Boundaries and physical characterization of a new domain shared between mammalian 53BP1 and yeast Rad9 checkpoint proteins

Protein Science

Volumn 14, Issue 7, 2005, Pages 1827-1839

  Alpha Bazin, Béatrice ^a,c   Lorphelin, Alain ^a   Nozerand, Nathalie ^a   Charier, Gaëlle ^b   Marchetti, Charles ^a   Bérenguer, Frédéric ^a   Couprie, Joël ^b   Gilquin, Bernard ^b   Zinn Justin, Sophie ^b   Quéméneur, Eric ^a  

^a DIF   (France)

^b CEA SACLAY   (France)

^c CEA Marcoule   (France)

Author keywords

Cell cycle checkpoint; DNA damage; Mouse 53bp1; Protein domain; Tudor domain; Yeast Rad9

Indexed keywords

GLOBULAR PROTEIN; PROTEIN; PROTEIN RAD9;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA DAMAGE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; YEAST;

AMINO ACID SEQUENCE; BRCA1 PROTEIN; CELL CYCLE PROTEINS; DNA DAMAGE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEIN P53;

EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 22244459207     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041305205     Document Type: Article

References (60)

1. Aboussekhra, A., Vialard, J.E., Morrison, D.E., de la Torre-Ruiz, M.A., Cernakova, L., Fabre, F., and Lowndes, N.F. 1996. A novel role for the budding yeast RAD9 checkpoint gene in DNA damage-dependent transcription. EMBO J. 15: 3912-3922.
2. Aslanidis, C. and de Jong, P.J. 1990. Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res. 18: 6069-6074.
3. Baneyx, F. 1999. Recombinant protein expression in Escherichia coli. Curr. Opin. Biotechnol. 10: 411-421.
4. 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.
5. Callebaut, I. and Mornon, J.P. 1997a. From BRCA1 to RAP1: A widespread BRCT module closely associated with DNA repair. FEBS Lett. 400: 25-30.
6. _. 1997b. The human EBNA-2 coactivator p100: Multidomain organization and relationship to the staphylococcal nuclease fold and to the tudor protein involved in Drosophila melanogaster development. Biochem. J. 321: 125-132.
7. Chang, J.Y. 1985. Thrombin specificity. Requirement for apolar amino acids adjacent to the thrombin cleavage site of polypeptide substrate. Eur. J. Biochem. 151: 217-224.
8. 15N resonance assignments of the region 1463-1617 of the mouse p53 binding protein 1 (53BP1). J. Biomol. NMR 28: 303-304.
9. Charier, G., Couprie, J., Alpha-Bazin, B., Meyer, V., Quemeneur, E., Guerois, R., Callebaut, I., Gilquin, B., and Zinn-Justin, S. 2004b. The Tudor tandem of 53BP1: A new structural motif involved in DNA and RG-rich peptide binding. Structure (Camb.) 12: 1551-1562.
10. Cordingley, M.G., Callahan, P.L., Sardana, V.V., Garsky, V.M., and Colonno, R.J. 1990. Substrate requirements of human rhinovirus 3C protease for peptide cleavage in vitro. J. Biol. Chem. 265: 9062-9065.
11. DiTullio Jr., R.A., Mochan, T.A., Venere, M., Bartkova, J., Sehested, M., Bartek, J., and Halazonetis, T.D. 2002. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 4: 998-1002.
12. Doerks, T., Copley, R.R., Schultz, J., Ponting, C.P., and Bork, P. 2002. Systematic identification of novel protein domain families associated with nuclear functions. Genome Res. 12: 47-56.
13. Durocher, D., Henckel, J., Fersht, A.R., and Jackson, S.P. 1999. The FHA domain is a modular phosphopeptide recognition motif. Mol. Cell 4: 387-394.
14. Fernandez-Capetillo, O., Chen, H.T., Celeste, A., Ward, I., Romanienko, P.J., Morales, J.C., Naka, K., Xia, Z., Camerini-Otero, R.D., Motoyama, N., et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4: 993-997.
15. Haun, R.S. and Moss, J. 1992. Ligation-independent cloning of glutathione S-transferase fusion genes for expression in Escherichia coli. Gene 112: 37-43.
16. Haun, R.S., Serventi, I.M., and Moss, J. 1992. Rapid, reliable ligation-independent cloning of PCR products using modified plasmid vectors. Biotechniques 13: 515-518.
17. Hochuli, E. 1988. Large-scale chromatography of recombinant proteins. J. Chromatogr. 444: 293-302.
18. Huyen, Y., Zgheib, O., Ditullio Jr., R.A., Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S., and Halazonetis, T.D. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432: 406-411.
19. Huyton, T., Bates, P.A., Zhang, X., Sternberg, M.J., and Freemont, P.S. 2000. The BRCA1 C-terminal domain: Structure and function. Mutat. Res. 460: 319-332.
20. Iwabuchi, K., Li, B., Massa, H.F., Trask, B.J., Date, T., Fields, S., Bartel, P.L., and Marraccino, R. 1998. Stimulation of p53-mediated transcriptional activation by the p53-binding proteins, 53BP1 and 53BP2 two cellular proteins that bind to wild-type but not mutant p53. J. Biol. Chem. 273: 26061-26068.
21. Iwabuchi, K., Basu, B.P., Kysela, B., Kurihara, T., Shibata, M., Guan, D., Cao, Y., Hamada, T., Imamura, K., Jeggo, P.A., et al. 2003. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278: 36487-36495. http://www.jbc.org.
22. Janin, J. and Chothia, C. 1985. Domains in proteins: Definitions, location, and structural principles. Methods Enzymol. 115: 420-430.
23. Jullien, D., Vagnarelli, P., Earnshaw, W.C., and Adachi, Y. 2002. Kinetochore localisation of the DNA damage response component 53BP1 during mitosis. J. Cell Sci. 115: 71-79.
24. Kawahire, S., Takeuchi, M., Gohshi, T., Sasagawa, S., Shimada, M., Takahashi, M., Abe, T.K., Ueda, T., Kuwano, R., Hikawa, A., et al. 1997. cDNA cloning of nuclear localization signal binding protein NBP60, a rat homologue of lamin B receptor, and identification of binding sites of human lamin B receptor for nuclear localization signals and chromatin. J. Biochem. (Tokyo) 121: 881-889.
25. Koonin, E.V., Altschul, S.F., and Bork, P. 1996. BRCA1 protein products... Functional motifs. Nat. Genet. 13: 266-268.
26. Kumagai, A. and Dunphy, W.G. 2000. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 6: 839-849.
27. LaVallie, E.R., DiBlasio, E.A., Kovacic, S., Grant, K.L., Schendel, P.F., and McCoy, J.M. 1993. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (N Y) 11: 187-193.
28. Lowndes, N.F. and Murguia, J.R. 2000. Sensing and responding to DNA damage. Curr. Opin. Genet. Dev. 10: 17-25.
29. Maurer-Stroh, S., Dickens, N.J., Hughes-Davies, L., Kouzarides, T., Eisenhaber, F., and Ponting, C.P. 2003. The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci. 28: 69-74.
30. McGuffin, L.J., Bryson, K., and Jones, D.T. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
31. Melo, J. and Toczyski, D. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14: 237-245.
32. Motoyama, N. and Naka, K. 2004. DNA damage tumor suppressor genes and genomic instability. Curr. Opin. Genet. Dev. 14: 11-16.
33. Nyberg, K.A., Michelson, R.J., Putnam, C.W., and Weinert, T.A. 2002. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36: 617-656.
34. Parks, T.D., Leuther, K.K., Howard, E.D., Johnston, S.A., and Dougherty, W.G. 1994. Release of proteins and peptides from fusion proteins using a recombinant plant virus proteinase. Anal. Biochem. 216: 413-417.
35. Ponting, C.P. 1997a. P100, a transcriptional coactivator, is a human homologue of staphylococcal nuclease. Protein Sci. 6: 459-463.
36. _. 1997b. Tudor domains in proteins that interact with RNA. Trends Biochem. Sci. 22: 51-52.
37. Privalov, P.L. and Potekhin, S.A. 1986. Scanning microcalorimetry in studying temperature-induced changes in proteins. Methods Enzymol. 131: 4-51.
38. Qiu, C., Sawada, K., Zhang, X., and Cheng, X. 2002. The PWWP domain of mammalian DNA methyltransferase Dnmt3b defines a new family of DNA-binding folds. Nat. Struct. Biol. 9: 217-224.
39. Rouse, J. and Jackson, S.P. 2002. Interfaces between the detection, signaling, and repair of DNA damage. Science 297: 547-551.
40. Schein, C.H. 1990. Solubility as a function of protein structure and solvent components. Biotechnology (N Y) 8: 308-317.
41. Schiestl, R.H., Reynolds, P., Prakash, S., and Prakash, L. 1989. Cloning and sequence analysis of the Saccharomyces cerevisiae RAD9 gene and further evidence that its product is required for cell cycle arrest induced by DNA damage. Mol. Cell. Biol. 9: 1882-1896.
42. Selenko, P., Sprangers, R., Stier, G., Buhler, D., Fischer, U., and Sattler, M. 2001. SMN tudor domain structure and its interaction with the Sm proteins. Nat. Struct. Biol. 8: 27-31.
43. Siede, W., Friedberg, A.S., Dianova, I., and Friedberg, E.C. 1994. Characterization of G1 checkpoint control in the yeast Saccharomyces cerevisiae following exposure to DNA-damaging agents. Genetics 138: 271-281.
44. Slater, L.M., Allen, M.D., and Bycroft, M. 2003. Structural variation in PWWP domains. J. Mol. Biol. 330: 571-576.
45. Smith, D.B. and Johnson, K.S. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67: 31-40.
46. Sprangers, R., Groves, M.R., Sinning, I., and Sattler, M. 2003a. High-resolution X-ray and NMR structures of the SMN Tudor domain: Conformational variation in the binding site for symmetrically dimethylated arginine residues. J. Mol. Biol. 327: 507-520.
47. Sprangers, R., Selenko, P., Sattler, M., Sinning, I., and Groves, M.R. 2003b. Definition of domain boundaries and crystallization of the SMN Tudor domain. Acta Crystallogr. D Biol. Crystallogr. 59: 366-368.
48. Stec, I., Nagl, S.B., van Ommen, G.J., and den Dunnen, J.T. 2000. The PWWP domain: A potential protein-protein interaction domain in nuclear proteins influencing differentiation? FEBS Lett. 473: 1-5.
49. Swartz, J.R. 2001. Advances in Escherichia coli production of therapeutic proteins. Curr. Opin. Biotechnol. 12: 195-201.
50. Tanaka, K. and Russell, P. 2001. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3: 966-972.
51. Thompson, J.D., Higgins, D.G., and Gibson, T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
52. Walhout, A.J., Temple, G.F., Brasch, M.A., Hartley, J.L., Lorson, M.A., van den Heuvel, S., and Vidal, M. 2000. GATEWAY recombinational cloning: Application to the cloning of large numbers of open reading frames or ORFeomes. Methods Enzymol. 328: 575-592.
53. Wang, B., Matsuoka, S., Carpenter, P.B., and Elledge, S.J. 2002. 53BP1, a mediator of the DNA damage checkpoint. Science 298: 1435-1438. http://www.sciencemag.org.
54. Ward, I.M., Minn, K., van Deursen, J., and Chen, J. 2003. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23: 2556-2563.
55. Weinert, T. and Hartwell, L. 1989. Control of G2 delay by the rad9 gene of Saccharomyces cerevisiae. J. Cell Sci. Suppl. 12: 145-148.
56. Weinert, T.A., Kiser, G.L., and Hartwell, L.H. 1994. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes & Dev. 8: 652-665.
57. Wetlaufer, D.B. 1973. Nucleation, rapid folding, and globular intrachain regions in proteins. Proc. Natl. Acad. Sci. 70: 697-701.
58. Wilkinson, D.L. and Harrison, R.G. 1991. Predicting the solubility of recombinant proteins in Escherichia coli. Biotechnology (N Y) 9:443-448.
59. 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.
60. Zhou, B.B. and Elledge, S.J. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408: 433-439.