Structural and functional characterization of a novel phosphatase from the Arabidopsis thaliana gene locus At1g05000

Proteins: Structure, Function and Genetics

Volumn 73, Issue 1, 2008, Pages 241-253

  Aceti, David J ^a   Bitto, Eduard ^a   Yakunin, Alexander F ^b   Proudfoot, Michael ^b   Bingman, Craig A ^a   Frederick, Ronnie O ^a   Sreenath, Hassan K ^a   Vojtik, Frank C ^a   Wrobel, Russell L ^a   Fox, Brian G ^a   Markley, John L ^a   Phillips Jr , George N ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Arabidopsis; At1g05000; Crystallography; Phosphatase; Polyphosphate; Structure

Indexed keywords

PHOSPHATASE; POLYPHOSPHATE;

ARABIDOPSIS; ARTICLE; CRYSTAL STRUCTURE; DIFFRACTION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; GENE LOCUS; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CATALYTIC DOMAIN; CLONING, MOLECULAR; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORIC MONOESTER HYDROLASES; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 50849111782     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22041     Document Type: Article

References (59)

1. Alonso A, Sasin J, Bottini N, Friedberg I, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T. Protein tyrosine phosphatases in the human genome. Cell 2004;117:699-711.
2. Mustelin T, Abraham RT, Rudd CE, Alonso A, Merlo JJ. Protein tyrosine phosphorylation in T cell signaling. Front Biosci 2002;7: d918-d969.
3. Mustelin T, Tasken K. Positive and negative regulation of T-cell activation through kinases and phosphatases. Biochem J 2003;371 (Part 1):15-27.
4. Luan S. Protein phosphatases in plants. Annu Rev Plant Biol 2003;54: 63-92.
5. Zhou G, Denu JM, Wu L, Dixon JE. The catalytic role of Cys124 in the dual specificity phosphatase VHR. J Biol Chem 1994;269: 28084-28090.
6. Guan KL, Dixon JE. Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate. J Biol Chem 1991;266:17026-17030.
7. Sun JP, Wang WQ, Yang H, Liu S, Liang F, Fedorov AA, Almo SC, Zhang ZY. Structure and biochemical properties of PRL-1, a phosphatase implicated in cell growth, differentiation, and tumor invasion. Biochemistry 2005;44:12009-12021.
8. Song H, Hanlon N, Brown NR, Noble ME, Johnson LN, Barford D. Phosphoprotein-protein interactions revealed by the crystal structure of kinase-associated phosphatase in complex with phosphoCDK2. Mol Cell 2001;7:615-626.
9. Diamond RH, Cressman DE, Laz TM, Abrams CS, Taub R. PRL-1, a unique nuclear protein tyrosine phosphatase, affects cell growth. Mol Cell Biol 1994;14:3752-3762.
10. Changela A, Ho CK, Martins A, Shuman S, Mondragon A. Structure and mechanism of the RNA triphosphatase component of mammalian mRNA capping enzyme. Embo J 2001;20:2575-2586.
11. Martins A, Shuman S. Mutational analysis of baculovirus phosphatase identifies structural residues important for triphosphatase activity in vitro and in vivo. Biochemistry 2002;41:13403-13409.
12. Changela A, Martins A, Shuman S, Mondragon A. Crystal structure of baculovirus RNA triphosphatase complexed with phosphate. J Biol Chem 2005;280:17848-17856.
13. Lee JO, Yang H, Georgescu MM, Di Cristofano A, Maehama T, Shi Y, Dixon JE, Pandolfi P, Pavletich NP. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999;99:323-334.
14. Martins A, Shuman S. The domain order of mammalian capping enzyme can be inverted and baculovirus phosphatase can function in cap formation in vivo. Virology 2002;304:167-175.
15. Worby CA, Gentry MS, Dixon JE. Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 2006;281:30412-30418.
16. Gentry MS, Dowen RH, 3rd, Worby CA, Mattoo S, Ecker JR, Dixon JE. The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J Cell Biol 2007; 178:477-488.
17. Thao S, Zhao Q, Kimball T, Steffen E, Blommel PG, Riters M, Newman CS, Fox BG, Wrobel RL. Results from high-throughput DNA cloning of Arabidopsis thaliana target genes using site-specific recombination. J Struct Funct Genomics 2004;5:267-276.
18. Sreenath HK, Bingman CA, Buchan BW, Seder KD, Burns BT, Geetha HV, Jeon WB, Vojtik FC, Aceti DJ, Frederick RO, Phillips GN, Jr. Fox BG. Protocols for production of selenomethionine-labeled proteins in 2-L polyethylene terephthalate bottles using auto-induction medium. Protein Expr Purif 2005;40:256-267.
19. Jeon WB, Aceti DJ, Bingman CA, Vojtik FC, Olson AC, Ellefson JM, McCombs JE, Sreenath HK, Blommel PG, Seder KD, Burns BT, Geetha HV, Harms AC, Sabat G, Sussman MR, Fox BG, Phillips GN, Jr. High-throughput purification and quality assurance of Arabidopsis thaliana proteins for eukaryotic structural genomics. J Struct Funct Genomics 2005;6:143-147.
20. Zolnai Z, Lee PT, Li J, Chapman MR, Newman CS, Phillips GN, Jr, Rayment I, Ulrich EL, Volkman BF, Markley JL. Project management system for structural and functional proteomics: sesame. J Struct Funct Genomics 2003;4:11-23.
21. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol 1997;276:307-326.
22. Grosse-Kunstleve RW, Adams PD. Substructure search procedures for macromolecular structures. Acta Crystallogr D Biol Crystallogr 2003;59 (Part 11):1966-1973.
23. Cowtan K, Main P. Miscellaneous algorithms for density modification. Acta Crystallogr D Biol Crystallogr 1998;54 (Part 4):487-493.
24. Terwilliger TC. Maximum-likelihood density modification. Acta Crystallogr D Biol Crystallogr 2000;56 (Part 8):965-972.
25. McRee DE. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 1999;125: 156-165.
26. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 1998;54 (Part 5):905-921.
27. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-291.
28. Lovell SC, Davis IW, Arendall WB III, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003;50: 437-450.
29. Kuznetsova E, Proudfoot M, Sanders SA, Reinking J, Savchenko A, Arrowsmith CH, Edwards AM, Yakunin AF. Enzyme genomics: application of general enzymatic screens to discover new enzymes. FEMS Microbiol Rev 2005;29:263-279.
30. Baykov AA, Evtushenko OA, Avaeva SM. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Anal Biochem 1988;171: 266-270.
31. Saheki S, Takeda A, Shimazu T. Assay of inorganic phosphate in the mild pH range, suitable for measurement of glycogen phosphorylase activity. Anal Biochem 1985;148:277-281.
32. Heering HA, Weiner JH, Armstrong FA. J Am Chem Soc 1997;119: 11628-11638.
33. Pearl FM, Bennett CF, Bray JE, Harrison AP, Martin N, Shepherd A, Sillitoe I, Thornton J, Orengo CA. The CATH database: an extended protein family resource for structural and functional genomics. Nucleic Acids Res 2003;31:452-455.
34. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242.
35. Madej T, Gibrat JF, Bryant SH. Threading a database of piotein cores. Proteins 1995;23:356-369.
36. Begley MJ, Taylor GS, Brock MA, Ghosh P, Woods VL, Dixon JE. Molecular basis for substrate recognition by MTMR2, a myotubularin family phosphoinositide phosphatase. Proc Natl Acad Sci U S A 2006;103:927-932.
37. Marchler-Bauer A, Panchenko AR, Shoemaker BA, Thiessen PA, Geer LY, Bryant SH. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res 2002;30:281-283.
38. Yuvaniyama J, Denu JM, Dixon JE, Saper MA. Crystal structure of the dual specificity protein phosphatase VHR. Science 1996;272: 1328-1331.
39. Chu HM, Guo RT, Lin TW, Chou CC, Shr HL, Lai HL, Tang TY, Cheng KJ, Selinger BL, Wang AH. Structures of Selenomonas ruminantium phytase in complex with persulfated phytate: DSP phytase fold and mechanism for sequential substrate hydrolysis. Structure 2004;12:2015-2024.
40. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 1988;16:10881-10890.
41. Deshpande T, Takagi T, Hao L, Buratowski S, Charbonneau H. Human PIR1 of the protein-tyrosine phosphatase superfamily has RNA 5′-triphosphatase and diphosphatase activities. J Biol Chem 1999;274:16590-16594.
42. Care A, Vousden KA, Binley KM, Radcliffe P, Trevethick J, Mannazzu I, Sudbery PE. A synthetic lethal screen identifies a role for the cortical actin patch/endocytosis complex in the response to nutrient deprivation in Saccharomyces cerevisiae. Genetics 2004;166: 707-719.
43. Zhang ZY, Dixon JE. Active site labeling of the Yersinia protein tyrosine phosphatase: the determination of the pKa of the active site cysteine and the function of the conserved histidine 402. Biochemistry 1993;32:9340-9345.
44. Denu JM, Dixon JE. A catalytic mechanism for the dual-specific phosphatases. Proc Natl Acad Sci U S A 1995;92:5910-5914.
45. Daum G, Solca F, Diltz CD, Zhao Z, Cool DE, Fischer EH. A general peptide substrate for protein tyrosine phosphatases. Anal Biochem 1993;211:50-54.
46. Harder KW, Owen P, Wong LK, Aebersold R, Clark-Lewis I, Jirik FR. Characterization and kinetic analysis of the intracellular domain of human protein tyrosine phosphatase beta (HPTP beta) using synthetic phosphopeptides. Biochem J 1994;298 (Part 2):395-401.
47. Zhang ZY, Maclean D, Thieme-Sefler AM, Roeske RW, Dixon JE. A continuous spectrophotometric and fluorimetric assay for protein tyrosine phosphatase using phosphotyrosine-containing peptides. Anal Biochem 1993;211:7-15.
48. Agazie YM, Hayman MJ. Development of an efficient "substrate- trapping" mutant of Src homology phosphotyrosine phosphatase 2 and identification of the epidermal growth factor receptor. Gab1, and three other proteins as target substrates. J Biol Chem 2003; 278:13952-13958.
49. Kerk D, Bulgrien J, Smith DW, Barsam B, Veretnik S, Gribskov M. The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol 2002;129:908-925.
50. Gray CH, Good VM, Tonks NK, Barford D. The structure of the cell cycle protein Cdc14 reveals a proline-directed protein phosphatase. Embo J 2003;22:3524-3535.
51. Denu JM, Zhou G, Guo Y, Dixon JE. The catalytic role of aspartic acid-92 in a human dual-specific protein-tyrosine-phosphatase. Biochemistry 1995;34:3396-3403.
52. Stuckey JA, Schubert HL, Fauman EB, Zhang ZY, Dixon JE, Saper MA. Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 A and the complex with tungstate. Nature 1994;370:571-575.
53. Martins A, Shuman S. Mechanism of phosphoanhydride cleavage by baculovirus phosphatase. J Biol Chem 2000;275:35070-35076.
54. Kornberg A, Rao NN, Ault-Riche D. Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 1999;68:89-125.
55. Sethuraman A, Rao NN, Kornberg A. The endopolyphosphatase gene: essential in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2001;98:8542-8547.
56. Akiyama M, Crooke E, Kornberg A. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J Biol Chem 1993;268:633-639.
57. Kumble KD, Kornberg A. Endopolyphosphatases for long chain inorganic polyphosphate in yeast and mammals. J Biol Chem 1996;271:27146-27151.
58. Van Dien SJ, Keasling JD. Effect of polyphosphate metabolism on the Escherichia coli phosphate-starvation response. Biotechnol Prog 1999;15:587-593.
59. Landrieu I, Hassan S, Sauty M, Dewitte F, Wieruszeski JM, Inze D, De Veylder L, Lippens G. Characterization of the Arabidopsis thaliana Arath;CDC25 dual-specificity tyrosine phosphatase. Biochem Biophys Res Commun 2004;322:734-739.