Loss of BRCA1 impairs centromeric cohesion and triggers chromosomal instability

FASEB Journal

Volumn 28, Issue 12, 2014, Pages 5250-5261

  Di Paolo, Aurélie ^a,b   Racca, Carine ^a,b   Calsou, Patrick ^a,b,c   Larminat, Florence ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c Equipe Labellisée Ligue Nationale Contre le Cancer 2018   (France)

Author keywords

Aneuploidy; Chromosome spindle attachment; Mitosis

Indexed keywords

AURORA B KINASE; BRCA1 PROTEIN; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3B; CHROMATIN; DNA (CYTOSINE 5) METHYLTRANSFERASE; SMALL INTERFERING RNA;

ANEUPLOIDY; ARTICLE; CELL ADHESION; CENTROMERE; CHROMATIN CONDENSATION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL INSTABILITY; DNA METHYLATION; HCT116 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; MCF 7 CELL LINE; MITOSIS; PROTEIN DEPLETION; SISTER CHROMATID; CHROMATIN; FLUORESCENCE MICROSCOPY; METABOLISM; NUCLEOTIDE SEQUENCE; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE;

BASE SEQUENCE; CELL LINE, TUMOR; CENTROMERE; CHROMATIN; CHROMOSOMAL INSTABILITY; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; GENES, BRCA1; HUMANS; MICROSCOPY, FLUORESCENCE; RNA, SMALL INTERFERING;

EID: 84919798077     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-250266     Document Type: Article

References (50)

1. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P. A., Harshman, K., Tavtigian, S., Liu, Q., Cochran, C., Bennett, L. M., Ding, W., Bell, R., Rosenthal, J., Hussey, C., Tran, T., McClure, M., Frye, C., Hattier, T., Phelps, R., Haugen-Strano, A., Katcher, H., Yakumo, K., Gholami, Z., Shaffer, D., Stone, S., Bayer, S., Wray, C., Bogden, R., Dayananth, P., Ward, J., Tonin, P., Narod, S., Bristow, P. K., Norris, F. L., Helvering, L., Morrison, P., Rosteck, P., Lai, M., Barrett, J. C., Lewis, C., Neuhausen, S., Cannon-Albright, L., Goldgar, D., Wiseman, R., Kamb, A., Skolnick, M. H. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66-71
2. Huen, M. S., Sy, S. M., and Chen, J. (2010) BRCA1 and its toolbox for the maintenance of genome integrity. Nat. Rev. Mol. Cell Biol. 11, 138-148
3. Xu, X., Weaver, Z., Linke, S. P., Li, C., Gotay, J., Wang, X. W., Harris, C. C., Ried, T., and Deng, C. X. (1999) Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell. 3, 389-395
4. Tomlinson, G. E., Chen, T. T., Stastny, V. A., Virmani, A. K., Spillman, M. A., Tonk, V., Blum, J. L., Schneider, N. R., Wistuba, I. I., Shay, J. W., Minna, J. D., and Gazdar, A. F. (1998) Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58, 3237-3242
5. Hsu, L. C., and White, R. L. (1998) BRCA1 is associated with the centrosome during mitosis. Proc. Natl. Acad. Sci. U. S. A. 95, 12983-12988
6. Sankaran, S., Starita, L. M., Groen, A. C., Ko, M. J., and Parvin, J. D. (2005) Centrosomal microtubule nucleation activity is inhibited by BRCA1-dependent ubiquitination. Mol. Cell. Biol. 25, 8656-8668
7. Starita, L. M., Machida, Y., Sankaran, S., Elias, J. E., Griffin, K., Schlegel, B. P., Gygi, S. P., and Parvin, J. D. (2004) BRCA1-dependent ubiquitination of gamma-tubulin regulates centrosome number. Mol. Cell. Biol. 24, 8457-8466
8. Chabalier, C., Lamare, C., Racca, C., Privat, M., Valette, A., and Larminat, F. (2006) BRCA1 downregulation leads to premature inactivation of spindle checkpoint and confers paclitaxel resistance. Cell Cycle 5, 1001-1007
9. Wang, R. H., Yu, H., and Deng, C. X. (2004) A requirement for breast-cancer-associated gene 1 (BRCA1) in the spindle checkpoint. Proc. Natl. Acad. Sci. U. S. A. 101, 17108-17113
10. Bae, I., Rih, J. K., Kim, H. J., Kang, H. J., Haddad, B., Kirilyuk, A., Fan, S., Avantaggiati, M. L., and Rosen, E. M. (2005) BRCA1 regulates gene expression for orderly mitotic progression. Cell Cycle 4, 1641-1666
11. Cleveland, D. W., Mao, Y., and Sullivan, K. F. (2003) Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell 112, 407-421
12. Joukov, V., Groen, A. C., Prokhorova, T., Gerson, R., White, E., Rodriguez, A., Walter, J. C., and Livingston, D. M. (2006) The BRCA1/BARD1 heterodimer modulates ran-dependent mitotic spindle assembly. Cell 127, 539-552
13. Jin, S., Gao, H., Mazzacurati, L., Wang, Y., Fan, W., Chen, Q., Yu, W., Wang, M., Zhu, X., Zhang, C., and Zhan, Q. (2009) BRCA1 interaction of centrosomal protein Nlp is required for successful mitotic progression. J. Biol. Chem. 284, 22970-22977
14. Stolz, A., Ertych, N., Kienitz, A., Vogel, C., Schneider, V., Fritz, B., Jacob, R., Dittmar, G., Weichert, W., Petersen, I., and Bastians, H. (2010) The CHK2-BRCA1 tumour suppressor pathway ensures chromosomal stability in human somatic cells. Nat. Cell Biol. 12, 492-499
15. 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
16. Verdaasdonk, J. S., and Bloom, K. (2011) Centromeres: unique chromatin structures that drive chromosome segregation. Nat. Rev. Mol. Cell Biol. 12, 320-332
17. Amor, D. J., Kalitsis, P., Sumer, H., and Choo, K. H. (2004) Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol. 14, 359-368
18. Pageau, G. J., and Lawrence, J. B. (2006) BRCA1 foci in normal S-phase nuclei are linked to interphase centromeres and replication of pericentric heterochromatin. J. Cell Biol. 175, 693-701
19. Zhu, Q., Pao, G. M., Huynh, A. M., Suh, H., Tonnu, N., Nederlof, P. M., Gage, F. H., and Verma, I. M. (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 477, 179-184
20. Ganesan, S., Silver, D. P., Greenberg, R. A., Avni, D., Drapkin, R., Miron, A., Mok, S. C., Randrianarison, V., Brodie, S., Salstrom, J., Rasmussen, T. P., Klimke, A., Marrese, C., Marahrens, Y., Deng, C. X., Feunteun, J., and Livingston, D. M. (2002) BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 111, 393-405
21. Chabalier-Taste, C., Racca, C., Dozier, C., and Larminat, F. (2008) BRCA1 is regulated by Chk2 in response to spindle damage. Biochim. Biophys. Acta 1783, 2223-2233
22. Iacovoni, J. S., Caron, P., Lassadi, I., Nicolas, E., Massip, L., Trouche, D., and Legube, G. (2010) High-resolution profiling of gammaH2AX around DNA double-strand breaks in the mammalian genome. EMBO J. 29, 1446-1457
23. Kallenberg, C. G. (1990) Anti-centromere antibodies (ACA). Clin. Rheumatol. 9, 136-139
24. Gopalakrishnan, S., Sullivan, B. A., Trazzi, S., Della Valle, G., and Robertson, K. D. (2009) DNMT3B interacts with constitutive centromere protein CENP-C to modulate DNA methylation and the histone code at centromeric regions. Hum. Mol. Genet. 18, 3178-3193
25. Tu, Z., Aird, K. M., Bitler, B. G., Nicodemus, J. P., Beeharry, N., Xia, B., Yen, T. J., and Zhang, R. (2011) Oncogenic RAS regulates BRIP1 expression to induce dissociation of BRCA1 from chromatin, inhibit DNA repair, and promote senescence. Dev. Cell. 21, 1077-1091
26. Ruchaud, S., Carmena, M., and Earnshaw, W. C. (2007) Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8, 798-812
27. Yasui, Y., Urano, T., Kawajiri, A., Nagata, K., Tatsuka, M., Saya, H., Furukawa, K., Takahashi, T., Izawa, I., and Inagaki, M. (2004) Autophosphorylation of a newly identified site of Aurora-B is indispensable for cytokinesis. J. Biol. Chem. 279, 12997-13003
28. Giet, R., and Glover, D. M. (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669-682
29. Zeitlin, S. G., Shelby, R. D., and Sullivan, K. F. (2001) CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J. Cell Biol. 155, 1147-1157
30. Kapoor, T. M., Mayer, T. U., Coughlin, M. L., and Mitchison, T. J. (2000) Probing spindle assembly mechanisms with monastrol, a small molecule inhibitor of the mitotic kinesin, Eg5. J. Cell Biol. 150, 975-988
31. Yamagishi, Y., Honda, T., Tanno, Y., and Watanabe, Y. (2010) Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330, 239-243
32. Kawashima, S. A., Yamagishi, Y., Honda, T., Ishiguro, K., and Watanabe, Y. (2010) Phosphorylation of H2A by Bub1 prevents chromosomal instability through localizing shugoshin. Science 327, 172-177
33. Monier, K., Mouradian, S., and Sullivan, K. F. (2007) DNA methylation promotes Aurora-B-driven phosphorylation of histone H3 in chromosomal subdomains. J. Cell Sci. 120, 101-114
34. Filipponi, D., Muller, J., Emelyanov, A., and Bulavin, D. V. (2013) Wip1 controls global heterochromatin silencing via ATM/BRCA1-dependent DNA methylation. Cancer Cell 24, 528-541
35. Hayakawa, T., Haraguchi, T., Masumoto, H., and Hiraoka, Y. (2003) Cell cycle behavior of human HP1 subtypes: distinct molecular domains of HP1 are required for their centromeric localization during interphase and metaphase. J. Cell Sci. 116, 3327-3338
36. Salimian, K. J., Ballister, E. R., Smoak, E. M., Wood, S., Panchenko, T., Lampson, M. A., and Black, B. E. (2011) Feedback control in sensing chromosome biorientation by the Aurora B kinase. Curr. Biol. 21, 1158-1165
37. Lampson, M. A., Renduchitala, K., Khodjakov, A., and Kapoor, T. M. (2004) Correcting improper chromosome-spindle attachments during cell division. Nat. Cell Biol. 6, 232-237
38. Cimini, D., Howell, B., Maddox, P., Khodjakov, A., Degrassi, F., and Salmon, E. D. (2001) Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. J. Cell Biol. 153, 517-527
39. Knowlton, A. L., Lan, W., and Stukenberg, P. T. (2006) Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Curr. Biol. 16, 1705-1710
40. Ditchfield, C., Johnson, V. L., Tighe, A., Ellston, R., Haworth, C., Johnson, T., Mortlock, A., Keen, N., and Taylor, S. S. (2003) Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161, 267-280
41. Sgura, A., Antoccia, A., Ramirez, M. J., Marcos, R., Tanzarella, C., and Degrassi, F. (1997) Micronuclei, centromere-positive micronuclei and chromosome nondisjunction in cytokinesis blocked human lymphocytes following mitomycin C or vincristine treatment. Mutat. Res. 392, 97-107
42. Bochar, D. A., Wang, L., Beniya, H., Kinev, A., Xue, Y., Lane, W. S., Wang, W., Kashanchi, F., and Shiekhattar, R. (2000) BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 102, 257-265
43. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M., and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316, 1198-1202
44. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil, S., Doyle, M., Sibilia, M., and Jenuwein, T. (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337
45. Bakhoum, S. F., Genovese, G., and Compton, D. A. (2009) Deviant kinetochore microtubule dynamics underlie chromosomal instability. Curr. Biol. 19, 1937-1942
46. Slee, R. B., Steiner, C. M., Herbert, B. S., Vance, G. H., Hickey, R. J., Schwarz, T., Christan, S., Radovich, M., Schneider, B. P., Schindelhauer, D., and Grimes, B. R. (2011) Cancer-associated alteration of pericentromeric heterochromatin may contribute to chromosome instability. Oncogene 31, 3244-3253
47. Crasta, K., Ganem, N. J., Dagher, R., Lantermann, A. B., Ivanova, E. V., Pan, Y., Nezi, L., Protopopov, A., Chowdhury, D., and Pellman, D. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58
48. Marcus, J. N., Watson, P., Page, D. L., Narod, S. A., Lenoir, G. M., Tonin, P., Linder-Stephenson, L., Salerno, G., Conway, T. A., and Lynch, H. T. (1996) Hereditary breast cancer: pathobiology, prognosis, and BRCA1 and BRCA2 gene linkage. Cancer 77, 697-709
49. Miyoshi, Y., Iwao, K., Ikeda, N., Egawa, C., and Noguchi, S. (2002) Acceleration of chromosomal instability of BRCA1-associated hereditary breast cancers by p53 abnormality. Breast J. 8, 77-80
50. Tirkkonen, M., Johannsson, O., Agnarsson, B. A., Olsson, H., Ingvarsson, S., Karhu, R., Tanner, M., Isola, J., Barkardottir, R. B., Borg, A., and Kallioniemi, O. P. (1997) Distinct somatic genetic changes associated with tumor progression in carriers of BRCA1 and BRCA2 germ-line mutations. Cancer Res. 57, 1222-1227