Cytoplasmic mislocalization of BRCA1 caused by cancer-associated mutations in the BRCT domain

Experimental Cell Research

Volumn 293, Issue 1, 2004, Pages 14-21

  Rodriguez, José Antonio ^a,b   Au, Wendy W Y ^a   Henderson, Beric R ^a  

^a WESTMEAD HOSPITAL   (Australia)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

BRCA1 mutations; BRCT domains; Breast cancer; DNA repair; Nuclear transport

Indexed keywords

BRAP PROTEIN, HUMAN; CARRIER PROTEIN;

ARTICLE; BREAST ADENOCARCINOMA; BREAST EPITHELIUM; BREAST TUMOR; CANCER CELL; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL FUNCTION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CHEMISTRY; COLON CANCER; CYTOPLASM; DNA DAMAGE; FEMALE; GENE MUTATION; GENETICS; HUMAN; HUMAN CELL; METABOLISM; ONCOGENE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE; STAINING; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; WILD TYPE;

EID: 0347320584     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.09.027     Document Type: Article

References (40)

1. Miki Y., Swensen J., Shattuck-Eidens D., Futreal P.A., Ahrshman K., Tavigian S., Liu Q., Cochran C., Bennett L.M., Ding W.et al. A strong candidate for the breast cancer susceptibility gene BRCA1. Science. 266:1994;66-71.
2. Couch F.J., Weber B.L. Mutations and polymorphisms in the familial early-onset breast cancer (BRCA1) gene. Breast Cancer Information Core. Hum. Mutat. 8:1996;8-18.
3. Chen Y., Lee W.H., Chew H.K. Emerging roles of BRCA1 in transcriptional regulation and DNA repair. J. Cell Physiol. 1:1999;385-392.
4. Scully R., Livingston D.M. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature. 408:2000;429-432.
5. Harkin D.P., Bean J.M., Miklos D., Song Y.-H., Truong V.B., Englert C., Christians F.C., Ellisen L.W., Maheswaran S., Oliner J.D., Haber D.A. Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1. Cell. 97:1999;575-586.
6. Baer R., Ludwig T. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Gen. Dev. 12:2002;86-91.
7. Brzovic P.S., Keeffe J.R., Nishikawa H., Miyamoto K., Fox D. III, Fukuda M., Ohta T., Klevit R. Binding and recognition in the assembly of an active BRCA1/BARD1 ubiquitin-ligase complex. Proc. Natl. Acad. Sci. U. S. A. 100:2003;5646-5651.
8. Chapman M.S., Verma I.M. Transcriptional activation by BRCA1. Nature. 382:1996;678-679.
9. Monteiro A.N.A., August A., Hanafusa H. Evidence for a transcriptional activation function of BRCA1 C-terminal region. Proc. Natl. Acad. Sci. U. S. A. 93:1996;13595-13599.
10. Scully R., Ganesan S., Vlaskova K., Chen J., Socolovsky M., Livingston D.M. Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell. 4:1999;1093-1099.
11. Zhong Q., Chen C.-F., Li S., Chen Y., Wang C.-C., Xiao J., Chen P.-L., Sharp Z.D., Lee W.-H. Association of BRCA1 with the hRAD50-hMRE11-p95 complex and the DNA damage response. Science. 285:1999;747-750.
12. Hayes F., Cayanan C., Barilla D., Monteiro A.N. Functional assay for BRCA1: mutagenesis of the COOH-terminal region reveals critical residues for transcription activation. Cancer Res. 60:2000;2408-2411.
13. Vallon-Christersson J., Cayanan C., Haraldsson K., Loman N., Bergthorsson J.T., Brondum-Nielsen K., Gerdes A.M., Moller P., Kristoffersson U., Olsson H., Borg A., Monteiro A.N. Functional analysis of BRCA1 C-terminal missense mutations identified in breast and ovarian cancer families. Hum. Mol. Genet. 10:2001;353-360.
14. Chen Y., Chen C.-F., Riley D.J., Allred D.C., Chen P.-L., Hoff D.V., Osborne C.K., Lee W.-H. Aberrant subcellular localization of BRCA1 in breast cancer. Science. 270:1995;789-791.
15. Scully R.S., Ganesan S., Brown M., Caprio J.A.D., Cannistra S.A., Feunteun J., Schnitt S., Livingston D.M. Location of BRCA1 in human breast and ovarian cancer cells. Science. 272:1996;123-125.
16. Wilson C.A., Ramos L., Villasenor M.R., Anders K.H., Press M.F., Clarke K., Karlan B., Chen J.-J., Scully R., Livingston D., Zuch R.H., Kanter M.H., Cohen S., Calzone F.J., Slamon D.J. Localization of human BRCA1 and its loss in high-grade, non-inherited breast carcinomas. Nat. Genet. 21:1999;236-240.
17. Jarvis E.M., Kirk J.A., Clarke C.L. Loss of nuclear BRCA1 expression in breast cancers is associated with a highly proliferative tumor phenotype. Cancer Genet. Cytogenet. 101:1998;109-115.
18. Taylor J., Lymboura M., Pace P.E., Hern R.P.A., Desai A.J., Shousha S., Coombes R.C., Ali S. An important role for BRCA1 in breast cancer progression is indicated by its loss in a large proportion of non-familial breast cancers. Int. J. Cancer. 79:1998;334-342.
19. Thomas J.E., Smith M., Rubinfeld B., Gutowski M., Beckman R.P., Polakis P. Subcellular localisation and analysis of apparent 180-kDa and 220-kDa proteins of the breast cancer susceptibility gene, BRCA1. J. Biol. Chem. 271:1996;28630-28635.
20. Fabbro M., Rodriguez J.A., Baer R., Henderson B.R. BARD1 induces BRCA1 intranuclear foci formation by increasing RING-dependent BRCA1 nuclear import and inhibiting BRCA1 nuclear export. J. Biol. Chem. 277:2002;21315-21324.
21. Chen C.-F., Li S., Chen Y., Chen P.-L., Sharp Z.D., Lee W.-H. The nuclear localization sequences of the BRCA1 protein interact with the importin-α subunit of the nuclear transport signal. J. Biol. Chem. 271:1996;32863-32868.
22. Thakur S., Zhang H.B., Peng Y., Le H., Carroll B., Ward T., Yao J., Farid L.M., Couch F.J., Wilson R.B., Weber B. Localization of BRCA1 and a splice variant identifies the nuclear localization signal. Mol. Cell. Biol. 17:1997;444-452.
23. Rodriguez J.A., Henderson B.R. Identification of a functional nuclear export signal in BRCA1. J. Biol. Chem. 275:2000;38589-38596.
24. Stenson P.D., Ball E.V., Mort M., Phillips A.D., Shiel J.A., Thomas N.S., Abeysinghe S., Krawczak M., Cooper D.N. Human Gene Mutation Database (HGMD): 2003 update. Hum. Mutat. 21:2003;577-581.
25. Friedman L.S., Ostermeyer E.A., Szabo C.I., Dowd P., Lynch E.D., Rowell S.E., King M.-C. Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat. Genet. 8:1994;399-404.
26. Shattuck-Eidens D., McClure M., Simard J., Labrie F., Narod S., Couch F., Hoskins K., Weber B., Castilla L., Erdos M., Brody L., Friedman L., Ostermeyer E., Szabo C., King M.-C., Jhanwar S., Offit K., Norton L., Gilewski T., Lubin M., Osborne M., Black D., Boyd M., Steel M., Ingles M.S., Haile R., Lindblom A., Olsson H., Borg A., Bishop D.T., Solomon E., Radice P., Spatti G., Gayther S., Ponder B., Warren W., Stratton M., Liu Q., Fujimura F., Lewis C., Skolnick M., Goldgar G., David E. A collaborative survey of 80 mutations in the BRCA1 breast and ovarian cancer susceptibility gene: implications for presymptomatic testing and screening. J. Am. Med. Assoc. 273:1995;535-541.
27. Gayther S.A., Harrington P., Russell P., Kharkevich G., Garkavtseva R.F., Ponder B.A. Rapid detection of regionally clustered germ-line BRCA1 mutations by multiplex heteroduplex analysis. UKCCCR Familial Ovarian Cancer Study Group. Am. J. Hum. Genet. 58:1996;451-456.
28. WAF-1/CIP1. Nature. 389:1997;187-190.
29. Zhang H., Somasundaram K., Peng Y., Tian H., Zhang H., Bi D., Weber B.L., El-Deiry W.S. BRCA1 physically associates with p53 and stimulates its transcriptional activity. Oncogene. 16:1998;1713-1721.
30. Fan S., Yuan R.-Q., Ma Y.X., Meng Q., Goldberg I.D., Rosen E.M. Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene. 20:2001;8215-8235.
31. Hu Y.F., Hao Z.L., Li R. Chromatin remodeling and activation of chromosomal DNA replication by an acidic transcriptional activation domain from BRCA1. Genes Dev. 13:1999;637-642.
32. Williams R.S., Green R., Glover J.N.M. Crystal structure of the BRCT repeat region from the breast cancer-associated protein BRCA1. Nat. Struct. Biol. 8:2001;838-842.
33. Fabbro M., Henderson B.R. Regulation of tumor suppressors by nuclear-cytoplasmic shuttling. Exp. Cell Res. 282:2003;59-69.
34. 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., Gazdar A.F. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58:1998;3237-3242.
35. Jin Y., Xu X.L., Yang M.-C.W., Wei F., Ayi T.-C., Bowcock A.M., Baer R. Cell cycle-dependent colocalisation of BARD1 and BRCA1 proteins in discrete nuclear domains. Proc. Natl. Acad. Sci. U. S. A. 94:1997;12075-12080.
36. Scully R.S., Chen J., Plug A., Xiao Y., Weaver D., Feunteun J., Ashley T., Livingston D.M. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 88:1997;265-275.
37. Scully R., Chen J., Ochs R.L., Keegan K., Hoekstra M., Feunteun J., Livingston D.M. Dynamic changes of BRCA1 subcellular location and phosphorylation state are initiated by DNA damage. Cell. 90:1997;425-435.
38. Wu X., Petrini J.H.J., Heine W.F., Weaver D.T., Livingston D.M., Chen J. Independence of R/M/N focus formation and the presence of intact BRCA1. Science. 289:2000;11a.
39. Kashima K., Oite T., Aoki Y., Takakuwa K., Aida H., Nagata H., Sekine M., Wu H.J., Hirai Y., Wada Y., Yamamoto K., Hasegawa K., Sonoda T., Maruo T., Nagata I., Ohno M., Suzuki M., Kobayashi I., Kuzuya K., Takahashi T., Torii Y., Tanaka K. Screening of BRCA1 mutation using immunohistochemical staining with C-terminal and N-terminal antibodies in familial ovarian cancers. Jpn. J. Cancer Res. 91:2000;399-409.
40. Hsu L.-C., White R.L. BRCA1 is associated with the centrosome during mitosis. Proc. Natl. Acad. Sci. U. S. A. 95:1998;12983-12988.