Specific recognition of phosphorylated tail of H2AX by the tandem BRCT domains of MCPH1 revealed by complex structure

Journal of Structural Biology

Volumn 177, Issue 2, 2012, Pages 459-468

  Shao, Zhenhua ^a   Li, Fudong ^a   Sy, Shirley M H ^b   Yan, Wei ^a   Zhang, Zhiyong ^a   Gong, Deshun ^a   Wen, Bin ^a   Huen, Michael S Y ^b   Gong, Qingguo ^a   Wu, Jihui ^a   Shi, Yunyu ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

H2AX; BRCT; DNA damage; MCPH1; MDC1; SWI SNF

Indexed keywords

BRCA1 PROTEIN; BRCT PROTEIN; HISTONE H2AX; MCPH1 PROTEIN; PHOSPHOPEPTIDE; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; FLUORESCENCE POLARIZATION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HISTONES; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; SEQUENCE ALIGNMENT; SURFACE PROPERTIES;

EID: 84857033669     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.11.022     Document Type: Article

References (48)

1. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 2001, 15:2177-2196.
2. Afonine P.V., Grosse-Kunstleve R.W., Adams P.D. A robust bulk-solvent correction and anisotropic scaling procedure. Acta Crystallogr. Sect D: Biol. Crystallogr. 2005, 61:850-855.
3. Bailey S. The Ccp4 suite - programs for protein crystallography. Acta Crystallogr. Sect. D: Biol. Crystallogr. 1994, 50:760-763.
4. Bassing C.H., Alt F.W. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst) 2004, 3:781-796.
5. Berendsen H.J.C., Postma J.P.M., Vangunsteren W.F., Dinola A., et al. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81:3684-3690.
6. Bussi G., Donadio D., Parrinello M. Canonical sampling through velocity rescaling. J. Chem. Phys. 2007, 126.
7. Campbell S.J., Edwards R.A., Glover J.N.M. Comparison of the structures and peptide binding specificities of the BRCT domains of MDC1 and BRCA1. Structure 2010, 18:167-176.
8. Clapperton J.A., Manke I.A., Lowery D.M., Ho T., Haire L.F., et al. Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer. Nat. Struct. Mol. Biol. 2004, 11:512-518.
9. Coquelle N., Green R., Glover J.N.M. Impact of BRCA1 BRCT domain missense substitutions on phosphopeptide recognition. Biochemistry 2011, 50:4579-4589.
10. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D: Biol. Crystallogr. 2004, 60:2126-2132.
11. Essmann U., Perera L., Berkowitz M.L., Darden T., Lee H., et al. A smooth particle mesh Ewald method. J. Chem. Phys. 1995, 103:8577-8593.
12. Fernandez-Capetillo O., Lee A., Nussenzweig M., Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair (Amst) 2004, 3:959-967.
13. Hess B. P-LINCS: a parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput. 2008, 4:116-122.
14. Hess B., Kutzner C., van der Spoel D., Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 2008, 4:435-447.
15. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 1993, 233:123-138.
16. Huen M.S., Huang J., Leung J.W., Sy S.M., Leung K.M., et al. Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol. Cell 2010, 37:854-864.
17. Jackson A.P., Eastwood H., Bell S.M., Adu J., Toomes C., et al. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 2002, 71:136-142.
18. Joo W.S., Jeffrey P.D., Cantor S.B., Finnin M.S., Livingston D.M., et al. Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brcal1 BRCT structure. Genes Dev. 2002, 16:583-593.
19. Kilkenny M.L., Dore A.S., Roe S.M., Nestoras K., Ho J.C.Y., et al. Structural and functional analysis of the Crb2-BRCT2 domain reveals distinct roles in checkpoint signaling and DNA damage repair. Genes Dev. 2008, 22:2034-2047.
20. Kumar A., Markandaya M., Girimaji S.C. Primary microcephaly: microcephalin and ASPM determine the size of the human brain. J. Biosci. 2002, 27:629-632.
21. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
22. Lee M.S., Edwards R.A., Thede G.L., Glover J.N.M. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J. Biol. Chem. 2005, 280:32053-32056.
23. Leung C.C.Y., Gong Z.H., Chen J.J., Glover J.N.M. Molecular Basis of BACH1/FANCJ recognition by TopBP1 in DNA replication checkpoint control. J. Biol. Chem. 2011, 286:4292-4301.
24. Lin S.Y., Elledge S.J. Multiple tumor suppressor pathways negatively regulate telomerase. Cell 2003, 113:881-889.
25. Lin S.Y., Rai R., Li K., Xu Z.X., Elledge S.J. BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl. Acad. Sci. USA 2005, 102:15105-15109.
26. Lin S.Y., Liang Y., Li K. Multiple roles of BRIT1/MCPH1 in DNA damage response, DNA repair, and cancer suppression. Yonsei Med. J. 2010, 51:295-301.
27. Lok G.T., Sy S.M., Dong S.S., Ching Y.P., Tsao S.W., et al. Differential regulation of RNF8-mediated Lys48- and Lys63-based poly-ubiquitylation. Nucleic Acids Res. 2011.
28. MacKerell A.D., Bashford D., Bellott M., Dunbrack R.L., Evanseck J.D., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 1998, 102:3586-3616.
29. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. Sect. D: Biol. Crystallogr. 2005, 61:458-464.
30. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D: Biol. Crystallogr. 1997, 53:240-255.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. Pt A 1997, 276:307-326.
32. Pei H.D., Zhang L., Luo K.T., Qin Y.X., Chesi M., et al. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 2011, 470:124-128.
33. Peng G., Yim E.K., Dai H., Jackson A.P., Burgt I., et al. BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat. Cell Biol. 2009, 11:865-872.
34. Rai R., Dai H., Multani A.S., Li K., Chin K., et al. BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 2006, 10:145-157.
35. Shiozaki E.N., Gu L.C., Yan N., Shi Y.G. Structure of the BRCT repeats of BRCA1 bound to a BACH1 phosphopeptide: implications for signaling. Mol. Cell 2004, 14:405-412.
36. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., et al. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005, 123:1213-1226.
37. Trimborn M., Bell S.M., Felix C., Rashid Y., Jafri H., et al. Mutations in microcephalin cause aberrant regulation of chromosome condensation. Am. J. Hum. Genet. 2004, 75:261-266.
38. Trimborn M., Richter R., Sternberg N., Gavvovidis I., Schindler D., et al. The first missense alteration in the MCPH1 gene causes autosomal recessive microcephaly with an extremely mild cellular and clinical phenotype. Hum. Mutat. 2005, 26:496.
39. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
40. Verlet L. Computer experiments on classical fluids: I. Thermodynamical properties of Lennard-Jones molecules. Phys. Rev. 1967, 159:98-103.
41. Wang J.K., Li Y., Su B. A common SNP of MCPH1 is associated with cranial volume variation in Chinese population. Hum. Mol. Genet. 2008, 17:1329-1335.
42. Williams J.S., Williams R.S., Dovey C.L., Guenther G., Tainer J.A., et al. Gamma H2A binds Brc1 to maintain genome integrity during S-phase. EMBO J. 2010, 29:1136-1148.
43. Wood J.L., Singh N., Mer G., Chen J. MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J. Biol. Chem. 2007, 282:35416-35423.
44. Woods C.G., Bond J., Enard W. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 2005, 76:717-728.
45. Wu X., Mondal G., Wang X., Wu J., Yang L., et al. Microcephalin regulates BRCA2 and Rad51-associated DNA double-strand break repair. Cancer Res. 2009, 69:5531-5536.
46. Xu X., Lee J., Stern D.F. Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem. 2004, 279:34091-34094.
47. Yang S.Z., Lin F.T., Lin W.C. MCPH1/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis. EMBO Rep. 2008, 9:907-915.
48. Yuan J., Adamski R., Chen J. Focus on histone variant H2AX: to be or not to be. FEBS Lett. 2010, 584:3717-3724.