DNA damage to a single chromosome end delays anaphase onset

Journal of Biological Chemistry

Volumn 289, Issue 33, 2014, Pages 22771-22784

  Alcaraz Silva, Bárbara ^a,b   Stambaugh, Jessica R ^a   Yokomori, Kyoko ^d   Shah, Jagesh V ^e   Berns, Michael W ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California at Irvine   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; NUCLEIC ACIDS; PROTEINS; REPAIR;

ATAXIA-TELANGIECTASIA MUTATED; CELL-CYCLE ARREST; DNA DAMAGE RESPONSE; DNA DAMAGES; HIGHER FREQUENCIES; KIDNEY EPITHELIAL CELL; SPINDLE-ASSEMBLY; TELOMERES;

CHROMOSOMES;

53BP1 PROTEIN; ATM PROTEIN; ATR PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 1; FANCONI ANEMIA GROUP D2 PROTEIN; KU ANTIGEN; MDC1 PROTEIN; MPS1 KINASE; NIBRIN; NUCLEIC ACID BINDING PROTEIN; PROTEIN KINASE; PROTEIN KU80; UBIQUITIN; UNCLASSIFIED DRUG; WERNER SYNDROME PROTEIN; EXODEOXYRIBONUCLEASE; FOCAL ADHESION KINASE 2; HISTONE;

ANAPHASE; ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL DAMAGE; CHROMOSOME; CHROMOSOME ENDS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA DAMAGE RESPONSE; EPITHELIUM CELL; FEMALE; IRRADIATION; KIDNEY EPITHELIUM; MALE; MICRONUCLEUS; MITOSIS; MITOSIS SPINDLE; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; ANIMAL; CELL LINE; CYTOLOGY; KIDNEY; LASER; METABOLISM; PHOSPHORYLATION; RAT KANGAROO;

ANAPHASE; ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE; CHROMOSOMES, MAMMALIAN; DNA DAMAGE; EPITHELIAL CELLS; EXODEOXYRIBONUCLEASES; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FOCAL ADHESION KINASE 2; HISTONES; KIDNEY; LASERS; PHOSPHORYLATION; POTOROIDAE; PROTEIN KINASES;

EID: 84905988461     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.535955     Document Type: Article

References (75)

1. Berns, M. W. (1974) Directed chromosome loss by laser microirradiation. Science 186, 700-705
2. Phillips, J. W., and Morgan, W. F. (1994) Illegitimate recombination induced by DNA double-strand breaks in a mammalian chromosome. Mol. Cell. Biol. 14, 5794-5803 (Pubitemid 24264408)
3. Richardson, C., and Jasin, M. (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405, 697-700 (Pubitemid 30428657)
4. Pfeiffer, P., Goedecke, W., and Obe, G. (2000) Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 15, 289-302 (Pubitemid 30612188)
5. Noon, A. T., and Goodarzi, A. A. (2011) 53BP1-mediated DNA double strand break repair: insert bad pun here. DNA Repair 10, 1071-1076
6. Takai, H., Smogorzewska, A., and de Lange, T. (2003)DNA damage foci at dysfunctional telomeres. Curr. Biol. 13, 1549-1556 (Pubitemid 37078413)
7. Xiao, W., and Samson, L. (1993) In vivo evidence for endogenous DNA alkylation damage as a source of spontaneous mutation in eukaryotic cells. Proc. Natl. Acad. Sci. U.S.A. 90, 2117-2121 (Pubitemid 23078576)
8. Shigenaga, M. K., Gimeno, C. J., and Ames, B. N. (1989) Urinary 8-hy-droxy- 2′-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc. Natl. Acad. Sci. U.S.A. 86, 9697-9701 (Pubitemid 20030700)
9. Blackburn, E. H. (2001) Switching and signaling at the telomere. Cell 106, 661-673
10. de Lange, T. (2002) Protection of mammalian telomeres. Oncogene 21, 532-540
11. Greider, C. W. (1999) Telomeres do D-loop-T-loop. Cell 97, 419-422
12. Palm, W., and de Lange, T. (2008) How shelterin protects mammalian telomeres. Annu. Rev. Genet. 42, 301-334
13. Wright, W. E., and Shay, J. W. (2005) Telomere-binding factors and general DNA repair. Nat. Genet. 37, 116-118
14. Hockemeyer, D., Sfeir, A. J., Shay, J. W., Wright, W. E., and de Lange, T. (2005) POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24, 2667-2678 (Pubitemid 41076322)
15. Bailey, S. M., Meyne, J., Chen, D. J., Kurimasa, A., Li, G. C., Lehnert, B. E., and Goodwin, E. H. (1999) DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. U.S.A. 96, 14899-14904 (Pubitemid 30019737)
16. Yang, Q., Zheng, Y. L., and Harris, C. C. (2005) POT1 and TRF2 cooperate to maintain telomeric integrity. Mol. Cell. Biol. 25, 1070-1080 (Pubitemid 40165813)
17. d'Adda di Fagagna, F., Reaper, P. M., Clay-Farrace, L., Fiegler, H., Carr, P., Von Zglinicki, T., Saretzki, G., Carter, N. P., and Jackson, S. P. (2003) A DNA damage checkpoint response in telomere-initiated senescence. Nature 426, 194-198 (Pubitemid 37442589)
18. Verdun, R. E., Crabbe, L., Haggblom, C., and Karlseder, J. (2005) Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 20, 551-561 (Pubitemid 41668640)
19. Fumagalli, M., Rossiello, F., Clerici, M., Barozzi, S., Cittaro, D., Kaplunov, J. M., Bucci, G., Dobreva, M., Matti, V., Beausejour, C. M., Herbig, U., Longhese, M. P., and d'Adda di Fagagna, F. (2012) Telomeric DNA damage is irreparable and causes persistent DNA-damage-response activation. Nat. Cell Biol. 14, 355-365
20. Thanasoula, M., Escandell, J. M., Suwaki, N., and Tarsounas, M. (2012) ATM/ATR checkpoint activation downregulates CDC25C to prevent mitotic entry with uncapped telomeres. EMBO J. 31, 3398-3410
21. Giunta, S., Belotserkovskaya, R., and Jackson, S. P. (2010) DNA damage signaling in response to double-strand breaks during mitosis. J. Cell Biol. 190, 197-207
22. Peterson, S. E., Li, Y., Chait, B. T., Gottesman, M. E., Baer, R., and Gautier, J. (2011) Cdk1 uncouples CtIP-dependent resection and Rad51 filament formation during M-phase double-strand break repair. J. Cell Biol. 194, 705-720
23. Orthwein, A., Fradet-Turcotte, A., Noordermeer, S. M., Canny, M. D., Brun, C. M., Strecker, J., Escribano-Diaz, C., and Durocher, D. (2014) Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344, 189-193
24. Cesare, A. J., Hayashi, M. T., Crabbe, L., and Karlseder, J. (2013) The telomere deprotection response is functionally distinct from the genomic DNA damage response. Mol. Cell 51, 141-155
25. Hayashi, M. T., Cesare, A. J., Fitzpatrick, J. A., Lazzerini-Denchi, E., and Karlseder, J. (2012) A telomere-dependent DNA damage checkpoint induced by prolonged mitotic arrest. Nat. Struct. Mol. Biol. 19, 387-394
26. Ferrando-May, E., Tomas, M., Blumhardt, P., Stöckl, M., Fuchs, M., and Leitenstorfer, A. (2013) Highlighting the DNA damage response with ultrashort laser pulses in the near infrared and kinetic modeling. Front. Genet. 4, 135
27. Gomez-Godinez, V., Wu, T., Sherman, A. J., Lee, C. S., Liaw, L. H., Zhongsheng, Y., Yokomori, K., and Berns, M. W. (2010) Analysis of DNA doublestrand break response and chromatin structure in mitosis using laser microirradiation. Nucleic Acids Res. 38, e202
28. Kong, X., Mohanty, S. K., Stephens, J., Heale, J. T., Gomez-Godinez, V., Shi, L. Z., Kim, J. S., Yokomori, K., and Berns, M. W. (2009) Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res. 37, e68
29. Botchway, S. W., Reynolds, P., Parker, A. W., and O'Neill, P. (2010) Use of near infrared femtosecond lasers as sub-micron radiation microbeam for cell DNA damage and repair studies. Mutat. Res. 704, 38-44
30. Träutlein, D., Deibler, M., Leitenstorfer, A., and Ferrando-May, E. (2010) Specific local induction of DNA strand breaks by infrared multi-photon absorption. Nucleic Acids Res. 38, e14
31. Mari, P. O., Florea, B. I., Persengiev, S. P., Verkaik, N. S., Brüggenwirth, H. T., Modesti, M., Giglia-Mari, G., Bezstarosti, K., Demmers, J. A., Luider, T. M., Houtsmuller, A. B., and van Gent, D. C. (2006) Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. U.S.A. 103, 18597-18602 (Pubitemid 44913456)
32. Hartlerode, A. J., Guan, Y., Rajendran, A., Ura, K., Schotta, G., Xie, A., Shah, J. V., and Scully, R. (2012) Impact of histone H4 lysine 20 methylation on 53BP1 responses to chromosomal double strand breaks. PLoS One 7, e49211
33. Silva, B. A., Stambaugh, J. R., and Berns, M. W. (2013) Targeting telomere-containing chromosome ends with a near-infrared femtosecond laser to study the activation of the DNA damage response and DNA damage repair pathways. J. Biomed. Opt. 18, 095003
34. Altmann, S. C. A., and Ellery, M. E. W. (1925) The chromosomes of four species of marsupials. Q. J. Microsc. Sci. 69, 463-469
35. Stout, J. R., Rizk, R. S., Kline, S. L., and Walczak, C. E. (2006) Deciphering protein function during mitosis in PtK cells using RNAi. BMCCell Biol. 7, 26
36. Baker, N. M., Zeitlin, S. G., Shi, L. Z., Shah, J., and Berns, M. W. (2010) Chromosome tips damaged in anaphase inhibit cytokinesis. PLoS One 5, e12398
37. Holland, A. J., Fachinetti, D., Han, J. S., and Cleveland, D. W. (2012) Inducible, reversible system for the rapid and complete degradation of proteins in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 109, E3350-E3357
38. Dimitrova, N., Chen, Y. C., Spector, D. L., and de Lange, T. (2008) 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528 (Pubitemid 50304845)
39. Shah, J. V., Botvinick, E., Bonday, Z., Furnari, F., Berns, M., and Cleveland, D. W. (2004) Dynamics of centromere and kinetochore proteins: implications for checkpoint signaling and silencing. Curr. Biol. 14, 942-952 (Pubitemid 38722608)
40. Duquette, M. L., Zhu, Q., Taylor, E. R., Tsay, A. J., Shi, L. Z., Berns, M. W., and McGowan, C. H. (2012) CtIP is required to initiate replication-dependent interstrand crosslink repair. PLoS Genet. 8, e1003050
41. Botvinick, E. L., and Berns, M. W. (2005) Internet-based robotic laser scissors and tweezers microscopy. Microsc. Res. Tech. 68, 65-74 (Pubitemid 41566388)
42. Heale, J. T., Ball, A. R., Jr., Schmiesing, J. A., Kim, J. S., Kong, X., Zhou, S., Hudson, D. F., Earnshaw, W. C., and Yokomori, K. (2006) Condensin I interacts with the PARP-1-XRCC1 complex and functions in DNA single strand break repair. Mol. Cell 21, 837-848 (Pubitemid 43376133)
43. Santaguida, S., Tighe, A., D'Alise, A. M., Taylor, S. S., and Musacchio, A. (2010) Dissecting the role of MPS1 in chromosome biorientation and the spindle checkpoint through the small molecule inhibitor reversine. J. Cell Biol. 190, 73-87
44. Terradas, M., Martín, M., Tusell, L., and Genescá, A. (2009) DNA lesions sequestered in micronuclei induce a local defective-damage response. DNA Repair 8, 1225-1234
45. Thanasoula, M., Escandell, J. M., Martinez, P., Badie, S., Muñoz, P., Blasco, M. A., and Tarsounas, M. (2010) p53 prevents entry into mitosis with uncapped telomeres. Curr. Biol. 20, 521-526
46. Shang, Z. F., Huang, B., Xu, Q. Z., Zhang, S. M., Fan, R., Liu, X. D., Wang, Y., and Zhou, P. K. (2010) Inactivation of DNA-dependent protein kinase leads to spindle disruption and mitotic catastrophe with attenuated checkpoint protein 2 phosphorylation in response to DNA damage. Cancer Res. 70, 3657-3666
47. Shang, Z., Yu, L., Lin, Y. F., Matsunaga, S., Shen, C. Y., and Chen, B. P. (2014) DNA-PKcs activates the Chk2-Brca1 pathway during mitosis to ensure chromosomal stability. Oncogenesis 3, e85
48. Wang, B., and Elledge, S. J. (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 104, 20759-20763
49. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C., and Lukas, J. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900 (Pubitemid 350138084)
50. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D. H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., Lukas, J., and Lukas, C. (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446
51. Zachos, G., Black, E. J., Walker, M., Scott, M. T., Vagnarelli, P., Earnshaw, W. C., and Gillespie, D. A. (2007) Chk1 is required for spindle checkpoint function. Dev. Cell 12, 247-260 (Pubitemid 46193970)
52. Kops, G. J., and Shah, J. V. (2012) Connecting up and clearing out: how kinetochore attachment silences the spindle assembly checkpoint. Chromosoma 121, 509-525
53. Kwiatkowski, N., Jelluma, N., Filippakopoulos, P., Soundararajan, M., Manak, M. S., Kwon, M., Choi, H. G., Sim, T., Deveraux, Q. L., Rottmann, S., Pellman, D., Shah, J. V., Kops, G. J., Knapp, S., and Gray, N. S. (2010) Small-molecule kinase inhibitors provide insight into Mps1 cell cycle function. Nat. Chem. Biol. 6, 359-368
54. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R., 3rd, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Solimini, N., Lerenthal, Y., Shiloh, Y., Gygi, S. P., and Elledge, S. J. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (Pubitemid 46877472)
55. Eliezer, Y., Argaman, L., Kornowski, M., Roniger, M., and Goldberg, M. (2014) Interplay between the DNA damage proteins MDC1 and ATM in the regulation of the spindle assembly checkpoint. J. Biol. Chem. 289, 8182-8193
56. Musarò, M., Ciapponi, L., Fasulo, B., Gatti, M., and Cenci, G. (2008) Unprotected Drosophila melanogaster telomeres activate the spindle assembly checkpoint. Nat. Genet. 40, 362-366 (Pubitemid 351311761)
57. Valerio-Santiago, M., de Los Santos-Velázquez, A. I., and Monje-Casas, F. (2013) Inhibition of the mitotic exit network in response to damaged telomeres. PLoS Genet. 9, e1003859
58. Mikhailov, A., Cole, R. W., and Rieder, C. L. (2002) DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Curr. Biol. 12, 1797-1806 (Pubitemid 35273899)
59. Smits, V. A., Klompmaker, R., Arnaud, L., Rijksen, G., Nigg, E. A., and Medema, R. H. (2000) Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol. 2, 672-676
60. Chow, J. P., Siu, W. Y., Fung, T. K., Chan, W. M., Lau, A., Arooz, T., Ng, C. P., Yamashita, K., and Poon, R. Y. (2003) DNA damage during the spindle-assembly checkpoint degrades CDC25A, inhibits cyclin-CDC2 complexes, and reverses cells to interphase. Mol. Biol. Cell 14, 3989-4002 (Pubitemid 37186303)
61. Sibon, O. C., Kelkar, A., Lemstra, W., and Theurkauf, W. E. (2000) DNA replication/ DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat. Cell Biol. 2, 90-95
62. Su, T. T., and Jaklevic, B. (2001) DNA damage leads to a cyclin A-dependent delay in metaphase-anaphase transition in the Drosophila gastrula. Curr. Biol. 11, 8-17 (Pubitemid 32062710)
63. Tinker-Kulberg, R. L., and Morgan, D. O. (1999) Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage. Genes Dev. 13, 1936-1949
64. Dotiwala, F., Harrison, J. C., Jain, S., Sugawara, N., and Haber, J. E. (2010) Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr. Biol. 20, 328-332
65. Kim, E. M., and Burke, D. J. (2008) DNA damage activates the SAC in an ATM/ATR-dependent manner, independently of the kinetochore. PLoS Genet. 4, e1000015
66. Albrecht, D. R., Underhill, G. H., Resnikoff, J., Mendelson, A., Bhatia, S. N., and Shah, J. V. (2010) Microfluidics-integrated time-lapse imaging for analysis of cellular dynamics. Integr. Biol. (Camb.) 2, 278-287
67. Yu, B., Dalton, W. B., and Yang, V. W. (2012) CDK1 regulates mediator of DNA damage checkpoint 1 (MDC1) during mitotic DNA damage. Cancer Res. 72, 5448-5453
68. Imamura, O., Fujita, K., Itoh, C., Takeda, S., Furuichi, Y., and Matsumoto, T. (2002) Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene 21, 954-963 (Pubitemid 34146309)
69. Eller, M. S., Liao, X., Liu, S., Hanna, K., Bäckvall, H., Opresko, P. L., Bohr, V. A., and Gilchrest, B. A. (2006) A role for WRN in telomere-based DNA damage responses. Proc. Natl. Acad. Sci. U.S.A. 103, 15073-15078 (Pubitemid 44583166)
70. Mendez-Bermudez, A., Hidalgo-Bravo, A., Cotton, V. E., Gravani, A., Jeyapalan, J. N., and Royle, N. J. (2012) The roles of WRN and BLM RecQ helicases in the alternative lengthening of telomeres. Nucleic Acids Res. 40, 10809-10820
71. Fan, Q., Zhang, F., Barrett, B., Ren, K., and Andreassen, P. R. (2009) A role for monoubiquitinated FANCD2 at telomeres in ALT cells. Nucleic Acids Res. 37, 1740-1754
72. Reynolds, P., Botchway, S. W., Parker, A. W., and O'Neill, P. (2013) Spatiotemporal dynamics of DNA repair proteins following laser microbeam induced DNA damage: when is a DSB not a DSB? Mutat. Res. 756, 14-20
73. Yan, Q., Xu, R., Zhu, L., Cheng, X., Wang, Z., Manis, J., and Shipp, M. A. (2013) BAL1 and its partner E3 ligase, BBAP, link poly(ADP-ribose) activation, ubiquitylation, and double-strand DNA repair independent of ATM, MDC1, and RNF8. Mol. Cell. Biol. 33, 845-857
74. Crasta, K., Ganem, N. J., Dagher, R., Lantermann, A. B., Ivanova, E. V., Pan, Y., Nezi, L., Protopopov, A., Chowdhury, D., and Pellman, D. (2012)DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58
75. Pampalona, J., Soler, D., Genescà, A., and Tusell, L. (2010) Whole chromosome loss is promoted by telomere dysfunction in primary cells. Genes Chromosomes Cancer 49, 368-378