Cytokinesis breaks dicentric chromosomes preferentially at pericentromeric regions and telomere fusions

Genes and Development

Volumn 29, Issue 3, 2015, Pages 322-336

  Lopez, Virginia ^a,b   Barinova, Natalja ^a,b   Onishi, Masayuki ^c   Pobiega, Sabrina ^a,b   Pringle, John R ^c   Dubrana, Karine ^a,b   Marcand, Stéphane ^a,b  

^a INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^b INSERM   (France)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell cycle exit; Centromere; Chromosome; Cytokinesis; Telomere

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE;

ANAPHASE; ARTICLE; CELL CYCLE; CENTROMERE; CYTOKINESIS; DICENTRIC CHROMOSOME; DNA STRAND BREAKAGE; MITOSIS SPINDLE; NONHUMAN; PRIORITY JOURNAL; SPINDLE POLE BODY; TELOMERE; CHROMOSOME; CHROMOSOME BREAKAGE; GENETICS; METABOLISM; MITOSIS; NUCLEAR DIVISION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCETALES;

CELL NUCLEUS DIVISION; CENTROMERE; CHROMOSOME BREAKAGE; CHROMOSOMES, FUNGAL; CYTOKINESIS; MITOSIS; SACCHAROMYCES CEREVISIAE; TELOMERE;

EID: 84961290258     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.254664.114     Document Type: Article

References (75)

1. Akiyoshi B, Sarangapani KK, Powers AF, Nelson CR, Reichow SL, Arellano-Santoyo H, Gonen T, Ranish JA, Asbury CL, Biggins S. 2010. Tension directly stabilizes reconstituted kinetochore-microtubule attachments. Nature 468: 576-579.
2. Avarello R, Pedicini A, Caiulo A, Zuffardi O, Fraccaro M. 1992. Evidence for an ancestral alphoid domain on the long arm of human chromosome 2. Hum Genet 89: 247-249.
3. Bajer A. 1964. Cine-micrographic studies on dicentric chromosomes. Chromosoma 15: 630-651.
4. Baxter J, Diffley JF. 2008. Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast. Mol Cell 30: 790-802.
5. Bi E, Maddox P, Lew DJ, Salmon ED, McMillan JN, Yeh E, Pringle JR. 1998. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J Cell Biol 142: 1301-1312.
6. Biebricher A, Hirano S, Enzlin JH, Wiechens N, Streicher WW, Huttner D, Wang LHC, Nigg EA, Owen-Hughes T, Liu Y, et al. 2013. PICH: a DNA translocase specially adapted for processing anaphase bridge DNA. Mol Cell 51: 691-701.
7. Chen X, Niu H, Chung W-H, Zhu Z, Papusha A, Shim EY, Lee SE, Sung P, Ira G. 2011. Cell cycle regulation of DNA doublestrand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 18: 1015-1019.
8. Ciullo M, Debily M-A, Rozier L, Autiero M, Billault A, Mayau V, Marhomy El S, Guardiola J, Bernheim A, Coullin P, et al. 2002. Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: the model of PIP gene duplication from a break at FRA7I. Hum Mol Genet 11: 2887-2894.
9. Croll D, Zala M, McDonald BA. 2013. Breakage-fusion-bridge cycles and large insertions contribute to the rapid evolution of accessory chromosomes in a fungal pathogen. PLoS Genet 9: e1003567.
10. Cuylen S, Metz J, Hruby A, Haering CH. 2013. Entrapment of chromosomes by condensin rings prevents their breakage during cytokinesis. Dev Cell 27: 469-478.
11. Denchi EL, Celli G, de Lange T. 2006. Hepatocytes with extensive telomere deprotection and fusion remain viable and regenerate liver mass through endoreduplication. Genes Dev 20: 2648-2653.
12. Dimitrov LN, Brem RB, Kruglyak L, Gottschling DE. 2009. Polymorphisms in multiple genes contribute to the spontaneous mitochondrial genome instability of Saccharomyces cerevisiae S288C strains. Genetics 183: 365-383.
13. Dubarry M, Loıodice I, Chen CL, Thermes C, Taddei A. 2011. Tight protein-DNA interactions favor gene silencing. Genes Dev 25: 1365-1370.
14. Elia N, Ott C, Lippincott-Schwartz J. 2013. Incisive imaging and computation for cellular mysteries: lessons from abscission. Cell 155: 1220-1231.
15. Fisher JK, Ballenger M, O’Brien ET, Haase J, Superfine R, Bloom K. 2009. DNA relaxation dynamics as a probe for the intracellular environment. Proc Natl Acad Sci 106: 9250-9255.
16. Gascoigne KE, Cheeseman IM. 2013. Induced dicentric chromosome formation promotes genomic rearrangements and tumorigenesis. Chromosome Res 21: 407-418.
17. Hill A, Bloom K. 1987. Genetic manipulation of centromere function. Mol Cell Biol 7: 2397-2405.
18. Hirano T, Funahashi S, Uemura T, Yanagida M. 1986. Isolation and characterization of Schizosaccharomyces pombe cutmutants that block nuclear division but not cytokinesis. EMBO J 5: 2973-2979.
19. Ishii K, Ogiyama Y, Chikashige Y, Soejima S, Masuda F, Kakuma T, Hiraoka Y, Takahashi K. 2008. Heterochromatin integrity affects chromosome reorganization after centromere dysfunction. Science 321: 1088-1091.
20. Jones RE, Oh S, Grimstead JW, Zimbric J, Roger L, Heppel NH, Ashelford KE, Liddiard K, Hendrickson EA, Baird DM. 2014. Escape from telomere-driven crisis is DNA ligase III dependent. Cell Reports 8: 1063-1076.
21. Kitamura E, Tanaka K, Kitamura Y, Tanaka TU. 2007. Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev 21: 3319-3330.
22. Ko N, Nishihama R, Tully GH, Ostapenko D, Solomon MJ, Morgan DO, Pringle JR. 2007. Identification of yeast IQGAP (Iqg1p) as an anaphase-promoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol Biol Cell 18: 5139-5153.
23. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE. 1994. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol Cell Biol 14: 1293-1301.
24. Kruithof M, Chien F-T, Routh A, Logie C, Rhodes D, van Noort J. 2009. Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fiber. Nat Struct Mol Biol 16: 534-540.
25. Lee SE, Paques F, Sylvan J, Haber JE. 1999. Role of yeast SIR genes and mating type in directing DNA double-strand breaks to homologous and non-homologous repair paths. Curr Biol 9: 767-770.
26. Lei X, Hu J, Fang H. 2010. Radial compression property of ds-DNA molecules studied by a mesoscale model. Europhys Lett 89: 48003.
27. Lejeune J, Dutrillaux B, Rethore MO, Prieur M. 1973. [Comparison of the structure of chromatids of Homo sapiens and Pan troglodytes (author’s transl)]. Chromosoma 43: 423-444.
28. Li Y, Schwab C, Ryan SL, Papaemmanuil E, Robinson HM, Jacobs P, Moorman AV, Dyer S, Borrow J, Griffiths M, et al. 2014. Constitutional and somatic rearrangement of chromosome 21 in acute lymphoblastic leukaemia. Nature 508: 98-102.
29. Lobachev KS, Gordenin DA, Resnick MA. 2002. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108: 183-193.
30. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
31. Mackinnon RN, Campbell LJ. 2011. The role of dicentric chromosome formation and secondary centromere deletion in the evolution of myeloid malignancy. Genet Res Int 2011: 643-628.
32. Mann C, Davis RW. 1983. Instability of dicentric plasmids in yeast. Proc Natl Acad Sci 80: 228-232.
33. Marcand S. 2014. How do telomeres and NHEJ coexist? Mol Cell Oncol. doi: 10.4161/23723548.963438.
34. Marco E, Dorn JF, Hsu P-H, Jaqaman K, Sorger PK, Danuser G. 2013. S. cerevisiae chromosomes biorient via gradual resolution of syntely between S phase and anaphase. Cell 154: 1127-1139.
35. Marko JF. 2008. Micromechanical studies of mitotic chromosomes. Chromosome Res 16: 469-497.
36. Marotta M, Chen X, Watanabe T, Faber PW, Diede SJ, Tapscott S, Tubbs R, Kondratova A, Stephens R, Tanaka H. 2013. Homology-mediated end-capping as a primary step of sister chromatid fusion in the breakage-fusion-bridge cycles. Nucleic Acids Res 41: 9732-9740.
37. Martínez A C, van Wely KHM. 2011. Centromere fission, not telomere erosion, triggers chromosomal instability in human carcinomas. Carcinogenesis 32: 796-803.
38. McClintock B. 1941. The stability of broken ends of chromosomes in Zea Mays. Genetics 26: 234-282.
39. McGrew JT, Goetsch L, Byers B, Baum P. 1992. Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae. Mol Biol Cell 3: 1443-1454.
40. McMurray MA, Stefan X, Wemmer M, Odorizzi G, Emr SD, Thomer J. 2011. Genetic interactions with mutations affecting septin assembly reveal ESeRT functions in budding yeast cytokinesis. Biol Chem 392: 699-712.
41. Mizuno K, Lambert S, Baldacci G, Murray JM, Carr AM. 2009. Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev 23: 2876-2886.
42. Mizuno K, Miyabe I, Schalbetter SA, Carr AM, Murray JM. 2013. Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 493: 246-249.
43. Morawska M, Ulrich HD. 2013. An expanded tool kit for the auxin-inducible degron system in budding yeast. Yeast 30: 341-351.
44. Murnane JP, Sabatier L. 2004. Chromosome rearrangements resulting from telomere dysfunction and their role in cancer. BioEssays 26: 1164-1174.
45. Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y. 2006. The nocut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 125: 85-98.
46. Onishi M, Ko N, Nishihama R, Pringle JR. 2013. Distinct roles of Rho1, Cdc42, and Cyk3 in septum formation and abscission during yeast cytokinesis. J Cell Biol 202: 311-329.
47. Pampalona J, Frías C, Genescà A, Tusell L. 2012. Progressive telomere dysfunction causes cytokinesis failure and leads to the accumulation of polyploid cells. PLoS Genet 8: e1002679.
48. Panja D, Barkema GT, Kolomeisky AB. 2013. Through the eye of the needle: recent advances in understanding biopolymer translocation. J Phys Condens Matter 25: 413101.
49. Pennaneach V, Kolodner RD. 2009. Stabilization of dicentric translocations through secondary rearrangements mediated by multiple mechanisms in S. cerevisiae. PLoS ONE 4: e6389.
50. Pinto IM, Rubinstein B, Kucharavy A, Unruh JR, Li R. 2012. Actin depolymerization drives actomyosin ring contraction during budding yeast cytokinesis. Dev Cell 22: 1247-1260.
51. Pobiega S, Marcand S. 2010. Dicentric breakage at telomere fusions. Genes Dev 24: 720-733.
52. Pollard LW, Onishi M, Pringle JR, Lord M. 2012. Fission yeast Cyk3p is a transglutaminase-like protein that participates in cytokinesis and cell morphogenesis. Mol Biol Cell 23: 2433-2444.
53. Renshaw MJ, Ward JJ, Kanemaki M, Natsume K, Nédélec FJ, Tanaka TU. 2010. Condensins promote chromosome recoiling during early anaphase to complete sister chromatid separation. Dev Cell 19: 232-244.
54. Sabatier L, Ricoul M, Pottier G, Murnane JP. 2005. The loss of a single telomere can result in instability of multiple chromosomes in a human tumor cell line. Mol Cancer Res 3: 139-150.
55. Sato H, Masuda F, Takayama Y, Takahashi K, Saitoh S. 2012. Epigenetic inactivation and subsequent heterochromatinization of a centromere stabilize dicentric chromosomes. Curr Biol 22: 658-667.
56. Selvarajah S, Yoshimoto M, Park PC, Maire G, Paderova J, Bayani J, Lim G, Al-Romaih K, Squire JA, Zielenska M. 2006. The breakage-fusion-bridge (BFB) cycle as amechanism for generating genetic heterogeneity in osteosarcoma. Chromosoma 115: 459-467.
57. Shimizu N, Shingaki K, Kaneko-Sasaguri Y, Hashizume T, Kanda T. 2005. When, where and how the bridge breaks: anaphase bridge breakage plays a crucial role in gene amplification and HSR generation. Exp Cell Res 302: 233-243.
58. Song W, Gawel M, Dominska M, Greenwell PW, Hazkani-Covo E, Bloom K, Petes TD. 2013. Nonrandom distribution of interhomolog recombination events induced by breakage of a dicentric chromosome in Saccharomyces cerevisiae. Genetics 194: 69-80.
59. Sorzano COS, Pascual-Montano A, Sànchez de Diego A, Martínez A C, van Wely KHM. 2013. Chromothripsis: breakage-fusion-bridge over and over again. Cell Cycle 12: 2016-2023.
60. Stewénius Y, Gorunova L, Jonson T, Larsson N, Höglund M, Mandahl N, Mertens F, Mitelman F, Gisselsson D. 2005. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc Natl Acad Sci 102: 5541-5546.
61. Stimpson KM, Sullivan BA. 2010. Epigenomics of centromere assembly and function. Curr Opin Cell Biol 22: 772-780.
62. Stimpson KM, Song IY, Jauch A, Holtgreve-Grez H, Hayden KE, Bridger JM, Sullivan BA. 2010. Telomere disruption results in non-random formation of de novo dicentric chromosomes involving acrocentric human chromosomes. PLoS Genet 6: e1001061.
63. Stimpson KM, Matheny JE, Sullivan BA. 2012. Dicentric chromosomes: unique models to study centromere function and inactivation. Chromosome Res 20: 595-605.
64. Suto Y, Hirai M, Akiyama M, Kobashi G, Itokawa M, Akashi M, Sugiura N. 2013. Biodosimetry of restoration workers for the Tokyo Electric Power Company (TEPCO) Fukushima Daiichi Nuclear Power Station aAccident. Health Phys 105: 366-373.
65. Symington LS. 2014. End resection at double-strand breaks: mechanism and regulation. Cold Spring Harb Perspect Biol 6: a016436.
66. Tanaka K, Mukae N, Dewar H, van Breugel M, James EK, Prescott AR, Antony C, Tanaka TU. 2005. Molecular mechanisms of kinetochore capture by spindle microtubules. Nature 434: 987-994.
67. Thrower DA, Bloom K. 2001. Dicentric chromosome stretching during anaphase reveals roles of Sir2/Ku in chromatin compaction in budding yeast. Mol Biol Cell 12: 2800-2812.
68. Tolliday N, Pitcher M, Li R. 2003. Direct evidence for a critical role of myosin II in budding yeast cytokinesis and the evolvability of new cytokinetic mechanisms in the absence of myosin II. Mol Biol Cell 14: 798-809.
69. van Steensel B, Smogorzewska A, de Lange T. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92: 401-413.
70. Weiss EL. 2012. Mitotic exit and separation of mother and daughter cells. Genetics 192: 1165-1202.
71. Westmoreland J, Ma W, Yan Y, Van Hulle K, Malkova A, Resnick MA. 2009. RAD50 is required for efficient initiation of resection and recombinational repair at random, g-induced double-strand break ends. PLoS Genet 5: e1000656.
72. Wloka C, Bi E. 2012. Mechanisms of cytokinesis in budding yeast. Cytoskeleton 69: 710-726.
73. Woodruff JB, Drubin DG, Barnes G. 2009. Dynein-driven mitotic spindle positioning restricted to anaphase by She1p inhibition of dynactin recruitment. Mol Biol Cell 20: 3003-3011.
74. Woodruff JB, Drubin DG, Barnes G. 2010. Mitotic spindle disassembly occurs via distinct subprocesses driven by the anaphase-promoting complex, Aurora B kinase, and kinesin-8. J Cell Biol 191: 795-808.
75. Zierhut C, Diffley JFX. 2008. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J 27: 1875-1885.