromeres ranges from 6.5 kb to 57.7 kb. Two major classes of repair products, homology-based (homologous recombination (HR) and single-strand annealing (SSA)) and end-joining (non-homologous (NHEJ) and micro-homology mediated (MMEJ)) were identified. The distribution of repair products varies as a function of distance between the two centromeres. Genetic dependencies on double strand break repair (Rad52), DNA ligase (Lif1), and S phase checkpoint (Mrc1) are indicative of distinct repair pathway choices for DNA breaks in the pericentromeric chromatin versus the arms.
Klíčová slova:
Centromeres – DNA repair – DNA replication – Genomics – Homologous recombination – Nucleolus – Polymerase chain reaction – Dicentric chromosomes
Zdroje
1. Haber JE, Thorburn PC. Healing of broken linear dicentric chromosomes in yeast. Genetics. 1984;106(2):207–26. Epub 1984/02/01. 6365688; PubMed Central PMCID: PMC1202252.
2. Haber JE, Thorburn PC, Rogers D. Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae. Genetics. 1984;106(2):185–205. Epub 1984/02/01. 6321297; PubMed Central PMCID: PMC1202251.
3. McClintock B. The Production of Homozygous Deficient Tissues with Mutant Characteristics by Means of the Aberrant Mitotic Behavior of Ring-Shaped Chromosomes. Genetics. 1938;23(4):315–76. Epub 1938/07/01. 17246891; PubMed Central PMCID: PMC1209016.
4. McClintock B. Induction of Instability at Selected Loci in Maize. Genetics. 1953;38(6):579–99. Epub 1953/11/01. 17247459; PubMed Central PMCID: PMC1209627.
5. Hill A, Bloom K. Genetic manipulation of centromere function. Mol Cell Biol. 1987;7(7):2397–405. doi: 10.1128/mcb.7.7.2397 3302676.
6. Hill A, Bloom K. Acquisition and processing of a conditional dicentric chromosome in Saccharomyces cerevisiae. Mol Cell Biol. 1989;9(3):1368–70. Epub 1989/03/01. doi: 10.1128/mcb.9.3.1368 2657392; PubMed Central PMCID: PMC362735.
7. Brock JA, Bloom K. A chromosome breakage assay to monitor mitotic forces in budding yeast. J Cell Sci. 1994;107 (Pt 4):891–902. Epub 1994/04/01. 8056845.
8. Komura J, Ikehata H, Mori T, Ono T. Fully functional global genome repair of (6–4) photoproducts and compromised transcription-coupled repair of cyclobutane pyrimidine dimers in condensed mitotic chromatin. Exp Cell Res. 2012;318(5):623–31. Epub 2012/01/18. doi: 10.1016/j.yexcr.2012.01.003 22248875.
9. Lopez V, Barinova N, Onishi M, Pobiega S, Pringle JR, Dubrana K, et al. Cytokinesis breaks dicentric chromosomes preferentially at pericentromeric regions and telomere fusions. Genes Dev. 2015;29(3):322–36. Epub 2015/02/04. doi: 10.1101/gad.254664.114 25644606; PubMed Central PMCID: PMC4318148.
10. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Molecular and cellular biology. 1994;14(2):1293–301. Epub 1994/02/01. doi: 10.1128/mcb.14.2.1293 8289808; PubMed Central PMCID: PMC358484.
11. Song W, Gawel M, Dominska M, Greenwell PW, Hazkani-Covo E, Bloom K, et al. Nonrandom distribution of interhomolog recombination events induced by breakage of a dicentric chromosome in Saccharomyces cerevisiae. Genetics. 2013;194(1):69–80. Epub 2013/02/16. genetics.113.150144 [pii] doi: 10.1534/genetics.113.150144 23410835; PubMed Central PMCID: PMC3632482.
12. Thrower DA, Stemple J, Yeh E, Bloom K. Nuclear oscillations and nuclear filament formation accompany single-strand annealing repair of a dicentric chromosome in Saccharomyces cerevisiae. J Cell Sci. 2003;116(Pt 3):561–9. Epub 2003/01/01. doi: 10.1242/jcs.00251 12508116.
13. Jager D, Philippsen P. Stabilization of dicentric chromosomes in Saccharomyces cerevisiae by telomere addition to broken ends or by centromere deletion. Embo j. 1989;8(1):247–54. Epub 1989/01/01. 2653811; PubMed Central PMCID: PMC400796.
14. Surosky RT, Tye BK. Resolution of dicentric chromosomes by Ty-mediated recombination in yeast. Genetics. 1985;110(3):397–419. Epub 1985/07/01. 2991081; PubMed Central PMCID: PMC1202571.
15. Kim HS, Choi YB, Lee JH, Park SY, Kim HK, Koh JS, et al. Condensed chromatin staining of CKAP2 as surrogate marker for mitotic figures. J Cancer Res Clin Oncol. 2012;138(1):95–102. Epub 2011/10/25. doi: 10.1007/s00432-011-1053-6 22020800.
16. Thrower DA, Bloom K. Dicentric chromosome stretching during anaphase reveals roles of Sir2/Ku in chromatin compaction in budding yeast. Mol Biol Cell. 2001;12(9):2800–12. Epub 2001/09/13. doi: 10.1091/mbc.12.9.2800 11553718; PubMed Central PMCID: PMC59714.
17. Yan J, Xu L, Crawford G, Wang Z, Burgess SM. The forkhead transcription factor FoxI1 remains bound to condensed mitotic chromosomes and stably remodels chromatin structure. Mol Cell Biol. 2006;26(1):155–68. Epub 2005/12/16. doi: 10.1128/MCB.26.1.155-168.2006 16354687; PubMed Central PMCID: PMC1317626.
18. Hasegawa H, Nakano T, Hozumi Y, Takagi M, Ogino T, Okada M, et al. Diacylglycerol kinase zeta is associated with chromatin, but dissociates from condensed chromatin during mitotic phase in NIH3T3 cells. J Cell Biochem. 2008;105(3):756–65. Epub 2008/08/06. doi: 10.1002/jcb.21873 18680142.
19. Lawrimore J, Bloom K. The regulation of chromosome segregation via centromere loops. Crit Rev Biochem Mol Biol. 2019;54(4):352–70. Epub 2019/10/02. doi: 10.1080/10409238.2019.1670130 31573359; PubMed Central PMCID: PMC6856439.
20. Winey M, Bloom K. Mitotic spindle form and function. Genetics. 2012;190(4):1197–224. Epub 2012/04/12. 190/4/1197 [pii] doi: 10.1534/genetics.111.128710 22491889; PubMed Central PMCID: PMC3316638.
21. Lemaitre C, Grabarz A, Tsouroula K, Andronov L, Furst A, Pankotai T, et al. Nuclear position dictates DNA repair pathway choice. Genes Dev. 2014;28(22):2450–63. Epub 2014/11/05. doi: 10.1101/gad.248369.114 25366693; PubMed Central PMCID: PMC4233239.
22. Tsouroula K, Furst A, Rogier M, Heyer V, Maglott-Roth A, Ferrand A, et al. Temporal and Spatial Uncoupling of DNA Double Strand Break Repair Pathways within Mammalian Heterochromatin. Mol Cell. 2016;63(2):293–305. Epub 2016/07/12. doi: 10.1016/j.molcel.2016.06.002 27397684.
23. van Sluis M, McStay B. Nucleolar reorganization in response to rDNA damage. Curr Opin Cell Biol. 2017;46:81–6. Epub 2017/04/22. doi: 10.1016/j.ceb.2017.03.004 28431265.
24. Defossez PA, Prusty R, Kaeberlein M, Lin SJ, Ferrigno P, Silver PA, et al. Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol Cell. 1999;3(4):447–55. Epub 1999/05/07. doi: 10.1016/s1097-2765(00)80472-4 10230397.
25. Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, et al. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nature cell biology. 2007;9(8):923–31. Epub 2007/07/24. doi: 10.1038/ncb1619 17643116.
26. Stephens AD, Quammen CW, Chang B, Haase J, Taylor RM, 2nd, Bloom K. The spatial segregation of pericentric cohesin and condensin in the mitotic spindle. Mol Biol Cell. 2013;24(24):3909–19. Epub 2013/10/25. doi: 10.1091/mbc.E13-06-0325 24152737; PubMed Central PMCID: PMC3861086.
27. Lawrimore CJ, Bloom K. Common Features of the Pericentromere and Nucleolus. Genes. 2019;10(12). Epub 2019/12/15. doi: 10.3390/genes10121029 31835574.
28. Aze A, Sannino V, Soffientini P, Bachi A, Costanzo V. Centromeric DNA replication reconstitution reveals DNA loops and ATR checkpoint suppression. Nat Cell Biol. 2016;18(6):684–91. Epub 2016/04/26. doi: 10.1038/ncb3344 27111843; PubMed Central PMCID: PMC4939857.
29. Kabeche L, Nguyen HD, Buisson R, Zou L. A mitosis-specific and R loop-driven ATR pathway promotes faithful chromosome segregation. Science. 2018;359(6371):108–14. Epub 2017/11/25. doi: 10.1126/science.aan6490 29170278; PubMed Central PMCID: PMC5875943.
30. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, et al. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature. 2003;424(6952):1078–83. Epub 2003/08/29. doi: 10.1038/nature01900 12944972.
31. Hodgson B, Calzada A, Labib K. Mrc1 and Tof1 regulate DNA replication forks in different ways during normal S phase. Mol Biol Cell. 2007;18(10):3894–902. Epub 2007/07/27. doi: 10.1091/mbc.e07-05-0500 17652453; PubMed Central PMCID: PMC1995724.
32. Koshland D, Rutledge L, Fitzgerald-Hayes M, Hartwell LH. A genetic analysis of dicentric minichromosomes in Saccharomyces cerevisiae. Cell. 1987;48(5):801–12. Epub 1987/03/13. doi: 10.1016/0092-8674(87)90077-8 3545498.
33. Chang SC, Heacock PN, Clancey CJ, Dowhan W. The PEL1 gene (renamed PGS1) encodes the phosphatidylglycero-phosphate synthase of Saccharomyces cerevisiae. J Biol Chem. 1998;273(16):9829–36. Epub 1998/05/23. doi: 10.1074/jbc.273.16.9829 9545322.
34. Sfeir A, Symington LS. Microhomology-Mediated End Joining: A Back-up Survival Mechanism or Dedicated Pathway? Trends Biochem Sci. 2015;40(11):701–14. Epub 2015/10/07. doi: 10.1016/j.tibs.2015.08.006 26439531; PubMed Central PMCID: PMC4638128.
35. Bloom KS, Carbon J. Yeast centromere DNA is in a unique and highly ordered structure in chromosomes and small circular minichromosomes. Cell. 1982;29(2):305–17. doi: 10.1016/0092-8674(82)90147-7 6288253.
36. Funk M, Hegemann JH, Philippsen P. Chromatin digestion with restriction endonucleases reveals 150–160 bp of protected DNA in the centromere of chromosome XIV in Saccharomyces cerevisiae. Molecular & general genetics: MGG. 1989;219(1–2):153–60. Epub 1989/10/01. doi: 10.1007/BF00261171 2693939.
37. Jinks-Robertson S, Michelitch M, Ramcharan S. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Molecular and Cellular Biology. 1993;13(7):3937. doi: 10.1128/mcb.13.7.3937 8321201
38. Zhang Y, Hefferin ML, Chen L, Shim EY, Tseng HM, Kwon Y, et al. Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat Struct Mol Biol. 2007;14(7):639–46. Epub 2007/06/26. doi: 10.1038/nsmb1261 17589524.
39. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell. 2011;144(5):732–44. Epub 2011/03/01. doi: 10.1016/j.cell.2011.02.012 21353298; PubMed Central PMCID: PMC3417143.
40. Ryu T, Spatola B, Delabaere L, Bowlin K, Hopp H, Kunitake R, et al. Heterochromatic breaks move to the nuclear periphery to continue recombinational repair. Nat Cell Biol. 2015;17(11):1401–11. Epub 2015/10/27. doi: 10.1038/ncb3258 26502056; PubMed Central PMCID: PMC4628585.
41. Neff MW, Burke DJ. A delay in the Saccharomyces cerevisiae cell cycle that is induced by a dicentric chromosome and dependent upon mitotic checkpoints. Mol Cell Biol. 1992;12(9):3857–64. Epub 1992/09/01. doi: 10.1128/mcb.12.9.3857 1324407; PubMed Central PMCID: PMC360258.
42. Symington LS, Petes TD. Expansions and contractions of the genetic map relative to the physical map of yeast chromosome III. Molecular and Cellular Biology. 1988;8(2):595. doi: 10.1128/mcb.8.2.595 2832729
43. Yuan LW, Keil RL. Distance-independence of mitotic intrachromosomal recombination in Saccharomyces cerevisiae. Genetics. 1990;124(2):263–73. Epub 1990/02/01. 2407612; PubMed Central PMCID: PMC1203919.
44. Ahn BY, Dornfeld KJ, Fagrelius TJ, Livingston DM. Effect of limited homology on gene conversion in a Saccharomyces cerevisiae plasmid recombination system. Mol Cell Biol. 1988;8(6):2442–8. Epub 1988/06/01. doi: 10.1128/mcb.8.6.2442 3043177; PubMed Central PMCID: PMC363443.
45. Jackson JA, Fink GR. Gene conversion between duplicated genetic elements in yeast. Nature. 1981;292(5821):306–11. Epub 1981/07/23. doi: 10.1038/292306a0 6265790.
46. Klein HL, Petes TD. Intrachromosomal gene conversion in yeast. Nature. 1981;289(5794):144–8. Epub 1981/01/15. doi: 10.1038/289144a0 7005693.
47. Schiestl RH, Igarashi S, Hastings PJ. Analysis of the mechanism for reversion of a disrupted gene. Genetics. 1988;119(2):237–47. 2840335.
48. Cho JE, Jinks-Robertson S. Deletions associated with stabilization of the Top1 cleavage complex in yeast are products of the nonhomologous end-joining pathway. Proc Natl Acad Sci U S A. 2019;116(45):22683–91. Epub 2019/10/23. doi: 10.1073/pnas.1914081116 31636207; PubMed Central PMCID: PMC6842612.
49. Sorenson KS, Mahaney BL, Lees-Miller SP, Cobb JA. The non-homologous end-joining factor Nej1 inhibits resection mediated by Dna2-Sgs1 nuclease-helicase at DNA double strand breaks. J Biol Chem. 2017;292(35):14576–86. Epub 2017/07/07. doi: 10.1074/jbc.M117.796011 28679532; PubMed Central PMCID: PMC5582849.
50. Alabert C, Bianco JN, Pasero P. Differential regulation of homologous recombination at DNA breaks and replication forks by the Mrc1 branch of the S-phase checkpoint. Embo j. 2009;28(8):1131–41. Epub 2009/03/27. doi: 10.1038/emboj.2009.75 19322196; PubMed Central PMCID: PMC2683710.
51. Fabre F, Chan A, Heyer WD, Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc Natl Acad Sci U S A. 2002;99(26):16887–92. Epub 2002/12/12. doi: 10.1073/pnas.252652399 12475932; PubMed Central PMCID: PMC139239.
52. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell. 2008;134(6):981–94. Epub 2008/09/23. doi: 10.1016/j.cell.2008.08.037 18805091; PubMed Central PMCID: PMC2662516.
53. Onaka AT, Su J, Katahira Y, Tang C, Zafar F, Aoki K, et al. DNA replication machinery prevents Rad52-dependent single-strand annealing that leads to gross chromosomal rearrangements at centromeres. Commun Biol. 2020;3(1):202. Epub 2020/05/02. doi: 10.1038/s42003-020-0934-0 32355220; PubMed Central PMCID: PMC7193609.
54. Greenfeder SA, Newlon CS. Replication forks pause at yeast centromeres. Molecular and cellular biology. 1992;12(9):4056–66. Epub 1992/09/01. doi: 10.1128/mcb.12.9.4056 1508202; PubMed Central PMCID: PMC360298.
55. Boddy MN, Russell P. DNA replication checkpoint. Curr Biol. 2001;11(23):R953–6. Epub 2001/12/01. doi: 10.1016/s0960-9822(01)00572-3 11728320.
56. Sims J, Copenhaver GP, Schlogelhofer P. Meiotic DNA Repair in the Nucleolus Employs a Nonhomologous End-Joining Mechanism. Plant Cell. 2019;31(9):2259–75. Epub 2019/07/04. doi: 10.1105/tpc.19.00367 31266898; PubMed Central PMCID: PMC6751124.
57. Harding SM, Boiarsky JA, Greenberg RA. ATM Dependent Silencing Links Nucleolar Chromatin Reorganization to DNA Damage Recognition. Cell Rep. 2015;13(2):251–9. Epub 2015/10/07. doi: 10.1016/j.celrep.2015.08.085 26440899; PubMed Central PMCID: PMC4607662.
58. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nature biotechnology. 2011;29(1):24–6. doi: 10.1038/nbt.1754 21221095.
59. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics. 2012;14(2):178–92. doi: 10.1093/bib/bbs017 22517427
Článek vyšel v časopise
PLOS Genetics
2021 Číslo 3
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- DNA polymerase theta suppresses mitotic crossing over
- IKAROS is required for the measured response of NOTCH target genes upon external NOTCH signaling
- activin-2 is required for regeneration of polarity on the planarian anterior-posterior axis
- The etiology of Down syndrome: Maternal MCM9 polymorphisms increase risk of reduced recombination and nondisjunction of chromosome 21 during meiosis I within oocyte