Solution structure, backbone dynamics, and association behavior of the C-terminal BRCT domain from the breast cancer-associated protein BRCA1

Biochemistry

Volumn 43, Issue 51, 2004, Pages 15983-15995

  Gaiser, Olaf J ^a,b   Ball, Linda J ^b,d   Schmieder, Peter ^b   Leitner, Dietmar ^b   Strauss, Holger ^b   Wahl, Martin ^b   Kühne, Ronald ^b   Oschkinat, Hartmut ^b   Heinemann, Udo ^a,c  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CENTRIFUGATION; CONFORMATIONS; CRYSTAL STRUCTURE; NUCLEAR MAGNETIC RESONANCE; SIZE EXCLUSION CHROMATOGRAPHY; TUMORS;

BACKBONE DYNAMICS; CANCER-ASSOCIATED MUTATIONS; CELL-CYCLE PROGRESSION;

PROTEINS;

BRCA1 PROTEIN;

ARTICLE; BREAST CANCER; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; GEL PERMEATION CHROMATOGRAPHY; GENE FUNCTION; GENE MUTATION; GENE SEQUENCE; GENE STRUCTURE; MITOSIS RATE; NUCLEAR MAGNETIC RESONANCE; NUCLEOTIDE SEQUENCE; ONCOGENE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS; TRANSCRIPTION REGULATION; ULTRACENTRIFUGATION;

EID: 11144310680     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049550q     Document Type: Article

References (74)

1. Bork, P., Hofmann, K., Bucher, P., Neuwald, A. F., Altschul, S. F., and Koonin, E. V. (1997) A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins, FASEB J. 11, 68-76.
2. Callebaut, I., and Mornon, J. P. (1997) From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair, FEBS Lett. 400, 25-30.
3. Wu, L. C., Wang, Z. W., Tsan, J. T., Spillman, M. A., Phung, A., Xu, X. L., Yang, M. C., Hwang, L. Y., Bowcock, A. M., and Baer, R. (1996) Identification of a RING protein that can interact in vivo with the BRCA1 gene product, Nat. Genet. 14, 430-440.
4. Goldberg, M., Stucki, M., Falck, J., D'Amours, D., Rahman, D., Pappin, D., Bartek, J., and Jackson, S. P. (2003) MDC1 is required for the intra-S-phase DNA damage checkpoint, Nature 421, 952-956.
5. Lou, Z., Minter-Dykhouse, K., Wu, X., and Chen, J. (2003) MDC1 is coupled to activate CHK2 in mammalian DNA damage response pathways, Nature 421, 957-961.
6. Stewart, G. S., Wang, B., Bignell, C. R., Taylor, A. M., and Elledge, S. J. (2003) MDC1 is a mediator of the mammalian DNA damage checkpoint, Nature 421, 961-966.
7. Caldecott, K. W. (2003) Cell signaling. The BRCT domain: signaling with friends? Science 302, 579-580.
8. Koonin, E. V., Altschul, S. F., and Bork, P. (1996) BRCA1 protein products ... functional motifs ..., Nat. Genet. 13, 266-268.
9. Moore, D. J., Taylor, R. M., Clements, P., and Caldecott, K. W. (2000) Mutation of a BRCT domain selectively disrupts DNA single-strand break repair in non-cycling Chinese hamster ovary cells, Proc. Natl. Acad. Sci. U.S.A. 97, 13649-13654.
10. Xia, Z., Morales, J. C., Dunphy, W. G., and Carpenter, P. B. (2001) Negative cell cycle regulation and DNA damage-inducible phosphorylation of the BRCT protein 53BP1, J. Biol. Chem. 276, 2708-2718.
11. Makiniemi, M., Hillukkala, T., Tuusa, J., Reini, K., Vaara, M., Huang, D., Pospiech, H., Majuri, I., Westerling, T., Makela, T. P., and Syvaoja, J. E. (2001) BRCT domain-containing protein TopBP1 functions in DNA replication and damage response, J. Biol. Chem. 276, 30399-30406.
12. Yamane, K., Wu, X., and Chen, J. (2002) A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival, Mol. Cell. Biol. 22, 555-566.
13. Liu, K., Lin, F. T., Ruppert, J. M., and Lin, W. C. (2003) Regulation of E2F1 by BRCT domain-containing protein TopBP1, Mol. Cell. Biol. 23, 3287-3304.
14. Abbott, D. W., Thompson, M. E., Robinson-Benion, C., Tomlinson, G., Jensen, R. A., and Holt, J. T. (1999) BRCA1 expression restores radiation resistance in BRCA1-defective cancer cells through enhancement of transcription-coupled DNA repair, J. Biol. Chem. 274, 18808-18812.
15. Cantor, S. B., Bell, D. W., Ganesan, S., Kass, E. M., Drapkin, R., Grossman, S., Wahrer, D. C., Sgroi, D. C., Lane, W. S., Haber, D. A., and Livingston, D. M. (2001) BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function, Cell 105, 149-160.
16. Yarden, R. I., Pardo-Reoyo, S., Sgagias, M., Cowan, K. H., and Brody, L. C. (2002) BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage, Nat. Genet. 30, 285-289.
17. Gowen, L. C., Avrutskaya, A. V., Latour, A. M., Koller, B. H., and Leadon, S. A. (1998) BRCA1 required for transcription-coupled repair of oxidative DNA damage, Science 281, 1009-1012.
18. 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., and Haber, D. A. (1999) Induction of GADD45 and JNK/SAPK-dependent apoptosis following inducible expression of BRCA1, Cell 97, 575-586.
19. WAF1/CiP1, Nature 389, 187-190.
20. 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, 2544-2550.
21. Ludwig, T., Fisher, P., Ganesan, S., and Efstratiadis, A. (2001) Tumorigenesis in mice carrying a truncating Brca1 mutation, Genes Dev. 15, 1188-1193.
22. Ye, Q., Hu, Y. F., Zhong, H., Nye, A. C., Belmont, A. S., and Li, R. (2001) BRCA1-induced large-scale chromatin unfolding and allele-specific effects of cancer-predisposing mutations, J. Cell Biol. 155, 911-921.
23. Chapman, M. S., and Verma, I. M. (1996) Transcriptional activation by BRCA1, Nature 382, 678-679.
24. Monteiro, A. N., August, A., and Hanafusa, H. (1996) Evidence for a transcriptional activation function of BRCA1 C-terminal region, Proc. Natl. Acad. Sci. U.S.A. 93, 13595-13599.
25. Monteiro, A. N. (2000) BRCA1: exploring the links to transcription, Trends Biochem. Sci. 25, 469-474.
26. Miyake, T., Hu, Y. F., Yu, D. S., and Li, R. (2000) A functional comparison of BRCA1 C-terminal domains in transcription activation and chromatin remodeling, J. Biol. Chem. 275, 40169-40173.
27. Welcsh, P. L., Lee, M. K., Gonzalez-Hernandez, R. M., Black, D. J., Mahadevappa, M., Swisher, E. M., Warrington, J. A., and King, M. C. (2002) BRCA1 transcriptionally regulates genes involved in breast tumorigenesis, Proc. Natl. Acad. Sci. U.S.A. 99, 7560-7565.
28. Ouchi, T., Monteiro, A. N., August, A., Aaronson, S. A., and Hanafusa, H. (1998) BRCA1 regulates p53-dependent gene expression, Proc. Natl. Acad. Sci. U.S.A. 95, 2302-2306.
29. Chai, Y. L., Cui, J., Shao, N., Shyam, E., Reddy, P., and Rao, V. N. (1999) The second BRCT domain of BRCA1 proteins interacts with p53 and stimulates transcription from the p21WAF1/ciP1 promoter, Oncogene 18, 263-268.
30. Hayes, F., Cayanan, C., Barilla, D., and Monteiro, A. N. (2000) Functional assay for BRCA1: mutagenesis of the COOH-terminal region reveals critical residues for transcription activation, Cancer Res. 60, 2411-2418.
31. Williams, R. S., Chasman, D. I., Hau, D. D., Hui, B., Lau, A. Y., and Glover, J. N. (2003) Detection of protein folding defects caused by BRCA1-BRCT truncation and missense mutations, J. Biol. Chem. 278, 53007-53016.
32. Friedman, L. S., Ostermeyer, E. A., Szabo, C. I., Dowd, P., Lynch, E. D., Rowell, S. E., and King, M. C. (1994) Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families, Nat. Genet. 8, 399-404.
33. Miki, Y., Swensen, J., Shattuck-Eidens, D., Futreal, P. A., Harshman, K., Tavtigian, S., Liu, Q., Cochran, C., Bennett, L. M., Ding, W., et al. (1994) A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1, Science 266, 66-71.
34. Futreal, P. A., Liu, Q., Shattuck-Eidens, D., Cochran, C., Harshman, K., Tavtigian, S., Bennett, L. M., Haugen-Strano, A., Swensen, J., Miki, Y., et al. (1994) BRCA1 mutations in primary breast and ovarian carcinomas, Science 266, 120-122.
35. Breast Cancer Information Core (BIC), http://research.nhgri.nih.gov/bic/.
36. Yarden, R. I., and Brody, L. C. (1999) BRCA1 interacts with components of the histone deacetylase complex, Proc. Natl. Acad. Sci. U.S.A. 96, 4983-4988.
37. Yu, X., Wu, L. 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.
38. 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.
39. Yamane, K., Katayama, E., and Tsuruo, T. (2000) The BRCT regions of tumor suppressor BRCA1 and of XRCC1 show DNA end binding activity with a multimerizing feature, Biochem. Biophys. Res. Commun. 279, 678-684.
40. 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.
41. 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.
42. Rodriguez, M., Yu, X., Chen, J., and Songyang, Z. (2003) Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains, J. Biol. Chem. 278, 52914-52918.
43. 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.
44. 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.
45. Joo, W. S., Jeffrey, P. D., Cantor, S. B., Finnin, M. S., Livingston, D. M., and Pavletich, N. P. (2002) Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brca1 BRCT structure, Genes Dev. 16, 583-593.
46. Derbyshire, D. J., Basu, B. P., Serpell, L. C., Joo, W. S., Date, T., Iwabuchi, K., and Doherty, A. J. (2002) Crystal structure of the human 53BP1 BRCT domains bound to p53 tumour suppressor, EMBO J. 21, 3863-3872.
47. Zhang, X., Moréra, S., Bates, P. A., Whitehead, P. C., Coffer, A. I., Hainbucher, K., Nash, R. A., Sternberg, M. J., Lindahl, T., and Freemont, P. S. (1998) Structure of an XRCC1 BRCT domain: a new protein-protein interaction module, EMBO J. 17, 6404-6411.
48. Krishnan, V. V., Thornton, K. H., Thelen, M. P., and Cosman, M. (2001) Solution structure and backbone dynamics of the human DNA liganse IIIα BRCT domain, Biochemistry 40, 13158-13166.
49. +- dependent DNA ligase: modular architecture and functional implications, Embo J. 19, 1119-1129.
50. Shiozaki, E. N., Gu, L., Yan, N., and Shi, Y. (2004) Structure of the BRCT repeats of BRCA1 bound to a BACH1 phosphopeptide: implications for signaling, Mol. Cell 14, 405-412.
51. Clapperton, J. A., Manke, I. A., Lowery, D. M., Ho, T., Haire, L. F., Yaffe, M. B., and Smerdon, S. J. (2004) Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer, Nat. Struct. Mol. Biol. 11, 512-518.
52. Williams, R. S., Lee, M. S., Hau, D. D., and Glover, J. N. (2004) Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1, Nat. Struct. Mol. Biol. 11, 519-525.
53. Neidhardt, F. C., Bloch, P. L., and Smith, D. F. (1974) Culture medium for enterobacteria, J. Bacteriol. 119, 736-747.
54. Kanelis, V., Forman-Kay, J. D., and Kay, L. E. (2001) Multi-dimensional NMR methods for protein structure determination, IUBMB Life 52, 291-302.
55. Goddard, T. D., and Kneller, D. G. (2003) SPARKY 3, University of California, San Francisco.
56. Ball, L. J., Kühne, R., Hoffmann, B., Hafner, A., Schmieder, P., Volkmer-Engert, R., Hof, M., Wahl, M., Schneider-Mergener, J., Walter, U., Oschkinat, H., and Jarchau, T. (2000) Dual epitope recognition by the VASP EVH1 domain modulates polyproline ligand specificity and binding affinity, EMBO J. 19, 4903-4914.
57. 1H 2D NMR spectra by interactive graphics, J. Magn. Reson. 24, 627-633.
58. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
59. 1H]-COSY experiments, J. Biomol. NMR 2, 257-274.
60. Zamyatnin, A. A. (1972) Protein volume in solution, Prog. Biophys. Mol. Biol. 24, 107-123.
61. Zamyatnin, A. A. (1984) Amino acid, peptide, and protein volume in solution, Annu. Rev. Biophys. Bioeng. 13, 145-165.
62. Lamm, O. (1929) Die Differentialgleichung der Ultrazentrifugierung, Ark. Mat., Astron. Fys. 21B, 1-4.
63. Schuck, P. (1998) Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation, Biophys. J. 75, 1503-1512.
64. Behlke, J., and Ristau, O. (1997) Molecular mass determination by sedimentation velocity experiments and direct fitting of the concentration profiles, Biophys. J. 72, 428-434.
65. Behlke, J., and Ristau, O. (2002) A new approximate whole boundary solution of the Lamm differential equation for the analysis of sedimentation velocity experiments, Biophys. Chem. 95, 59-68.
66. Van Holde, K. E., and Weischet, W. O. (1978) Boundary analysis of sedimentation velocity experiments with monodisperse and paucidisperse solutes, Biopolymers 17, 1387-1403.
67. Demeler, B., Saber, H., and Hansen, J. C. (1997) Identification and interpretation of complexity in sedimentation velocity boundaries, Biophys. J. 72, 397-407.
68. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
69. Johnson, M. L., Correia, J. J., Yphantis, D. A., and Halvorson, H. R. (1981) Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques, Biophys. J. 36, 575-588.
70. McRorie, D. K., and Voelker, P. J. (1993) Self-Associating Systems in the Analytical Ultracentrifuge, Beckman Instruments, Inc., Fullerton, CA.
71. Williams, R. S., and Glover, J. N. (2003) Structural consequences of a cancer-causing BRCA1-BRCT missense mutation, J. Biol. Chem. 278, 2630-2635.
72. Koonin, E. V., Wolf, Y. I., and Karev, G. P. (2002) The structure of the protein universe and genome evolution, Nature 420, 218-223.
73. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR, J. Biomol. NMR 8, 477-486.
74. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.