Elucidating human phosphatase-substrate networks

Science Signaling

Volumn 6, Issue 275, 2013, Pages

  Li, Xun ^a,b   Wilmanns, Matthias ^c   Thornton, Janet ^b   Köhn, Maja ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ACID PHOSPHATASE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ACIREDUCTONE SYNTHASE; ALKALINE PHOSPHATASE; EPOXIDE HYDROLASE; GLUCOSE 6 PHOSPHATASE; INOSITOL 3,4 BISPHOSPHATE 4 PHOSPHATASE; INOSITOL PHOSPHATE PHOSPHATASE; JANUS KINASE; PHOSPHATASE; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4 BIPHOSPHATE 4 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRIPHOSPHATE 3 PHOSPHATASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCOLATE PHOSPHATASE; PHOSPHOMANNOMUTASE; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORIC MONOESTER HYDROLASE; POLYNUCLEOTIDE 3' PHOSPHATASE; POLYNUCLEOTIDE 5' HYDROXYL KINASE; POLYNUCLEOTIDE 5' PHOSPHATASE; PYRIDOXAL PHOSPHATASE; PYRIMIDINE 5' NUCLEOTIDE NUCLEOSIDASE; SYNAPTOJANIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; DATA BASE; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

DATABASES, PROTEIN; HUMANS; MODELS, BIOLOGICAL; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; SEQUENCE ANALYSIS, PROTEIN; SYSTEMS BIOLOGY;

EID: 84877992759     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003203     Document Type: Article

References (93)

1. T. Hunter, Signaling - 2000 and beyond. Cell 100, 113-127 (2000).
2. K. Tonks, Protein tyrosine phosphatases: From genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 7, 833-846 (2006).
3. D. L. Brautigan, Protein Ser/Thr phosphatases - The ugly ducklings of cell signaling. FEBS J. 280, 324-345 (2013).
4. A. Alonso, J. Sasin, N. Bottini, I. Friedberg, A. Osterman, A. Godzik, T. Hunter, J. Dixon, T. Mustelin, Protein tyrosine phosphatases in the human genome. Cell 117, 699-711 (2004).
5. Y. Shi, Serine/threonine phosphatases: Mechanism through structure. Cell 139, 468-484 (2009).
6. D. M. Virshup, S. Shenolikar, From promiscuity to precision: Protein phosphatases get a makeover. Mol. Cell 33, 537-545 (2009).
7. A. Seifried, J. Schultz, A. Gohla, Human HAD phosphatases: Structure, mechanism and roles in health and disease. FEBS J. 280, 549-571 (2013).
8. M. Magrane; Uniprot Consortium, UniProt Knowledgebase: A hub of integrated protein data. Database 2011, bar009 (2011).
9. G. Lu, Y. Wang, Functional diversity of mammalian type 2C protein phosphatase isoforms: New tales from an old family. Clin. Exp. Pharmacol. Physiol. 35, 107-112 (2008).
10. P. T. Cohen, in Protein Phosphatases, J. Arino, Ed. (Springer, Berlin, 2004), pp. 1-20.
11. G. B. Moorhead, V. De Wever, G. Templeton, D. Kerk, Evolution of protein phosphatases in plants and animals. Biochem. J. 417, 401-409 (2009).
12. Y. Zhang, Y. Kim, N. Genoud, J. Gao, J. W. Kelly, S. L. Pfaff, G. N. Gill, J. E. Dixon, J. P. Noel, Determinants for dephosphorylation of the RNA polymerase II C-terminal domain by Scp1. Mol. Cell 24, 759-770 (2006).
13. F. Sacco, L. Perfetto, L. Castagnoli, G. Cesareni, The human phosphatase interactome: An intricate family portrait. FEBS Lett. 586, 2732-2739 (2012).
14. S. Liberti, F. Sacco, A. Calderone, L. Perfetto, M. Iannuccelli, S. Panni, E. Santonico, A. Palma, A. P. Nardozza, L. Castagnoli, G. Cesareni, HuPho: The human phosphatase portal. FEBS J. 280, 379-387 (2013).
15. Z. D. Zhang, A. Frankish, T. Hunt, J. Harrow, M. Gerstein, Identification and analysis of unitary pseudogenes: Historic and contemporary gene losses in humans and other primates. Genome Biol. 11, R26 (2010).
16. L. Cui, W. P. Yu, H. J. DeAizpurua, R. S. Schmidli, C. J. Pallen, Cloning and characterization of islet cell antigen-related protein-tyrosine phosphatase (PTP), a novel receptor-like PTP and autoantigen in insulin-dependent diabetes. J. Biol. Chem. 271, 24817-24823 (1996).
17. D. Blero, B. Payrastre, S. Schurmans, C. Erneux, Phosphoinositide phosphatases in a network of signalling reactions. Pflugers Arch. 455, 31-44 (2007).
18. M. Ooms, K. A. Horan, P. Rahman, G. Seaton, R. Gurung, D. S. Kethesparan, C. A. Mitchell, The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem. J. 419, 29-49 (2009).
19. P. J. Stankiewicz, M. J. Gresser, A. S. Tracey, L. F. Hass, 2,3-Diphosphoglycerate phosphatase activity of phosphoglycerate mutase: Stimulation by vanadate and phosphate. Biochemistry 26, 1264-1269 (1987).
20. X. Tan, D. R. Stover, K. A. Walsh, Demonstration of protein tyrosine phosphatase activity in the second of two homologous domains of CD45. J. Biol. Chem. 268, 6835-6838 (1993).
21. K. L. Lim, P. R. Kolatkar, K. P. Ng, C. H. Ng, C. J. Pallen, Interconversion of the kinetic identities of the tandem catalytic domains of receptor-like protein-tyrosine phosphatase PTPa by two point mutations is synergistic and substrate-dependent. J. Biol. Chem. 273, 28986-28993 (1998).
22. M. Knudsen, C. Wiuf, The CATH database. Hum. Genomics 4, 207-212 (2010).
23. J. D. Bjorge, A. Pang, D. J. Fujita, Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J. Biol. Chem. 275, 41439-41446 (2000).
24. G. Lin, V. Aranda, S. K. Muthuswamy, N. K. Tonks, Identification of PTPN23 as a novel regulator of cell invasion in mammary epithelial cells from a loss-of-function screen of the 'PTP-ome'. Genes Dev. 25, 1412-1425 (2011).
25. C. van Vliet, P. E. Bukczynska, M. A. Puryer, C. M. Sadek, B. J. Shields, M. L. Tremblay, T. Tiganis, Selective regulation of tumor necrosis factor-induced Erk signaling by Src family kinases and the T cell protein tyrosine phosphatase. Nat. Immunol. 6, 253-260 (2005).
26. P. Rios, X. Li, M. Köhn, Molecular mechanisms of the PRL phosphatases. FEBS J. 280, 505-524 (2013).
27. F. L. Robinson, J. E. Dixon, Myotubularin phosphatases: Policing 3-phosphoinositides. Trends Cell Biol. 16, 403-412 (2006).
28. V. McParland, G. Varsano, X. Li, J. Thornton, J. Baby, A. Aravind, C. Meyer, K. Pavic, P. Rios, M. Köhn, The metastasis-promoting phosphatase PRL-3 shows activity toward phosphoinositides. Biochemistry 50, 7579-7590 (2011).
29. K. Takeda, Y. Komuro, T. Hayakawa, H. Oguchi, Y. Ishida, S. Murakami, T. Noguchi, H. Kinoshita, Y. Sekine, S. Iemura, T. Natsume, H. Ichijo, Mitochondrial phosphoglycerate mutase 5 uses alternate catalytic activity as a protein serine/threonine phosphatase to activate ASK1. Proc. Natl. Acad. Sci. U.S.A. 106, 12301-12305 (2009).
30. T. S. K. Prasad, R. Goel, K. Kandasamy, S. Keerthikumar, S. Kumar, S. Mathivanan, D. Telikicherla, R. Raju, B. Shafreen, A. Venugopal, L. Balakrishnan, A. Marimuthu, S. Banerjee, D. S. Somanathan, A. Sebastian, S. Rani, S. Ray, C. J. Harrys Kishore, S. Kanth, M. Ahmed, M. K. Kashyap, R. Mohmood, Y. L. Ramachandra, V. Krishna, B. A. Rahiman, S. Mohan, P. Ranganathan, S. Ramabadran, R. Chaerkady, A. Pandey, Human Protein Reference Database - 2009 update. Nucleic Acids Res. 37, D767-D772 (2009).
31. B. Aranda, H. Blankenburg, S. Kerrien, F. S. L. Brinkman, A. Ceol, E. Chautard, J. M. Dana, J. De Las Rivas, M. Dumousseau, E. Galeota, A. Gaulton, J. Goll, R. E. W. Hancock, R. Isserlin, R. C. Jimenez, J. Kerssemakers, J. Khadake, D. J. Lynn, M. Michaut, G. O'Kelly, K. Ono, S. Orchard, C. Prieto, S. Razick, O. Rigina, L. Salwinski, M. Simonovic, S. Velankar, A. Winter, G. M. Wu, G. D. Bader, G. Cesareni, I. M. Donaldson, D. Eisenberg, G. J. Kleywegt, J. Overington, S. Ricard-Blum, M. Tyers, M. Albrecht, H. Hermjakob, PSICQUIC and PSISCORE: Accessing and scoring molecular interactions. Nat. Methods 8, 528-529 (2011).
32. S. Rastogi, B. Rost, LocDB: Experimental annotations of localization for Homo sapiens and Arabidopsis thaliana. Nucleic Acids Res. 39, D230-D234 (2011).
33. C. Y. Yang, C. H. Chang, Y. L. Yu, T. C. Lin, S. A. Lee, C. C. Yen, J. M. Yang, J. M. Lai, Y. R. Hong, T. L. Tseng, K. M. Chao, C. Y. Huang, PhosphoPOINT: A comprehensive human kinase interactome and phospho-protein database. Bioinformatics 24, i14-i20 (2008).
34. A. I. Su, T. Wiltshire, S. Batalov, H. Lapp, K. A. Ching, D. Block, J. Zhang, R. Soden, M. Hayakawa, G. Kreiman, M. P. Cooke, J. R. Walker, J. B. Hogenesch, A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A. 101, 6062-6067 (2004).
35. C. H. Gray, V. M. Good, N. K. Tonks, D. Barford, The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase. EMBO J. 22, 3524-3535 (2003).
36. B. M. Ham, H. Jayachandran, F. Yang, N. Jaitly, A. D. Polpitiya, M. E. Monroe, L. Wang, R. Zhao, S. O. Purvine, E. A. Livesay, D. G. Camp II, S. Rossie, R. D. Smith, Novel Ser/Thr protein phosphatase 5 (PP5) regulated targets during DNA damage identified by proteomics analysis. J. Proteome Res. 9, 945-953 (2010).
37. L. Ulloa, V. Dombradi, J. Díaz-Nido, K. Szücs, P. Gergely, P. Friedrich, J. Avila, Dephosphorylation of distinct sites on microtubule-associated protein MAP1B by protein phosphatases 1, 2A and 2B. FEBS Lett. 330, 85-89 (1993).
38. S. De Munter, M. Köhn, M. Bollen, Challenges and opportunities in the development of protein phosphatase-directed therapeutics. ACS Chem. Biol. 8, 36-45 (2013).
39. Z. Jia, D. Barford, A. J. Flint, N. K. Tonks, Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268, 1754-1758 (1995).
40. A. Schumacher, J. L. Todd, A. E. Rice, K. G. Tanner, J. M. Denu, Structural basis for the recognition of a bisphosphorylated MAP kinase peptide by human VHR protein phosphatase. Biochemistry 41, 3009-3017 (2002).
41. S. Hunter, R. Apweiler, T. K. Attwood, A. Bairoch, A. Bateman, D. Binns, P. Bork, U. Das, L. Daugherty, L. Duquenne, R. D. Finn, J. Gough, D. Haft, N. Hulo, D. Kahn, E. Kelly, A. Laugraud, I. Letunic, D. Lonsdale, R. Lopez, M. Madera, J. Maslen, C. McAnulla, J. McDowall, J. Mistry, A. Mitchell, N. Mulder, D. Natale, C. Orengo, A. F. Quinn, J. D. Selengut, C. J. Sigrist, M. Thimma, P. D. Thomas, F. Valentin, D. Wilson, C. H. Wu, C. Yeats, InterPro: The integrative protein signature database. Nucleic Acids Res. 37, D211-D215 (2009).
42. Y. Kim, Y. I. Lee, M. Seo, S. Y. Kim, J. E. Lee, H. D. Youn, Y. S. Kim, Y. S. Juhnn, Calcineurin dephosphorylates glycogen synthase kinase-3 beta at serine-9 in neuroblast-derived cells. J. Neurochem. 111, 344-354 (2009).
43. A. Cegielska, K. F. Gietzen, A. Rivers, D. M. Virshup, Autoinhibition of casein kinase Iε (CKIε) is relieved by protein phosphatases and limited proteolysis. J. Biol. Chem. 273, 1357-1364 (1998).
44. F. Diella, C. M. Gould, C. Chica, A. Via, T. J. Gibson, Phospho.ELM: A database of phosphorylation sites - Update 2008. Nucleic Acids Res. 36, D240-D244 (2008).
45. P. V. Hornbeck, I. Chabra, J. M. Kornhauser, E. Skrzypek, B. Zhang, PhosphoSite: A bioinformatics resource dedicated to physiological protein phosphorylation. Proteomics 4, 1551-1561 (2004).
46. F. Uhlmann, C. Bouchoux, S. López-Avilés, A quantitative model for cyclin-dependent kinase control of the cell cycle: Revisited. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 3572-3583 (2011).
47. A. Moccario, E. Schiebel, Cdc14: A highly conserved family of phosphatases with non-conserved functions? J. Cell Sci. 123, 2867-2876 (2010).
48. 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).
49. R. Linding, L. J. Jensen, G. J. Ostheimer, M. A. van Vugt, C. Jørgensen, I. M. Miron, F. Diella, K. Colwill, L. Taylor, K. Elder, P. Metalnikov, V. Nguyen, A. Pasculescu, J. Jin, J. G. Park, L. D. Samson, J. R. Woodgett, R. B. Russell, P. Bork, M. B. Yaffe, T. Pawson, Systematic discovery of in vivo phosphorylation networks. Cell 129, 1415-1426 (2007).
50. M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, M. Tanabe, KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114 (2012).
51. C. F. Schaefer, K. Anthony, S. Krupa, J. Buchoff, M. Day, T. Hannay, K. H. Buetow, PID: The Pathway Interaction Database. Nucleic Acids Res. 37, D674-D679 (2009).
52. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, D. J. Lipman, Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
53. C. Meyer, M. Köhn, Efficient scaled-up synthesis of N-a-Fmoc-4-phosphono(difluoromethyl)-L-phenylalanine and its incorporation into peptides. Synthesis 20, 3255-3260 (2011).
54. T. C. Meng, M. F. Lin, Tyrosine phosphorylation of c-ErbB-2 is regulated by the cellular form of prostatic acid phosphatase in human prostate cancer cells. J. Biol. Chem. 273, 22096-22104 (1998).
55. M. Tanaka, Y. Kishi, Y. Takanezawa, Y. Kakehi, J. Aoki, H. Arai, Prostatic acid phosphatase degrades lysophosphatidic acid in seminal plasma. FEBS Lett. 571, 197-204 (2004).
56. R. Zhao, Y. Qi, J. Chen, Z. J. Zhao, FYVE-DSP2, a FYVE domain-containing dual specificity protein phosphatase that dephosphorylates phosphotidylinositol 3-phosphate. Exp. Cell Res. 265, 329-338 (2001).
57. J. Yu, L. Pan, X. Qin, H. Chen, Y. Xu, Y. Chen, H. Tang, MTMR4 attenuates transforming growth factor b (TGFb) signaling by dephosphorylating R-Smads in endosomes. J. Biol. Chem. 285, 8454-8462 (2010).
58. M. S. Songs, L. Salmena, P. P. Pandolfi, The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 13, 283-296 (2012).
59. M. Wang, C. J. Fiol, A. A. DePaoli-Roach, P. J. Roach, Glycogen synthase kinase-3β is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J. Biol. Chem. 269, 14566-14574 (1994).
60. Y. Wang, Y. Liu, C. Wu, H. Zhang, X. Zheng, Z. Zheng, T. L. Geiger, G. J. Nuovo, P. Zheng, Epm2a suppresses tumor growth in an immunocompromised host by inhibiting Wnt signaling. Cancer Cell 10, 179-190 (2006).
61. D. R. Alessi, N. Gomez, G. Moorhead, T. Lewis, S. M. Keyse, P. Cohen, Inactivation of p42 MAP kinase by protein phosphatase 2A and a protein tyrosine phosphatase, but not CL100, in various cell lines. Curr. Biol. 5, 283-295 (1995).
62. N. G. Anderson, J. L. Maller, N. K. Tonks, T. W. Sturgill, Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature 343, 651-653 (1990).
63. S. M. Pettiford, R. Herbst, The MAP-kinase ERK2 is a specific substrate of the protein tyrosine phosphatase HePTP. Oncogene 19, 858-869 (2000).
64. F. Sacco, M. Tinti, A. Palma, E. Ferrari, A. P. Nardozza, R. Hooft van Huijsduijnen, T. Takahashi, L. Castagnoli, G. Cesareni, Tumor suppressor density-enhanced phosphatase-1 (DEP-1) inhibits the RAS pathway by direct dephosphorylation of ERK1/2 kinases. J. Biol. Chem. 284, 22048-22058 (2009).
65. K. L. Guan, E. Butch, Isolation and characterization of a novel dual specific phosphatase, HVH2, which selectively dephosphorylates the mitogen-activated protein kinase. J. Biol. Chem. 270, 7197-7203 (1995).
66. H. Sun, C. H. Charles, L. F. Lau, N. K. Tonks, MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75, 487-493 (1993).
67. V. Esteban, M. D. Vázquez-Novelle, E. Calvo, A. Bueno, M. P. Sacristán, Human Cdc14A reverses CDK1 phosphorylation of Cdc25A on serines 115 and 320. Cell Cycle 5, 2894-2898 (2006).
68. 2/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J. 21, 5911-5920 (2002).
69. M. D. Vázquez-Novelle, N. Mailand, S. Ovejero, A. Bueno, M. P. Sacristán, Human Cdc14A phosphatase modulates the G2/M transition through Cdc25A and Cdc25B. J. Biol. Chem. 285, 40544-40553 (2010).
70. C. Lammer, S. Wagerer, R. Saffrich, D. Mertens, W. Ansorge, I. Hoffmann, The Cdc25B phosphatase is essential for the G2/M phase transition in human cells. J. Cell Sci. 111, 2445-2453 (1998).
71. F. Dessauge, X. Cayla, J P. Albar, A. Fleischer, A. Ghadiri, M. Duhamel, A. Rebollo, Identification of PP1α as a caspase-9 regulator in IL-2 deprivation-induced apoptosis. J. Immunol. 177, 2441-2451 (2006).
72. L. A. Allan, P. R. Clarke, Phosphorylation of caspase-9 by CDK1/cyclin B1 protects mitotic cells against apoptosis. Mol. Cell 26, 301-310 (2007).
73. J. Q. Wu, J. Y. Guo, W. Tang, C. S. Yang, C. D. Freel, C. Chen, A. C. Nairn, S. Kornbluth, PP1-mediated dephosphorylation of phosphoproteins at mitotic exit is controlled by inhibitor-1 and PP1 phosphorylation. Nat. Cell Biol. 11, 644-651 (2009).
74. M. A. Lawlor, D. R. Alessi, PKB/Akt: A key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114, 2903-2910 (2001).
75. W. Xu, X. Yuan, Y. J. Jung, Y. Yang, A. Basso, N. Rosen, E. J. Chung, J. Trepel, L. Neckers, The heat shock protein 90 inhibitor geldanamycin and the ErbB inhibitor ZD1839 promote rapid PP1 phosphatase-dependent inactivation of AKT in ErbB2 overexpressing breast cancer cells. Cancer Res. 63, 7777-7784 (2003).
76. T. Obata, M. B. Yaffe, G. G. Leparc, E. T. Piro, H. Maegawa, A. Kashiwagi, R. Kikkawa, L. C. Cantley, Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J Biol. Chem. 275, 36108-36115 (2000).
77. M. H. Cardone, N. Roy, H. R. Stennicke, G. S. Salvesen, T. F. Franke, E. Stanbridge, S. Frisch, J. C. Reed, Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321 (1998).
78. C. Asencio, I. F. Davidson, R. Santarella-Mellwig, T. B. Ly-Hartig, M. Mall, M. R. Wallenfang, I. W. Mattaj, M. Gorjánácz, Coordination of kinase and phosphatase activities by Lem4 enables nuclear envelope reassembly during mitosis. Cell 150, 122-135 (2012).
79. P. Flicek, M. R. Amode, D. Barrell, K. Beal, S. Brent, D. Carvalho-Silva, P. Clapham, G. Coates, S. Fairley, S. Fitzgerald, L. Gil, L. Gordon, M. Hendrix, T. Hourlier, N. Johnson, A. K. Kähäri, D. Keefe, S. Keenan, R. Kinsella, M. Komorowska, G. Koscielny, E. Kulesha, P. Larsson, I. Longden, W. McLaren, M. Muffato, B. Overduin, M. Pignatelli, B. Pritchard, H. S. Riat, G. R. Ritchie, M. Ruffier, M. Schuster, D. Sobral, Y. A. Tang, K. Taylor, S. Trevanion, J. Vandrovcova, S. White, M. Wilson, S. P. Wilder, B. L. Aken, E. Birney, F. Cunningham, I. Dunham, R. Durbin, X. M. Fernández-Suarez, J. Harrow, J. Herrero, T. J. Hubbard, A. Parker, G. Proctor, G. Spudich, J. Vogel, A. Yates, A. Zadissa, S. M. Searle, Ensembl 2012. Nucleic Acids Res. 40, D84-D90 (2012).
80. 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).
81. 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).
82. J. M. Wilkes, C. Doerig, The protein-phosphatome of the human malaria parasite Plasmodium falciparum. BMC Genomics 9, 412 (2008).
83. H. H. Chen, R. Luche, B. Wei, N. K. Tonks, Characterization of two distinct dual specificity phosphatases encoded in alternative open reading frames of a single gene located on human chromosome 10q22.2. J. Biol. Chem. 279, 41404-41413 (2004).
84. C. T. Porter, G. J. Bartlett, J. M. Thornton, The Catalytic Site Atlas: A resource of catalytic sites and residues identified in enzymes using structural data. Nucleic Acids Res. 32, D129-D133 (2004).
85. I. Letunic, T. Doerks, P. Bork, SMART 7: Recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302-D305 (2012).
86. C. J. Sigrist, L. Cerutti, E. de Castro, P. S. Langendijk-Genevaux, V. Bulliard, A. Bairoch, N. Hulo, PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res. 38, D161-D166 (2010).
87. P. Rice, I. Longden, A. Bleasby, EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet. 16, 276-277 (2000).
88. P. Di Tommaso, S. Moretti, I. Xenarios, M. Orobitg, A. Montanyola, J. M. Chang, J. F. Taly, C. Notredame, T-Coffee: A web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13-W17 (2011).
89. H. M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, P. E. Bourne, The Protein Data Bank. Nucleic Acids Res. 28, 235-242 (2000).
90. J. D. Retief, Phylogenetic analysis using PHYLIP. Methods Mol. Biol. 132, 243-258 (2000).
91. C. Wu, C. Orozco, J. Boyer, M. Leglise, J. Goodale, S. Batalov, C. L. Hodge, J. Haase, J. Janes, J. W. Huss III, A. I. Su, BioGPS: An extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130 (2009).
92. E. Smoot, K. Ono, J. Ruscheinski, P. L. Wang, T. Ideker, Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27, 431-432 (2011).
93. G. E. Crooks, G. Hon, J. M. Chandonia, S. E. Brenner, WebLogo: A sequence logo generator. Genome Res. 14, 1188-1190 (2004).