Of mice and (wo)men: Genotype-phenotype correlations in BRCA1

Human Molecular Genetics

Volumn 12, Issue REV. ISS. 2, 2003, Pages

  Hohenstein, Peter ^a,b,d   Fodde, Riccardo ^b,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^d WESTERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; BRCA1 PROTEIN; MUTANT PROTEIN;

BREAST CANCER; CARCINOGENESIS; DISEASE MODEL; FEMALE; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GENE THERAPY; GENE TRANSFER; GENETIC DATABASE; GENETIC RISK; GENOTYPE PHENOTYPE CORRELATION; HUMAN; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; RISK ASSESSMENT; WILD TYPE;

EID: 0141960152     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg258     Document Type: Review

References (69)

1. Perrin-Vidoz, L., Sinilnikova, O.M., Stoppa-Lyonnet, D., Lenoir, G.M. and Mazoyer, S. (2002) The nonsense-mediated mRNA decay pathway triggers degradation of most BRCA1 mRNAs bearing premature termination codons. Hum. Mol. Genet., 11, 2805-2814.
2. Tomlinson, I.P.M., Novelli, M.R. and Bodmer, W.F. (1996) The mutation rate and cancer. Proc. Natl Acad. Sci. USA, 93, 14800-14803.
3. Scully, R., Ganesan, S., Vlasakova, K., Chen, J., Socolovsky, M. and Livingston, D.M. (1999) Genetic analysis of BRCA1 function in a defined tumor cell line. Mol. Cell, 4, 1093-1099.
4. Gayther, S.A., Warren, W., Mazoyer, S., Russell, P.A., Harrington, P.A., Chiano, M., Seal, S., Hamoudi, R., Van Rensburg, E.J., Dunning, A.M. et al. (1995) Germline mutations of the BRCA 1 gene in breast and ovarian cancer families provide evidence for a genotype-phenotype correlation. Nat. Genet., 11, 428-433.
5. Holt, J.T., Thompson, M.E., Szabo, C., Robinson-Benion, C., Arteaga, C.L., King, M.C. and Jensen, R.A. (1996) Growth retardation and tumour inhibition by BRCA1. Nat. Genet., 12, 298-302.
6. Thompson, D. and Easton, D. (2002) Variation in BRCA1 cancer risks by mutation position. Cancer Epidemiol. Biomark. Prev., 11, 329-336.
7. Spirio, L., Olschwang, S., Groden, J., Robertson, M., Samowitz, W., Joslyn, G., Gelbert, L., Thliveris, A., Carlson, M., Otterud, B. et al. (1993) Alleles of the APC gene: an attenuated form of familial polyposis. Cell, 75, 951-957.
8. van der Luijt, R.B., Meera Khan, P., Vasen, H.F., Breukel, C., Tops, C.M., Scott, R.J. and Fodde, R. (1996) Germline mutations in the 3′ part of APC exon 15 do not result in truncated proteins and are associated with attenuated adenomatous polyposis coli. Hum. Genet., 98, 727-734.
9. Heppner Goss, K., Trzepacz, C., Tuohy, T.M. and Groden, J. (2002) Attenuated APC alleles; produce functional protein from internal translation initiation. Proc. Natl Acad. Sci. USA, 99, 8161-8166.
10. Sobol, A., Stoppalyonnet, D., Bressacdepaillerets, B., Peyrat, J.P., Kerangueven, F., Janin, N., Noguchi, T., Eisinger, F., Guinebretiere, J.M., Jacquemier, J. et al. (1996) Truncation at conserved terminal regions of BRCA1 protein is associated with highly proliferating hereditary breast cancers. Cancer Res., 56, 3216-3219.
11. Sobol, H., Stoppalyonnet, D., Bressacdepaillerets, B., Peyrat, J.P., Guinebretiere, J.M., Jacquemier, J., Eisinger, F. and Birnbaum, D. (1997) BRCA1 p53 relationship in hereditary breast cancer. Int. J. Oncol., 10, 349-353.
12. Ludwig, T., Chapman, D.L., Papaioannou, V.E. and Efstratiadis, A. (1997) Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev., 11, 1226-1241.
13. Hakem, R., de la Pompa, J.L., Sirard, C., Mo, R., Woo, M., Hakem, A., Wakeham, A., Potter, J., Reitmair, A., Billia, F. et al. (1996) The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell, 85, 1009-1023.
14. Liu, C.Y., Fleskennikitin, A., Li, S., Zeng, Y.Y. and Lee, W.H. (1996) Inactivation of the mouse Brca 1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes Dev., 10, 1835-1843.
15. Fodde, R., Edelmann, W., Yang, K., van Leeuwen, C., Carlson, C., Renault, B., Breukel, C., Alt, E., Lipkin, M., Khan, P.M. et al. (1994) A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc. Natl Acad. Sci. USA, 91, 8969-8973.
16. Smits, R., Kielman, M.F., Breukel, C., Zurcher, C., Neufeld, K., Jagmohan-Changur, S., Hofland, N., van Dijk, J., White, R., Edelmann, W. et al. (1999) Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Genes Dev., 13, 1309-1321.
17. Kielman, M.F., Rindapaa, M., Gaspar, C., Van Poppel, N., Breukel, C., Van Leeuwen, S., Taketo, M.M., Roberts, S., Smits, R. and Fodde, R. (2002) Apc modulates embryonic stem-cell differentiation by controlling the dosage of beta-catenin signaling. Nat. Genet., 11, 11.
18. Hohenstein, P., Kielman, M.F., Breukel, C., Bennett, L.M., Wiseman, R., Krimpenfort, P., Cornelisse, C., van Ommen, G.J., Devilee, P. and Fodde, R. (2001) A targeted mouse Brca1 mutation removing the last BRCT repeat results in apoptosis and embryonic lethality at the headfold stage. Oncogene, 20, 2544-2450.
19. Xu, X., Qiao, W., Linke, S.P., Cao, L., Li, W.M., Furth, P.A., Harris, C.C. and Deng, C.X. (2001) Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat. Genet., 28, 266-271.
20. Ludwig, T., Fisher, P., Ganesan, S. and Efstratiadis, A. (2001) Tumorigenesis in mice carrying a truncating Brca1 mutation. Genes Dev., 15, 1188-1193.
21. Shen, S.-X, Weaver, Z., Xu, X., Li, C., Weinstein, M., Chen, L., Guan, X.-Y., Ried, T. and Deng, C.-X. (1998) A targetted disruption of the murine Brca1 gene causes γ-irradiation hypersensitivity and genetic instability. Oncogene, 17, 3115-3124.
22. Gowen, L.C., Johnson, B.L., Latour, A.M., Sulik, K.K. and Koller, B.H. (1996) Brca1 deficiency results in early embryonic lethality characterized by neuroepithelial abnormalities. Nat. Genet., 12, 191-194.
23. Huber, L.J., Yang, T.W., Sarkisian, C.J., Master, S.R., Deng, C.X. and Chodosh, L.A. (2001) Impaired DNA damage response in cells expressing an exon 11-deleted murine Brca1 variant that localizes to nuclear foci. Mol. Cell. Biol., 21, 4005-4015.
24. Welcsh, P.L., Owens, K.N. and King, M.C. (2000) Insights into the functions of BRCA1 and BRCA2. Trends Genet., 16, 69-74.
25. Venkitaraman, A.R. (2002) Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell, 108, 171-182.
26. Deng, C.-X. and Wang, R.-H. (2003) Roles of BRCA1 in DNA damage repair: a link between development and cancer. Hum. Mol. Genet., 12, 113R-123.
27. 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.
28. Scully, R., Chen, J.J., Plug, A., Xiao, Y.H., Weaver, D., Feunteun, J., Ashley, T. and Livingston, D.M. (1997) Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell, 88, 265-275.
29. Zhong, Q., Chen, C.F., Li, S., Chen, Y.M., Wang, C.C., Xiao, J., Chen, P.L., Sharp, Z.D. and Lee, W.H. (1999) Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science, 285, 747-750.
30. Folias, A., Matkovic, M., Bruun, D., Reid, S., Hejna, J., Grompe, M., D'Andrea, A. and Moses, R. (2002) BRCA1 interacts directly with the Fanconi anemia protein FANCA. Hum. Mol. Genet., 11, 2591-2597.
31. Wang, Q., Zhang, H., Guerrette, S., Chen, J., Mazurek, A., Wilson, T., Slupianek, A., Skorski, T., Fishel, R. and Greene, M.I. (2001) Adenosine nucleotide modulates the physical interaction between hMSH2 and BRCA1. Oncogene, 20, 4640-4649.
32. Lee, J.S., Collins, K.M., Brown, A.L., Lee, C.H. and Chung, J.H. (2000) hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature, 404, 201-204.
33. Tibbetts, R.S., Cortez, D., Brumbaugh, K.M., Scully, R., Livingston, D., Elledge, S.J. and Abraham, R.T. (2000) Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev., 14, 2989-3002.
34. Cortez, D., Wang, Y., Qin, J. and Elledge, S.J. (1999) Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science, 286, 1162-1166.
35. Chapman, M. and Verma, I.M. (1996) Transcriptional activation by BRCA1. Nature, 382, 678-679.
36. Monteiro, A.N., August, A. and Hanafusa, H. (1996) Evidence for a transcriptional activation function of BRCA1 C terminal region. Proc. Natl Acad. Sci. USA, 93, 13595-13599.
37. Ouchi, T., Monteiro, A.N., August, A., Aaronson, S.A. and Hanafusa, H. (1998) BRCA1 regulates p53-dependent gene expression. Proc. Natl Acad. Sci. USA, 95, 2302-2306.
38. Zhang, H., Somasundaram, K., Peng, Y., Tian, H., Bi, D., Weber, B.L. and El-Deiry, W.S. (1998) BRCA1 physically associates with p53 and stimulates its transcriptional activity. Oncogene, 16, 1713-1721.
39. Ouchi, T., Lee, S.W., Ouchi, M., Aaronson, S.A. and Horvath, C.M. (2000) Collaboration of signal transducer and activator of transcription 1 (STAT1) and BRCA1 in differential regulation of IFN-gamma target genes. Proc. Natl Acad. Sci. USA, 97, 520$-5213.
40. Pao, G.M., Janknecht, R., Ruffner, H., Hunter, T. and Verma, I.M. (2000) CBP/p300 interact with and function as transcriptional coactivators of BRCA1. Proc. Natl Acad. Sci. USA, 97, 1020-1025.
41. Yu, X., Wu, L.J.C., Bowcock, A.M., Aronheim, A. and Baer, R. (1998) The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem., 273, 25388-25392.
42. Wong, A.K., Ormonde, P.A., Pero, R., Chen, Y., Lian, L., Salada, G., Berry, S., Lawrence, Q., Dayananth, P., Ha, P. et al. (1998) Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene, 17, 2279-2285.
43. Li, S., Chen, P.L., Subramanian, T., Chinnadurai, G., Tomlinson, G., Osborne, C.K., Sharp, Z.D. and Lee, W.H. (1999) Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 is disrupted upon DNA damage. J. Biol. Chem., 274, 11334-11338.
44. Scully, R., Anderson, S.F., Chao, D.M., Wei, W.J., Ye, L.Y., Young, R.A., Livingston, D.M. and Parvin, J.D. (1997) BRCA1 is a component of the RNA polymerase II holoenzyme. Proc. Natl Acad. Sci. USA, 94, 5605-5610.
45. Anderson, S.E., Schlegel, B.P., Nakajima, T., Wolpin, E.S. and Parvin, J.D. (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase a. Nat. Genet., 19, 254-256.
46. Fan, S., Wang, J.A., Yuan, R., Ma, Y., Meng, Q., Erdos, M.R., Pestell, R.G., Yuan, F., Auborn, K.J., Goldberg, I.D. et al. (1999) BRCA1 inhibition of estrogen receptor signaling in transfected cells. Science, 284, 1354-1356.
47. Fan, S., Ma, Y.X., Wang, C., Yuan, R.Q., Meng, Q., Wang, J.A., Erdos, M., Goldberg, I.D., Webb, P., Kushner, P.J. et al. (2001) Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene, 20, 77-87.
48. Kawai, H., Li, H., Chun, P., Avraham, S. and Avraham, H.K. (2002) Direct interaction between BRCA1 and the estrogen receptor regulates vascular endothelial growth factor (VEGF) transcription and secretion in breast cancer cells. Oncogene, 21, 7730-7739.
49. Fan, S., Ma, Y.X., Wang, C., Yuan, R.Q., Meng, Q., Wang, J.A., Erdos, M., Goldberg, I.D., Webb, P., Kushner, P.J. et al. (2002) p300 Modulates the BRCA1 inhibition of estrogen receptor activity. Cancer Res., 62, 141-151.
50. Lee, D., Kim, J.W., Seo, T., Hwang, S.G., Choi, E.J. and Choe, J. (2002) SWI/SNF complex interacts with tumor suppressor p53 and is necessary for the activation of p53-mediated transcription. J. Biol. Chem., 277, 22330-22337.
51. Otsuki, T., Furukawa, Y., Ikeda, K., Endo, H., Yamashita, T., Shinohara, A., Iwamatsu, A., Ozawa, K. and Liu, J.M. (2001) Fanconi anemia protein, FANCA, associates with BRG1, a component of the human SWI/SNF complex. Hum. Mol. Genet., 10, 2651-2660.
52. Garcia-Higuera, I., Taniguchi, T., Ganesan, S., Meyn, M.S., Timmers, C., Hejna, J., Grompe, M. and D'Andrea, A.D. (2001) Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell, 7, 249-262.
53. Lim, D.S. and Hasty, P. (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol., 16, 7133-7143.
54. Bender, C.F., Sikes, M.L., Sullivan, R., Huye, L.E., Le Beau, M.M., Roth, D.B., Mirzoeva, O.K., Oltz, E.M. and Petrini, J.H. (2002) Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev., 16, 2237-2251.
55. Heyer, B.S., MacAuley, A., Behrendtsen, O. and Werb, Z. (2000) Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev., 14, 2072-2084.
56. Hakem, R., de la Pompa, J.L., Elia, A., Potter, J. and Mak, T.W. (1997) Partial rescue of Brca1 (5-6) early embryonic lethality by p53 or p21 null mutation. Nat. Genet., 16, 298-302.
57. Moynahan, M.E., Chiu, J.W., Koller, B.H. and Jasin, M. (1999) Brca1 controls homology-directed DNA repair. Mol. Cell, 4, 511-518.
58. Crook, T., Crossland, S., Crompton, M.R., Osin, P. and Gusterson, B.A. (1997) p53 mutations in BRCA1-associated familial breast cancer. Lancet, 350, 638-639.
59. Tait, D.L., Obermiller, P.S. and Holt, J.T. (2000) Preclinical studies of a new generation retroviral vector for ovarian cancer BRCA1 gene therapy. Gynecol. Oncol., 79, 471-476.
60. Randrianarison, V., Marot, D., Foray, N., Cabannes, J., Meret, V., Connault, E., Vitrat, N., Opolon, P., Perricaudet, M. and Feunteun, J. (2001) BRCA1 carries tumor suppressor activity distinct from that of p53 and p21. Cancer Gene Ther, 8, 759-770.
61. Fan, S., Yuan, R., Ma, Y.X., Meng, Q., Goldberg, I.D. and Rosen, E.M. (2001) Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene, 20, 8215-8235.
62. Sylvain, V., Lafarge, S. and Bignon, Y.J. (2002) Dominant-negative activity of a Brca1 truncation mutant: effects on proliferation, tumorigenicity in vivo, and chemosensitivity in a mouse ovarian cancer cell line. Int. J. Oncol., 20, 845-853.
63. Brown, M.A., Nicolai, H., Howe, K., Katagiri, T., Lalani el, N., Simpson, K.J., Manning, N.W., Deans, A., Chen, P., Khanna, K.K. et al. (2002) Expression of a truncated Brca1 protein delays lactational. mammary development in transgenic mice. Transgenic Res., 11, 467-478.
64. Cornelis, R.S., Neuhausen, S.L., Johansson, O., Arason, A., Kelsell, D., Ponder, B.A., Tonin, P., Hamann, U., Lindblom, A., Lalle, P. et al. (1995) High allele loss rates at 17q12-q21 in breast and ovarian tumors from BRCA1-linked families. The Breast Cancer Linkage Consortium. Genes Chromosomes Cancer, 13, 203-210.
65. Albuquerque, C., Breukel, C., van der Luijt, R., Fidalgo, P., Lage, P., Slors, F.J., Leitao, C.N., Fodde, R. and Smits, R. (2002) The 'just-right' signaling model: APC somatic mutations are selected based on a specific level of activation of the beta-catenin signaling cascade. Hum. Mol. Genet., 11, 1549-1560.
66. Smits, R., Hofland, N., Edelmann, W., Geugien, M., Jagmohan-Changur, S., Albuquerque, C., Breukel, C., Kucherlapati, R., Kielman, M.F. and Fodde, R. (2000) Somatic Apc mutations are selected upon their capacity to inactivate the β-catenin downregulating activity. Genes Chromosomes Cancer, 29, 229-239.
67. Lamlum, H., Ilyas, M., Rowan, A., Clark, S., Johnson, V., Bell, J., Frayling, I., Efstathiou, J., Pack, K., Payne, S. et al. (1999) The type of somatic mutation at APC in familial adenomatous polyposis is determined by the site of the germline mutation: a new facet to Knudson's 'two-hit' hypothesis. Nat. Med., 5, 1071-1075.
68. Fodde, R. and Smits, R. (2002) Cancer biology. A matter of dosage. Science, 298, 761-763.
69. Yang. Y., Swaminathan, S., Martin, B.K. and Sharan, S.K. (2003) Aberrant splicing induced by missense mutations in BRCA1: clues from a humanized mouse model. Hum. Mol. Genet., 12, 2121-2131.