Charting the landscape of tandem BRCT domain-mediated protein interactions

Science Signaling

Volumn 5, Issue 242, 2012, Pages

  Woods, Nicholas T ^a   Mesquita, Rafael D ^b,g   Sweet, Michael ^a,c   Carvalho, Marcelo A ^b,d   Li, Xueli ^a   Liu, Yun ^e   Nguyen, Huey ^a   Thomas, C Eric ^a   Iversen, Edwin S ^f   Marsillac, Sylvia ^a   Karchin, Rachel ^e   Koomen, John ^a   Monteiro, Alvaro N A ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b INSTITUTO FEDERAL DE EDUCAÇÃO   (Brazil)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d INSTITUTO NACIONAL DE CÂNCER   (Brazil)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f Duke University   (United States)

^g FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA DAMAGE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; TWO HYBRID SYSTEM;

EUKARYOTA;

EID: 84866525932     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002255     Document Type: Article

References (93)

1. J. W. Harper, S. J. Elledge, The DNA damage response: Ten years after. Mol. Cell 28, 739-745 (2007).
2. J. Bartkova, Z. Horejsi, K. Koed, A. Krämer, F. Tort, K. Zieger, P. Guldberg, M. Sehested, J. M. Nesland, C. Lukas, T. Ørntoft, J. Lukas, J. Bartek, DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870 (2005).
3. V. G. Gorgoulis, L. V. Vassiliou, P. Karakaidos, P. Zacharatos, A. Kotsinas, T. Liloglou, M. Venere, R. A. Ditullio Jr., N. G. Kastrinakis, B. Levy, D. Kletsas, A. Yoneta, M. Herlyn, C. Kittas, T. D. Halazonetis, Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913 (2005).
4. P. C. Fong, D. S. Boss, T. A. Yap, A. Tutt, P. Wu, M. Mergui-Roelvink, P. Mortimer, H. Swaisland, A. Lau, M. J. O'Connor, A. Ashworth, J. Carmichael, S.B.Kaye, J. H. Schellens, J. S. de Bono, Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361, 123-134 (2009).
5. T. Helleday, E. Petermann, C. Lundin, B. Hodgson, R. A. Sharma, DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8, 193-204 (2008).
6. T. Pawson, P. Nash, Assembly of cell regulatory systems through protein interaction domains. Science 300, 445-452 (2003).
7. R. P. Bhattacharyya, A. Reményi, B. J. Yeh, W. A. Lim, Domains, motifs, and scaffolds: The role of modular interactions in the evolution and wiring of cell signaling circuits. Annu. Rev. Biochem. 75, 655-680 (2006).
8. I. A. Manke, D. M. Lowery, A. Nguyen, M. B. Yaffe, BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302, 636-639 (2003).
9. X. Yu, C. C. Chini, M. He, G. Mer, J. Chen, The BRCT domain is a phospho-protein binding domain. Science 302, 639-642 (2003).
10. W. A. Lim, T. Pawson, Phosphotyrosine signaling: Evolving a new cellular communication system. Cell 142, 661-667 (2010).
11. R. B. Birge, H. Hanafusa, Closing in on SH2 specificity. Science 262, 1522-1524 (1993).
12. D. H. Mohammad, M. B. Yaffe, 14-3-3 proteins, FHA domains and BRCT domains in the DNA damage response. DNA Repair 8, 1009-1017 (2009).
13. E. V. Koonin, S. F. Altschul, P. Bork, BRCA1 protein products... Functional motifs... Nat. Genet. 13, 266-268 (1996).
14. I. Callebaut, J. P. Mornon, From BRCA1 to RAP1: A widespread BRCT module closely associated with DNA repair. FEBS Lett. 400, 25-30 (1997).
15. P. Bork, K. Hofmann, P. Bucher, A. F. Neuwald, S. F. Altschul, E. V. Koonin, A super-family of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 11, 68-76 (1997).
16. R. D. Mesquita, N. T. Woods, E. S. Seabra-Junior, A. N. Monteiro, Tandem BRCT domains: DNA's Praetorian Guard. Genes Cancer 1, 1140-1146 (2010).
17. M. Rodriguez, X. Yu, J. Chen, Z. Songyang, Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains. J. Biol. Chem. 278, 52914-52918 (2003).
18. N. Mirkovic, M. A. Marti-Renom, B. L. Weber, A. Sali, A. N. Monteiro, Structure-based assessment of missense mutations in human BRCA1: Implications for breast and ovarian cancer predisposition. Cancer Res. 64, 3790-3797 (2004).
19. W. S. Joo, P. D. Jeffrey, S. B. Cantor, M. S. Finnin, D. M. Livingston, N. P. Pavletich, Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brca1 BRCT structure. Genes Dev. 16, 583-593 (2002).
20. M. V. Botuyan, Y. Nominé, X. Yu, N. Juranic, S. Macura, J. Chen, G. Mer, Structural basis of BACH1 phosphopeptide recognition by BRCA1 tandem BRCT domains. Structure 12, 1137-1146 (2004).
21. R. S. Williams, M. S. Lee, D. D. Hau, J. N. Glover, Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1. Nat. Struct. Mol. Biol. 11, 519-525 (2004).
22. J. A. Clapperton, I. A. Manke, D. M. Lowery, T. Ho, L. F. Haire, M. B. Yaffe, S. J. Smerdon, Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer. Nat. Struct. Mol. Biol. 11, 512-518 (2004).
23. E. N. Shiozaki, L. Gu, N. Yan, Y. Shi, Structure of the BRCT repeats of BRCA1 bound to a BACH1 phosphopeptide: Implications for signaling. Mol. Cell 14, 405-412 (2004).
24. A. Ghosh, S. Shuman, C. D. Lima, The structure of Fcp1, an essential RNA polymerase II CTD phosphatase. Mol. Cell 32, 478-490 (2008).
25. M. Ashburner, C. A. Ball, J. A. Blake, D. Botstein, H. Butler, J. M. Cherry, A. P. Davis, K. Dolinski, S. S. Dwight, J. T. Eppig, M. A. Harris, D. P. Hill, L. Issel-Tarver, A. Kasarskis, S. Lewis, J. C. Matese, J. E. Richardson, M. Ringwald, G. M. Rubin, G. Sherlock, Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29 (2000).
26. E. Soutoglou, T. Misteli, Activation of the cellular DNA damage response in the absence of DNA lesions. Science 320, 1507-1510 (2008).
27. E. Sprinzak, S. Sattath, H. Margalit, How reliable are experimental protein-protein interaction data? J. Mol. Biol. 327, 919-923 (2003).
28. T. Ito, T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, Y. Sakaki, A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. U.S.A. 98, 4569-4574 (2001).
29. L. Giot, J. S. Bader, C. Brouwer, A. Chaudhuri, B. Kuang, Y. Li, Y. L. Hao, C. E. Ooi, B. Godwin, E. Vitols, G. Vijayadamodar, P. Pochart, H. Machineni, M. Welsh, Y. Kong, B. Zerhusen, R. Malcolm, Z. Varrone, A. Collis, M. Minto, S. Burgess, L. McDaniel, E. Stimpson, F. Spriggs, J. Williams, K. Neurath, N. Ioime, M. Agee, E. Voss, K. Furtak, R. Renzulli, N. Aanensen, S. Carrolla, E. Bickelhaupt, Y. Lazovatsky, A. DaSilva, J. Zhong, C. A. Stanyon, R. L. Finley Jr., K. P. White, M. Braverman, T. Jarvie, S. Gold, M. Leach, J. Knight, R. A. Shimkets, M. P. McKenna, J. Chant, J. M. Rothberg, A protein interaction map of Drosophila melanogaster. Science 302, 1727-1736 (2003).
30. H. Goehler, M. Lalowski, U. Stelzl, S. Waelter, M. Stroedicke, U. Worm, A. Droege, K. S. Lindenberg, M. Knoblich, C. Haenig, M. Herbst, J. Suopanki, E. Scherzinger, C. Abraham, B. Bauer, R. Hasenbank, A. Fritzsche, A. H. Ludewig, K. Büssow, S. H. Coleman, C. A. Gutekunst, B. G. Landwehrmeyer, H. Lehrach, E. E. Wanker, A protein interaction network links GIT1, an enhancer of huntingtin aggregation, to Huntington's disease. Mol. Cell 15, 853-865 (2004).
31. S. Li, C. M. Armstrong, N. Bertin, H. Ge, S. Milstein, M. Boxem, P. O. Vidalain, J. D. Han, A. Chesneau, T. Hao, D. S. Goldberg, N. Li, M. Martinez, J. F. Rual, P. Lamesch, L. Xu, M. Tewari, S. L. Wong, L. V. Zhang, G. F. Berriz, L. Jacotot, P. Vaglio, J. Reboul, T. Hirozane-Kishikawa, Q. Li, H.W. Gabel, A. Elewa, B. Baumgartner, D. J. Rose, H. Yu, S. Bosak, R. Sequerra, A. Fraser, S. E. Mango,W. M. Saxton, S. Strome, H. S. Van Den, F. Piano, J. Vandenhaute, C. Sardet, M. Gerstein, L. Doucette-Stamm, K. C. Gunsalus, J. W. Harper, M. E. Cusick, F. P. Roth, D. E. Hill, M. Vidal, A map of the interactome network of the metazoan C. elegans. Science 303, 540-543 (2004).
32. Y. Ho, A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Yang, C. Wolting, I. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sørensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. Hogue, D. Figeys, M. Tyers, Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415, 180-183 (2002).
33. Y. Liu, N. T. Woods, D. Kim, M. Sweet, A. N. Monteiro, R. Karchin, Yeast two-hybrid junk sequences contain selected linear motifs. Nucleic Acids Res. 39, e128 (2011).
34. P. Aloy, R. B. Russell, The third dimension for protein interactions and complexes. Trends Biochem. Sci. 27, 633-638 (2002).
35. C. von Mering, R. Krause, B. Snel, M. Cornell, S. G. Oliver, S. Fields, P. Bork, Comparative assessment of large-scale data sets of protein-protein interactions. Nature 417, 399-403 (2002).
36. A. Martin, M. E. Ochagavia, L. C. Rabasa, J. Miranda, J. Fernandez-de-Cossio, R. Bringas, BisoGenet: A new tool for gene network building, visualization and analysis. BMC Bioinformatics 11, 91 (2010).
37. B. Wang, S. Matsuoka, B. A. Ballif, D. Zhang, A. Smogorzewska, S. P. Gygi, S. J. Elledge, Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316, 1194-1198 (2007).
38. R. A. Greenberg, B. Sobhian, S. Pathania, S. B. Cantor, Y. Nakatani, D. M. Livingston, Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20, 34-46 (2006).
39. X. Yu, J. Chen, DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24, 9478-9486 (2004).
40. B. Neumann, T. Walter, J. K. Hériché, J. Bulkescher, H. Erfle, C. Conrad, P. Rogers, I. Poser, M. Held, U. Liebel, C. Cetin, F. Sieckmann, G. Pau, R. Kabbe, A. Wünsche, V. Satagopam, M. H. Schmitz, C. Chapuis, D.W. Gerlich, R. Schneider, R. Eils, W. Huber, J. M. Peters, A. A. Hyman, R. Durbin, R. Pepperkok, J. Ellenberg, Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727 (2010).
41. E. Burstein, L. Ganesh, R. D. Dick, B. van De Sluis, J. C. Wilkinson, L. W. Klomp, C. Wijmenga, G. J. Brewer, G. J. Nabel, C. S. Duckett, A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J. 23, 244-254 (2004).
42. B. van de Sluis, P. Muller, K. Duran, A. Chen, A. J. Groot, L. W. Klomp, P. P. Liu, C. Wijmenga, Increased activity of hypoxia-inducible factor 1 is associated with early embryonic lethality in Commd1 null mice. Mol. Cell. Biol. 27, 4142-4156 (2007).
43. G. N. Maine, X. Mao, C. M. Komarck, E. Burstein, COMMD1 promotes the ubiquitination of NF-kB subunits through a cullin-containing ubiquitin ligase. EMBO J. 26, 436-447 (2007).
44. R. D. Kennedy, J. E. Quinn, P. B. Mullan, P. G. Johnston, D. P. Harkin, The role of BRCA1 in the cellular response to chemotherapy. J. Natl. Cancer Inst. 96, 1659-1668 (2004).
45. A. R. Mufti, E. Burstein, R. A. Csomos, P. C. Graf, J. C. Wilkinson, R. D. Dick, M. Challa, J. K. Son, S. B. Bratton, G. L. Su, G. J. Brewer, U. Jakob, C. S. Duckett, XIAP is a copper binding protein deregulated in Wilson's disease and other copper toxicosis disorders. Mol. Cell 21, 775-785 (2006).
46. A. K. Freeman, V. Dapic, A. N. Monteiro, Negative regulation of CHK2 activity by protein phosphatase 2A is modulated by DNA damage. Cell Cycle 9, 736-747 (2010).
47. D. D. Sarbassov, D. A. Guertin, S. M. Ali, D. M. Sabatini, Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307, 1098-1101 (2005).
48. D. D. Sarbassov, S. M. Ali, D. H. Kim, D. A. Guertin, R. R. Latek, H. Erdjument-Bromage, P. Tempst, D. M. Sabatini, Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302 (2004).
49. L. R. Pearce, X. Huang, J. Boudeau, R. Pawlowski, S.Wullschleger, M. Deak, A. F. Ibrahim, R. Gourlay, M. A. Magnuson, D. R. Alessi, Identification of Protor as a novel Rictor-binding component of mTOR complex-2. Biochem. J. 405, 513-522 (2007).
50. Y. Ma, C. Hu, A. T. Riegel, S. Fan, E. M. Rosen, Growth factor signaling pathways modulate BRCA1 repression of estrogen receptor-a activity. Mol. Endocrinol. 21, 1905-1923 (2007).
51. T. Xiang, A. Ohashi, Y. Huang, T. K. Pandita, T. Ludwig, S. N. Powell, Q. Yang, Negative regulation of AKT activation by BRCA1. Cancer Res. 68, 10040-10044 (2008).
52. G. E. Tomlinson, T. T. Chen, V. A. Stastny, A. K. Virmani, M. A. Spillman, V. Tonk, J. L. Blum, N. R. Schneider, I. I. Wistuba, J. W. Shay, J. D. Minna, A. F. Gazdar, Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res. 58, 3237-3242 (1998).
53. A. Bensimon, A. Schmidt, Y. Ziv, R. Elkon, S. Y.Wang, D. J. Chen, R. Aebersold, Y. Shiloh, ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci. Signal. 3, rs3 (2010).
54. S. Matsuoka, B. A. Ballif, A. Smogorzewska, E. R. McDonald III, K. E. Hurov, J. Luo, C. E. Bakalarski, Z. Zhao, N. Solimini, Y. Lerenthal, Y. Shiloh, S. P. Gygi, S. J. Elledge, ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007).
55. P. V. Hornbeck, J. M. Kornhauser, S. Tkachev, B. Zhang, E. Skrzypek, B. Murray, V. Latham, M. Sullivan, PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 40, D261-D270 (2012).
56. B. A. Liu, K. Jablonowski, M. Raina, M. Arce, T. Pawson, P. D. Nash, The human and mouse complement of SH2 domain proteins - Establishing the boundaries of phosphotyrosine signaling. Mol. Cell 22, 851-868 (2006).
57. J. W. Yu, M. A. Lemmon, Genome-wide analysis of signaling domain function. Curr. Opin. Chem. Biol. 7, 103-109 (2003).
58. D. Scholtens, M. Vidal, R. Gentleman, Local modeling of global interactome networks. Bioinformatics 21, 3548-3557 (2005).
59. S. J. Boulton, A. Gartner, J. Reboul, P. Vaglio, N. Dyson, D. E. Hill, M. Vidal, Combined functional genomic maps of the C. elegans DNA damage response. Science 295, 127-131 (2002).
60. T. Tatsumoto, X. Xie, R. Blumenthal, I. Okamoto, T. Miki, Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol. 147, 921-928 (1999).
61. M. A. Pujana, J. D. Han, L. M. Starita, K. N. Stevens, M. Tewari, J. S. Ahn, G. Rennert, V. Moreno, T. Kirchhoff, B. Gold, V. Assmann, W. M. Elshamy, J. F. Rual, D. Levine, L. S. Rozek, R. S. Gelman, K. C. Gunsalus, R. A. Greenberg, B. Sobhian, N. Bertin, K. Venkatesan, N. Ayivi-Guedehoussou, X. Solé, P. Hernandez, C. Lazáro, K. L. Nathanson, B. L. Weber, M. E. Cusick, D. E. Hill, K. Offit, D. M. Livingston, S. B. Gruber, J. D. Parvin, M. Vidal, Network modeling links breast cancer susceptibility and centrosome dysfunction. Nat. Genet. 39, 1338-1349 (2007).
62. I. W. Taylor, R. Linding, D. Warde-Farley, Y. Liu, C. Pesquita, D. Faria, S. Bull, T. Pawson, Q. Morris, J. L.Wrana, Dynamic modularity in protein interaction networks predicts breast cancer outcome. Nat. Biotechnol. 27, 199-204 (2009).
63. F. Diella, N. Haslam, C. Chica, A. Budd, S. Michael, N. P. Brown, G. Trave, T. J. Gibson, Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front. Biosci. 13, 6580-6603 (2008).
64. M. B. Yaffe, G. G. Leparc, J. Lai, T. Obata, S. Volinia, L. C. Cantley, A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat. Biotechnol. 19, 348-353 (2001).
65. M. L. Miller, L. J. Jensen, F. Diella, C. Jørgensen, M. Tinti, L. Li, M. Hsiung, S. A. Parker, J. Bordeaux, T. Sicheritz-Ponten, M. Olhovsky, A. Pasculescu, J. Alexander, S. Knapp, N. Blom, P. Bork, S. Li, G. Cesareni, T. Pawson, B. E. Turk, M. B. Yaffe, S. Brunak, R. Linding, Linear motif atlas for phosphorylation-dependent signaling. Sci. Signal. 1, ra2 (2008).
66. M. E. Cusick, N. Klitgord, M. Vidal, D. E. Hill, Interactome: Gateway into systems biology. Hum. Mol. Genet. 14, R171-R181 (2005).
67. A. Ghavidel, G. Cagney, A. Emili, A skeleton of the human protein interactome. Cell 122, 830-832 (2005).
68. J. Lim, T. Hao, C. Shaw, A. J. Patel, G. Szabo, J. F. Rual, C. J. Fisk, N. Li, A. Smolyar, D. E. Hill, A. L. Barabási, M. Vidal, H. Y. Zoghbi, A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration. Cell 125, 801-814 (2006).
69. A. H. Tong, B. Drees, G. Nardelli, G. D. Bader, B. Brannetti, L. Castagnoli, M. Evangelista, S. Ferracuti, B. Nelson, S. Paoluzi, M. Quondam, A. Zucconi, C. W. Hogue, S. Fields, C. Boone, G. Cesareni, A combined experimental and computational strategy to define protein interaction networks for peptide recognition modules. Science 295, 321-324 (2002).
70. M. Carducci, L. Perfetto, L. Briganti, S. Paoluzi, S. Costa, J. Zerweck, M. Schutkowski, L. Castagnoli, G. Cesareni, The protein interaction network mediated by human SH3 domains. Biotechnol. Adv. 30, 4-15 (2012).
71. S. E. Meek, W. S. Lane, H. Piwnica-Worms, Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 279, 32046-32054 (2004).
72. M. Pozuelo Rubio, K. M. Geraghty, B. H. Wong, N. T. Wood, D. G. Campbell, N. Morrice, C. Mackintosh, 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 379, 395-408 (2004).
73. J. Jin, F. D. Smith, C. Stark, C. D. Wells, J. P. Fawcett, S. Kulkarni, P. Metalnikov, P. O'Donnell, P. Taylor, L. Taylor, A. Zougman, J. R. Woodgett, L. K. Langeberg, J. D. Scott, T. Pawson, Proteomic, functional, and domain-based analysis of in vivo 14-3-3 binding proteins involved in cytoskeletal regulation and cellular organization. Curr. Biol. 14, 1436-1450 (2004).
74. D.M. Lowery, K. R. Clauser, M. Hjerrild, D. Lim, J. Alexander, K. Kishi, S. E. Ong, S. Gammeltoft, S. A. Carr, M. B. Yaffe, Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. EMBO J. 26, 2262-2273 (2007).
75. M. Boxem, Z. Maliga, N. Klitgord, N. Li, I. Lemmens, M. Mana, L. de Lichtervelde, J. D. Mul, D. van de Peut, M. Devos, N. Simonis, M. A. Yildirim, M. Cokol, H. L. Kao, A. S. de Smet, H.Wang, A. L. Schlaitz, T. Hao, S. Milstein, C. Fan, M. Tipsword, K. Drew, M. Galli, K. Rhrissorrakrai, D. Drechsel, D. Koller, F. P. Roth, L. M. Iakoucheva, A. K. Dunker, R. Bonneau, K. C. Gunsalus, D. E. Hill, F. Piano, J. Tavernier, S. van den Heuvel, A. A. Hyman, M. Vidal, A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134, 534-545 (2008).
76. R. D. Finn, J. Mistry, J. Tate, P. Coggill, A. Heger, J. E. Pollington, O. L. Gavin, P. Gunasekaran, G. Ceric, K. Forslund, L. Holm, E. L. Sonnhammer, S. R. Eddy, A. Bateman, The Pfam protein families database. Nucleic Acids Res. 38, D211-D222 (2010).
77. P. R. Sibbald, P. Argos, Weighting aligned protein or nucleic acid sequences to correct for unequal representation. J. Mol. Biol. 216, 813-818 (1990).
78. K. Yamane, E. Katayama, K. Sugasawa, T. Tsuruo, Retinoblastoma susceptibility protein, Rb, possesses multiple BRCT-Ws, BRCA1 carboxyl-terminus-related W regions with DNA break-binding activity. Oncogene 19, 1982-1991 (2000).
79. K. D. Pruitt, T. Tatusova, D. R. Maglott, NCBI reference sequences (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35, D61-D65 (2007).
80. S. Veerassamy, A. Smith, E. R. Tillier, A transition probability model for amino acid substitutions from blocks. J. Comput. Biol. 10, 997-1010 (2003).
81. M. E. Cusick, H. Yu, A. Smolyar, K. Venkatesan, A. R. Carvunis, N. Simonis, J. F. Rual, H. Borick, P. Braun, M. Dreze, J. Vandenhaute, M. Galli, J. Yazaki, D. E. Hill, J. R. Ecker, F. P. Roth, M. Vidal, Literature-curated protein interaction datasets. Nat. Methods 6, 39-46 (2009).
82. P. Shannon, A. Markiel, O. Ozier, N. S. Baliga, J. T. Wang, D. Ramage, N. Amin, B. Schwikowski, T. Ideker, Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003).
83. M. Stucki, J. A. Clapperton, D. Mohammad, M. B. Yaffe, S. J. Smerdon, S. P. Jackson, MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226 (2005).
84. C. Xu, L. Wu, G. Cui, M. V. Botuyan, J. Chen, G. Mer, Structure of a second BRCT domain identified in the Nijmegen breakage syndrome protein Nbs1 and its function in an MDC1-dependent localization of Nbs1 to DNA damage sites. J. Mol. Biol. 381, 361-372 (2008).
85. P. James, J. Halladay, E. A. Craig, Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436 (1996).
86. J. Debnath, S. K. Muthuswamy, J. S. Brugge, Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268 (2003).
87. D. D. Sarbassov, S. M. Ali, S. Sengupta, J. H. Sheen, P. P. Hsu, A. F. Bagley, A. L.Markhard, D. M. Sabatini, Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168 (2006).
88. G. Caraux, S. Pinloche, PermutMatrix: A graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21, 1280-1281 (2005).
89. G. Rigaut, A. Shevchenko, B. Rutz, M. Wilm, M. Mann, B. Séraphin, A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17, 1030-1032 (1999).
90. D. N. Perkins, D. J. Pappin, D. M. Creasy, J. S. Cottrell, Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 (1999).
91. A. Keller, A. I. Nesvizhskii, E. Kolker, R. Aebersold, Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (2002).
92. A. I. Nesvizhskii, A. Keller, E. Kolker, R. Aebersold, A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (2003).
93. G. Manning, D. B. Whyte, R. Martinez, T. Hunter, S. Sudarsanam, The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).