Characterization of BRCA1 protein targeting, dynamics, and function at the centrosome: A role for the nuclear export signal, CRM1, and aurora a kinase

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7701-7716

  Brodie, Kirsty M ^a   Henderson, Beric R ^a  

^a WESTMEAD HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER CELLS; CENTROSOME AMPLIFICATION; DNA DAMAGE RESPONSE; DNA DAMAGES; DNA REPAIR; HETERODIMERS; MICROTUBULE NUCLEATION; MITOTIC SPINDLE; NUCLEAR EXPORT; NUCLEAR EXPORT SIGNALS; PROTEIN TARGETING;

BIOMOLECULES; PHOSPHORYLATION; PHOTOBLEACHING;

DNA;

AURORA A KINASE; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; EXPORTIN 1; GAMMA TUBULIN; HETERODIMER; PHOSPHOPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CENTROSOME; CONTROLLED STUDY; G2 PHASE CELL CYCLE CHECKPOINT; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MOLECULAR DYNAMICS; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL NUCLEUS; CENTROSOME; DNA DAMAGE; FEMALE; HUMANS; KARYOPHERINS; MUTATION; NUCLEAR EXPORT SIGNALS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TUBULIN; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84857735639     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.327296     Document Type: Article

References (68)

1. Narod, S. A., and Foulkes, W. D. (2004) BRCA1 and BRCA2: 1994 and beyond. Nat. Rev. Cancer 4, 665-676 (Pubitemid 39215065)
2. Antoniou, A., Pharoah, P. D., Narod, S., Risch, H. A., Eyfjord, J. E., Hopper, J. L., Loman, N., Olsson, H., Johannsson, O., Borg, A., Pasini, B., Radice, P., Manoukian, S., Eccles, D. M., Tang, N., Olah, E., Anton-Culver, H., Warner, E., Lubinski, J., Gronwald, J., Gorski, B., Tulinius, H., Thorlacius, S., Eerola, H., Nevanlinna, H., Syrjäkoski, K., Kallioniemi, O. P., Thompson, D., Evans, C., Peto, J., Lalloo, F., Evans, D. G., and Easton, D. F. (2003) Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history. A combined analysis of 22 studies. Am. J. Hum. Genet. 72, 1117-1130 (Pubitemid 36530000)
3. Easton, D. F., Ford, D., and Bishop, D. T. (1995) Breast and ovarian cancer incidence in BRCA1 mutation carriers. Breast Cancer Linkage Consortium. Am. J. Hum. Genet. 56, 265-271
4. Levy-Lahad, E., and Friedman, E. (2007) Cancer risks among BRCA1 and BRCA2 mutation carriers. Br. J. Cancer 96, 11-15 (Pubitemid 46094632)
5. Bekker-Jensen, S., and Mailand, N. (2010) Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair 9, 1219-1228
6. Xia, Y., Pao, G. M., Chen, H. W., Verma, I. M., and Hunter, T. (2003) Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J. Biol. Chem. 278, 5255-5263 (Pubitemid 36801039)
7. Thomson, T. M., and Guerra-Rebollo, M. (2010) Ubiquitin and SUMO signaling in DNA repair. Biochem. Soc. Trans. 38, 116-131
8. Parvin, J. D. (2009) The BRCA1-dependent ubiquitin ligase,γ- tubulin, and centrosomes. Environ. Mol. Mutagen. 50, 649-653
9. Yu, X., Chini, C. C., He, M., Mer, G., and Chen, J. (2003) The BRCT domain is a phospho-protein binding domain. Science 302, 639-642 (Pubitemid 37310919)
10. Krum, S. A., Miranda, G. A., Lin, C., and Lane, T. F. (2003) BRCA1 associates with processive RNA polymerase II. J. Biol. Chem. 278, 52012-52020 (Pubitemid 38035786)
11. Manke, I. A., Lowery, D. M., Nguyen, A., and Yaffe, M. B. (2003) BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302, 636-639 (Pubitemid 37310918)
12. Shakya, R., Reid, L. J., Reczek, C. R., Cole, F., Egli, D., Lin, C. S., deRooij, D. G., Hirsch, S., Ravi, K., Hicks, J. B., Szabolcs, M., Jasin, M., Baer, R., and Ludwig, T. (2011) BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 334, 525-528
13. Moritz, M., Braunfeld, M. B., Sedat, J. W., Alberts, B., and Agard, D. A. (1995) Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 378, 638-640 (Pubitemid 3005786)
14. 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 (Pubitemid 41369184)
15. Sankaran, S., Starita, L. M., Simons, A. M., and Parvin, J. D. (2006) Identification of domains of BRCA1 critical for the ubiquitin-dependent inhibition of centrosome function. Cancer Res. 66, 4100-4107
16. 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 γ-tubulin regulates centrosome number. Mol. Cell. Biol. 24, 8457-8466 (Pubitemid 39245068)
17. Schlegel, B. P., Starita, L. M., and Parvin, J. D. (2003) Overexpression of a protein fragment of RNA helicase A causes inhibition of endogenous BRCA1 function and defects in ploidy and cytokinesis in mammary epithelial cells. Oncogene 22, 983-991 (Pubitemid 36313142)
18. Deng, C. X. (2001) Tumorigenesis as a consequence of genetic instability in Brca1 mutant mice. Mutat. Res. 477, 183-189
19. 2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell 3, 389-395
20. Sankaran, S., Crone, D. E., Palazzo, R. E., and Parvin, J. D. (2007) BRCA1 regulates γ-tubulin binding to centrosomes. Cancer Biol. Ther. 6, 1853-1857 (Pubitemid 351590396)
21. Fukasawa, K. (2005) Centrosome amplification, chromosome instability, and cancer development. Cancer Lett. 230, 6-19
22. Miyoshi, Y., Iwao, K., Egawa, C., and Noguchi, S. (2001) Association of centrosomal kinase STK15/BTAK mRNA expression with chromosomal instability in human breast cancers. Int. J. Cancer 92, 370-373 (Pubitemid 32249713)
23. Zhou, H., Kuang, J., Zhong, L., Kuo, W. L., Gray, J. W., Sahin, A., Brinkley, B. R., and Sen, S. (1998) Tumor amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy, and transformation. Nat. Genet. 20, 189-193 (Pubitemid 28455454)
24. Kimura, M., Kotani, S., Hattori, T., Sumi, N., Yoshioka, T., Todokoro, K., and Okano, Y. (1997) Cell cycle-dependent expression and spindle pole localization of a novel human protein kinase, Aik, related to Aurora of Drosophila and yeast Ipl1. J. Biol. Chem. 272, 13766-13771 (Pubitemid 27224814)
25. Gopalan, G., Chan, C. S., and Donovan, P. J. (1997) A novel mammalian, mitotic spindle-associated kinase is related to yeast and fly chromosome segregation regulators. J. Cell Biol. 138, 643-656 (Pubitemid 27349844)
26. 2 to M transition. J. Biol. Chem. 279, 19643-19648
27. Rodríguez, J. A., and Henderson, B. R. (2000) Identification of a functional nuclear export sequence in BRCA1. J. Biol. Chem. 275, 38589-38596 (Pubitemid 32009187)
28. Rodriguez, J. A., Schüchner, S., Au, W. W., Fabbro, M., and Henderson, B. R. (2004) Nuclear-cytoplasmic shuttling of BARD1 contributes to its proapoptotic activity and is regulated by dimerization with BRCA1. Oncogene 23, 1809-1820 (Pubitemid 38445406)
29. Budhu, A. S., and Wang, X. W. (2005) Loading and unloading. Orchestrating centrosome duplication and spindle assembly by Ran/Crm1. Cell Cycle 4, 1510-1514
30. Forgues, M., Difilippantonio, M. J., Linke, S. P., Ried, T., Nagashima, K., Feden, J., Valerie, K., Fukasawa, K., and Wang, X. W. (2003) Involvement of Crm1 in hepatitis B virus X protein-induced aberrant centriole replication and abnormal mitotic spindles. Mol. Cell. Biol. 23, 5282-5292 (Pubitemid 36950883)
31. Liu, Q., Jiang, Q., and Zhang, C. (2009) A fraction of Crm1 locates at centrosomes by its CRIME domain and regulates the centrosomal localization of pericentrin. Biochem. Biophys. Res. Commun. 384, 383-388
32. Keryer, G., Di Fiore, B., Celati, C., Lechtreck, K. F., Mogensen, M., Delouvee, A., Lavia, P., Bornens, M., and Tassin, A. M. (2003) Part of Ran is associated with AKAP450 at the centrosome. Involvement in microtubule- organizing activity. Mol. Biol. Cell 14, 4260-4271 (Pubitemid 37186326)
33. Wang, W., Budhu, A., Forgues, M., and Wang, X. W. (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat. Cell Biol. 7, 823-830 (Pubitemid 41079055)
34. Shinmura, K., Tarapore, P., Tokuyama, Y., George, K. R., and Fukasawa, K. (2005) Characterization of centrosomal association of nucleophosmin/ B23 linked to Crm1 activity. FEBS Lett. 579, 6621-6634 (Pubitemid 41682450)
35. Han, X., Saito, H., Miki, Y., and Nakanishi, A. (2008) A CRM1-mediated nuclear export signal governs cytoplasmic localization of BRCA2 and is essential for centrosomal localization of BRCA2. Oncogene 27, 2969-2977 (Pubitemid 351668015)
36. Nakanishi, A., Han, X., Saito, H., Taguchi, K., Ohta, Y., Imajoh-Ohmi, S., and Miki, Y. (2007) Interference with BRCA2, which localizes to the centrosome during S and early M phase, leads to abnormal nuclear division. Biochem. Biophys. Res. Commun. 355, 34-40 (Pubitemid 46273362)
37. Brodie, K. M., Mok, M. T., and Henderson, B. R. (2012) Characterization of BARD1 targeting and dynamics at the centrosome. The role of CRM1, BRCA1, and the Q564H mutation. Cell. Signal. 24, 451-459
38. Brodie, K. M., and Henderson, B. R. (2010) Differential modulation of BRCA1 and BARD1 nuclear localization and foci assembly by DNA damage. Cell. Signal. 22, 291-302
39. Fabbro, M., Rodriguez, J. A., Baer, R., and Henderson, B. R. (2002) BARD1 induces BRCA1 intranuclear foci formation by increasing RING-dependent BRCA1 nuclear import and inhibiting BRCA1 nuclear export. J. Biol. Chem. 277, 21315-21324 (Pubitemid 34952270)
40. Au, W. W., and Henderson, B. R. (2005) The BRCA1 RING and BRCT domains cooperate in targeting BRCA1 to ionizing radiation-induced nuclear foci. J. Biol. Chem. 280, 6993-7001 (Pubitemid 40341255)
41. Schüchner, S., Tembe, V., Rodriguez, J. A., and Henderson, B. R. (2005) Nuclear targeting and cell cycle regulatory function of human BARD1. J. Biol. Chem. 280, 8855-8861 (Pubitemid 40409575)
42. Rodriguez, J. A., Au, W. W., and Henderson, B. R. (2004) Cytoplasmic mislocalization of BRCA1 caused by cancer-associated mutations in the BRCT domain. Exp. Cell Res. 293, 14-21 (Pubitemid 38064410)
43. Au, W. W., and Henderson, B. R. (2007) Identification of sequences that target BRCA1 to nuclear foci following alkylative DNA damage. Cell. Signal. 19, 1879-1892 (Pubitemid 47082540)
44. Gillingham, A. K., and Munro, S. (2000) The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep. 1, 524-529
45. Williams, R. S., Green, R., and Glover, J. N. (2001) Crystal structure of the BRCT repeat region from the breast cancer-associated protein BRCA1. Nat. Struct. Biol. 8, 838-842 (Pubitemid 32923600)
46. Matsumoto, Y., and Maller, J. L. (2004) A centrosomal localization signal in cyclin E required for Cdk2-independent S phase entry. Science 306, 885-888 (Pubitemid 39447000)
47. Pascreau, G., Eckerdt, F., Churchill, M. E., and Maller, J. L. (2010) Discovery of a distinct domain in cyclin A sufficient for centrosomal localization independently of Cdk binding. Proc. Natl. Acad. Sci. U.S.A. 107, 2932-2937
48. Hsu, L. C., Doan, T. P., and White, R. L. (2001) Identification of a γ-tubulin- binding domain in BRCA1. Cancer Res. 61, 7713-7718 (Pubitemid 33049353)
49. Sankaran, S., Crone, D. E., Palazzo, R. E., and Parvin, J. D. (2007) Aurora A kinase regulates breast cancer-associated gene 1 inhibition of centrosome- dependent microtubule nucleation. Cancer Res. 67, 11186-11194 (Pubitemid 350248543)
50. Saladino, C., Bourke, E., Conroy, P. C., and Morrison, C. G. (2009) Centriole separation in DNA damage-induced centrosome amplification. Environ. Mol. Mutagen. 50, 725-732
51. Maxwell, C. A., Keats, J. J., Crainie, M., Sun, X., Yen, T., Shibuya, E., Hendzel, M., Chan, G., and Pilarski, L. M. (2003) RHAMM is a centrosomal protein that interacts with dynein and maintains spindle pole stability. Mol. Biol. Cell 14, 2262-2276 (Pubitemid 36724319)
52. Kudo, N., Matsumori, N., Taoka, H., Fujiwara, D., Schreiner, E. P., Wolff, B., Yoshida, M., and Horinouchi, S. (1999) Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. U.S.A. 96, 9112-9117 (Pubitemid 29374716)
53. Baer, R., and Ludwig, T. (2002) The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12, 86-91 (Pubitemid 34094995)
54. Henderson, B. R. (2005) Regulation of BRCA1, BRCA2, and BARD1 intracellular trafficking. BioEssays 27, 884-893
55. Sato, K., Hayami, R., Wu, W., Nishikawa, T., Nishikawa, H., Okuda, Y., Ogata, H., Fukuda, M., and Ohta, T. (2004) Nucleophosmin/B23 is a candidate substrate for the BRCA1-BARD1 ubiquitin ligase. J. Biol. Chem. 279, 30919-30922 (Pubitemid 39037748)
56. Pujana, M. A., Han, J. D., Starita, L. M., Stevens, K. N., Tewari, M., Ahn, J. S., Rennert, G., Moreno, V., Kirchhoff, T., Gold, B., Assmann, V., Elshamy, W. M., Rual, J. F., Levine, D., Rozek, L. S., Gelman, R. S., Gunsalus, K. C., Greenberg, R. A., Sobhian, B., Bertin, N., Venkatesan, K., Ayivi- Guedehoussou, N., Solé, X., Hernández, P., Lázaro, C., Nathanson, K. L., Weber, B. L., Cusick, M. E., Hill, D. E., Offit, K., Livingston, D. M., Gruber, S. B., Parvin, J. D., and Vidal, M. (2007) Network modeling links breast cancer susceptibility and centrosome dysfunction. Nat. Genet. 39, 1338-1349 (Pubitemid 350035000)
57. Shimomura, A., Miyoshi, Y., Taguchi, T., Tamaki, Y., and Noguchi, S. (2009) Association of loss of BRCA1 expression with centrosome aberration in human breast cancer. J Cancer Res. Clin Oncol. 135, 421-430
58. 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
59. Lotti, L. V., Ottini, L., D'Amico, C., Gradini, R., Cama, A., Belleudi, F., Frati, L., Torrisi, M. R., and Mariani-Costantini, R. (2002) Subcellular localization of the BRCA1 gene product in mitotic cells. Genes Chromosomes Cancer 35, 193-203
60. Hashizume, R., Fukuda, M., Maeda, I., Nishikawa, H., Oyake, D., Yabuki, Y., Ogata, H., and Ohta, T. (2001) The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276, 14537-14540
61. Coene, E. D., Hollinshead, M. S., Waeytens, A. A., Schelfhout, V. R., Eechaute, W. P., Shaw, M. K., Van Oostveldt, P. M., and Vaux, D. J. (2005) Phosphorylated BRCA1 is predominantly located in the nucleus and mitochondria. Mol. Biol. Cell 16, 997-1010 (Pubitemid 40165588)
62. Thompson, H. M., Cao, H., Chen, J., Euteneuer, U., and McNiven, M. A. (2004) Dynamin 2 binds γ-tubulin and participates in centrosome cohesion. Nat. Cell Biol. 6, 335-342 (Pubitemid 38584823)
63. Stenoien, D. L., Sen, S., Mancini, M. A., and Brinkley, B. R. (2003) Dynamic association of a tumor amplified kinase, Aurora-A, with the centrosome and mitotic spindle. Cell Motil. Cytoskeleton 55, 134-146 (Pubitemid 36627264)
64. Hames, R. S., Crookes, R. E., Straatman, K. R., Merdes, A., Hayes, M. J., Faragher, A. J., and Fry, A. M. (2005) Dynamic recruitment of Nek2 kinase to the centrosome involves microtubules, PCM-1, and localized proteasomal degradation. Mol. Biol. Cell 16, 1711-1724 (Pubitemid 40471942)
65. Kallio, M. J., Beardmore, V. A., Weinstein, J., and Gorbsky, G. J. (2002) Rapid microtubule-independent dynamics of Cdc20 at kinetochores and centrosomes in mammalian cells. J. Cell Biol. 158, 841-847 (Pubitemid 35001075)
66. Khodjakov, A., and Rieder, C. L. (1999) The sudden recruitment of γ-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle do not require microtubules. J. Cell Biol. 146, 585-596 (Pubitemid 29388133)
67. Ouchi, T. (2006) BRCA1 phosphorylation. Biological consequences. Cancer Biol. Ther. 5, 470-475
68. Roghi, C., Giet, R., Uzbekov, R., Morin, N., Chartrain, I., Le Guellec, R., Couturier, A., Dorée, M., Philippe, M., and Prigent, C. (1998) The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules, and is involved in bipolar mitotic spindle assembly. J. Cell Sci. 111, 557-572 (Pubitemid 28142361)