An inactive protein phosphatase 2A population is associated with methylesterase and can be re-activated by the phosphotyrosyl phosphatase activator

Biochemical Journal

Volumn 380, Issue 1, 2004, Pages 111-119

  Longin, Sari ^a   Jordens, Jan ^a   Martens, Ellen ^a   Stevens, Ilse ^a   Janssens, Veerle ^a   Rondelez, Evelien ^a   De Baere, Ivo ^a   Derua, Rita ^a   Waelkens, Etienne ^a   Goris, Jozef ^a   Van Hoof, Christine ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Methylation; Methylesterase; Phosphorylation; Phosphotyrosyl phosphatase activator; Protein phosphatase 2A (PP2A); Signal transduction

Indexed keywords

CLONING; ENZYMES; PROTEINS; PURIFICATION;

ENZYME ACTIVATORS; ENZYME ACTIVITY;

BIOCHEMISTRY;

ESTERASE; METHYLESTERASE; METHYLTRANSFERASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CLONING; CONTROLLED STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

ANIMALS; BIOPOLYMERS; BRAIN; CARBOXYLIC ESTER HYDROLASES; ENZYME ACTIVATION; MAGNESIUM; MANGANESE; MUSCLE PROTEINS; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN O-METHYLTRANSFERASE; PROTEINS; RABBITS; RECOMBINANT PROTEINS; SWINE;

ANIMALIA;

EID: 2642530239     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031643     Document Type: Article

References (54)

1. Janssens, V. and Goris, J. (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353, 417-439
2. Kremmer, E., Ohst, K., Kiefer, J., Brewis, N. and Walter, G. (1997) Separation of PP2A core enzyme and holo-enzyme with monoclonal antibodies against the regulatory A subunit: abundant expression of both forms in cells. Mol. Cell. Biol. 17, 1692-1701
3. Li, X. and Virshup, D. M. (2002) Two conserved domains in regulatory B subunits mediate binding to the A subunit of protein phosphatase 2A. Eur. J. Biochem. 269, 546-552
4. Strack, S., Ruediger, R., Walter, G., Dagda, R. K., Barwacz, C. A. and Cribbs, J. T. (2002) Protein phosphatase 2A holo-enzyme assembly: identification of contacts between B family regulatory and scaffolding A subunits. J. Biol. Chem. 277, 20750-20755
5. Millward, T. A., Zolnierowicz, S. and Hemmings, B. A. (1999) Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem. Sci. 24, 186-191
6. Kapiloff, M. S., Jackson, N. and Airhart, N. (2001) mAKAP and the ryanodine receptor are part of a multi-component signaling complex on the cardiomyocyte nuclear envelope. J. Cell Sci. 114, 3167-3176
7. Hart, M. J., de los Santos, R., Albert, I. N., Rubinfeld, B. and Polakis, P. (1998) Downregulation of β-catenin by human Axin and its association with the APC tumor suppressor, β-catenin and GSK3β. Curr. Biol. 8, 573-581
8. Takahashi, M., Shibata, H., Shimakawa, M., Miyamoto, M., Mukai, H. and Ono, Y. (1999) Characterization of a novel giant scaffolding protein, CG-NAP, that anchors multiple signaling enzymes to centrosome and the Golgi apparatus. J. Biol. Chem. 274, 17267-17274
9. Li, X., Yost, H. J., Virshup, D. M. and Seeling, J. M. (2001) Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus. EMBO J. 20, 4122-4131
10. Ikeda, S., Kishida, M., Matsuura, Y., Usui, H. and Kikuchi, A. (2000) GSK-3β-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by β-catenin and protein phosphatase 2A complexed with axin. Oncogene 19, 537-545
11. Abraham, D., Podar, K., Pacher, M., Kubicek, M., Welzel, N., Hemmings, B. A., Dilworth, S. M., Mischak, H., Kolch, W. and Baccarini, M. (2000) Raf-1-associated PP2A as a positive regulator of kinase activation. J. Biol. Chem. 275, 22300-22304
12. Chen, J., Martin, B. L. and Brautigan, D. L. (1992) Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257, 1261-1264
13. Chen, J., Parsons, S. and Brautigan, D. L. (1994) Tyrosine phosphorylation of protein phosphatase 2A in response to growth stimulation and v-src transformation of fibroblasts. J. Biol. Chem. 269, 7957-7962
14. Guy, G. R., Philp, R. and Tan, Y. H. (1995) Activation of protein kinases and the inactivation of protein phosphatase 2A in tumour necrosis factor and interleukin-1 signal-transduction pathways. Eur. J. Biochem. 229, 503-511
15. Guo, H. and Damuni, Z. (1993) Autophosphorylation-activated protein kinase phosphorates and inactivates protein phosphatase 2A. Proc. Natl. Acad. Sci. U.S.A. 90, 2500-2504
16. Damuni, Z., Xiong, H. and Li, M. (1994) Autophosphorylation-activated protein kinase inactivates the protein tyrosine phosphatase activity of protein phosphatase 2A. FEBS Lett. 352, 311-314
17. McCright, B., Rivers, A. M., Audlin, S. and Virshup, D. M. (1996) The B56 family of protein phosphatase 2A (PP2A) regulatory subunits encodes differentiation-induced phosphoproteins that target PP2A to both nucleus and cytoplasm. J. Biol. Chem. 271, 22081-22089
18. Usui, H., Inoue, R., Tanabe, O., Nishito, Y., Shimizu, M., Hayashi, H., Kagamiyama, H. and Takeda, M. (1998) Activation of protein phosphatase 2A by cAMP-dependent protein kinase-catalyzed phosphorylation of the 74-kDa B″ (δ) regulatory subunit in vitro and identification of the phosphorylation sites. FEBS Lett. 430, 312-316
19. 2+-binding EF-hand motifs in the B″/PR72 subunit of protein phosphatase 2A. J. Biol. Chem. 278, 10697-10706
20. Lee, J. and Stock, J. (1993) Protein phosphatase 2A catalytic subunit is methyl-esterified at its carboxyl terminus by a novel methyltransferase. J. Biol. Chem. 268, 19192-19195
21. Xie, H. and Clarke, S. (1993) Methyl esterification of C-terminal leucine residues in cytosolic 36-kDa polypeptides of bovine brain. J. Biol. Chem. 268, 13364-13371
22. Xie, H. and Clarke, S. (1994) Protein phosphatase 2A is reversibly modified by methyl esterification at its C-terminal leucine residue in bovine brain. J. Biol. Chem. 269, 1981-1984
23. Favre, B., Zolnierowicz, S., Turowski, P. and Hemmings, B. A. (1994) The catalytic subunit of protein phosphatase 2A is carboxyl-methylated in vivo. J. Biol. Chem. 269, 16311-16317
24. Turowski, P., Fernandez, A., Favre, B., Lamb, N. J. C. and Hemmings, B. A. (1995) Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression. J. Cell Biol. 129, 397-410
25. de Baere, I., Derua, R., Janssens, V., Van Hoof, C., Waelkens, E., Merlevede, W. and Goris, J. (1999) Purification of porcine brain protein phosphatase 2A leucine carboxyl methyltransferase and cloning of the human homologue. Biochemistry 38, 16539-16547
26. Lee, J., Chen, Y., Tolstykh, T. and Stock, J. (1996) A specific protein carboxyl methylesterase that demethylates phosphoprotein phosphatase 2A in bovine brain. Proc. Natl. Acad. Sci. U.S.A. 93, 6043-6047
27. Ogris, E., Du, X., Nelson, K. C., Mak, E. K., Yu, X. X., Lane, W. S. and Pallas, D. C. (1999) A protein phosphatase methylesterase (PME-1) is one of several novel proteins stably associating with two inactive mutants of protein phosphatase 2A. J. Biol. Chem. 274, 14382-14391
28. Ogris, E., Gibson, D. M. and Pallas, D. C. (1997) Protein phosphatase 2A subunit assembly: the catalytic subunit carboxy terminus is important for binding cellular B subunit but not polyomavirus middle tumor antigen. Oncogene 15, 911-917
29. Chung, H., Nairn, A. C., Murata, K. and Brautigan, D. L. (1999) Mutation of Tyr307 and Leu309 in the protein phosphatase 2A catalytic subunit favors association with the α4 subunit which promotes dephosphorylation of elongation factor-2. Biochemistry 38, 10371-10376
30. Evans, D. R. H., Myles, T., Hofsteenge, J. and Hammings, B. A. (1999) Functional expression of human P2Ac in yeast permits the identification of novel C-terminal and dominant-negative mutant forms. J. Biol. Chem. 274, 24038-24046
31. Wei, H., Ashby, D. G., Moreno, C. S., Ogris, E., Yeong, F. M., Corbett, A. H. and Pallas, D. C. (2001) Carboxymethylation of the PP2A catalytic subunit in Saccharomyces cerevisae is required for efficient interaction with the B-type subunits Cdc55p and Rts1p. J. Biol. Chem. 276, 1570-1577
32. Wu, J., Tolstykh, T., Lee, J., Boyd, K., Stock, J. B. and Broach, J. R. (2000) Carboxyl methylation of the phosphoprotein phosphatase 2A catalytic subunit promotes its functional association with regulatory subunits in vivo. EMBO J. 19, 5672-5681
33. Tolstykh, T., Lee, J., Vafai, S. and Stock, J. B. (2000) Carboxyl methylation regulates phosphoprotein phosphatase 2A by controlling the association of regulatory B subunits. EMBO J. 19, 5682-5691
34. Yu, X. X., Du, X., Moreno, C. S., Green, R. E., Ogris, E., Feng, Q., Chou, L., McQuoid, M. J. and Pallas, D. C. (2001) Methylation of the protein phosphatase 2A catalytic subunit is essential for association of Bα regulatory subunit but not SG2NA, striatin, or polyomavirus middle tumor antigen. Mol. Biol. Cell 12, 185-199
35. Bryant, J. C., Westphal, R. S. and Wadzinski, B. E. (1999) Methylated C-terminal leucine residue of PP2A catalytic subunit is important tor binding of regulatory Bα subunit. Biochem. J. 339, 241-246
36. 0 during retinoic acid-induced granulocytic differentiation and a modification on the catalytic subunit in S phase of HL-60 cells. Arch. Biochem. Biophys. 339, 210-217
37. Cayla, X., Goris, J., Hermann, J., Hendrix, P., Ozon, R. and Merlevede, W. (1990) Isolation and characterization of a tyrosyl phosphatase activator from rabbit skeletal muscle and Xenopus laevis oocytes. Biochemistry 29, 658-667
38. Cayla, X., van Hoof, C., Bosch, M., Waelkens, E., Vandekerckhove, J., Peeters, B., Merlevede, W. and Goris, J. (1994) Molecular cloning, expression, and characterization of PTPA, a protein that activates the tyrosyl phosphatase activity of protein phosphatase 2A. J. Biol. Chem. 269, 15668-15675
39. Van Hoof, C., Cayla, X., Bosch, M., Merlevede, W. and Goris, J. (1994) The phosphotyrosyl phosphatase activator of protein phosphatase 2A. A novel purification method, immunological and enzymic characterization. Eur. J. Biochem. 226, 899-907
40. Waelkens, E., Goris, J. and Merlevede, W. (1987) Purification and properties of the polycation-stimulated phosphorylase phosphatases from rabbit skeletal muscle. J. Biol. Chem. 262, 1049-1059
41. 0 defines a novel multimember family of regulatory subunits. Biochem. J. 317, 187-194
42. Janssens, V., Van Hoof, C., Merlevede, W. and Goris, J. (1998) PTPA regulating PP2A as a dual specificity phosphatase. Methods Mol. Biol. 93, 103-115
43. Stevens, I., Janssens, V., Martens, E., Dilwortn, S., Goris, J. and Van Hoof, C. (2003) Identification and characterization of B″-subunits of protein phosphatase 2A in Xenopus laevis oocytes and adult tissues. Eur. J. Biochem. 270, 376-387
44. Rosenfeld, J., Capdevielle, J., Guillemot, J. C. and Ferrara, P. (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Biochem. 203, 173-179
45. Cai, L., Chu, Y., Wilson, S. E. and Schlender, K. K. (1995) A metal-dependent form of protein phosphatase 2A. Biochem. Biophys. Res. Commun. 208, 274-279
46. 2+ in protein phosphatase 2A. J. Biochem. (Tokyo) 126, 632-638
47. 2+-independent one. FEBS Lett. 447, 29-33
48. Myles, T., Schmidt, K., Evans, D. R. H., Cron, P. and Hemmings, B. A. (2001) Active-site mutations impairing the catalytic function of the catalytic subunit of human protein phosphatase 2A permit baculovirus-mediated overexpression in insect cells. Biochem. J. 357, 225-232
49. Iyengar, V. and Woittiez, J. (1988) Trace elements in human clinical specimens: evaluation of literature data to identify reference values. Clin. Chem. 34, 474-481
50. 1 phase of the yeast cell cycle. J. Mol. Biol. 302, 103-120
51. van Hoof, C., Janssens, V., De Baere, I., Stark, M. J. R., de Winde, J. H., Winderickx, J., Thevelein, J. M., Merlevede, W. and Goris, J. (2001) The Saccaromyces cerevisiae phosphotyrosyl phosphatase activator proteins are required for a subset of the functions disrupted by protein phosphatase 2A mutations. Exp. Cell Res. 264, 372-387
52. Rempola, B., Kaniak, A., Migdalski, A., Rytka, J., Slonimski, P. P. and di Rago, J.-P. (2000) Functional analysis of RRD1 (YIL153w) and RRD2 (YIL152w), which encode two putative activators of the phosphotyrosyl phosphatase activity of PP2A in Saccaromyces cerevisiae. Mol. Gen. Genet. 262, 1081-1092
53. Hunter, T. and Plowman, G. D. (1997) The protein kinases of budding yeast: six score and more. Trends Biochem. Sci. 22, 18-22
54. Fellner, T., Lackner, D. H., Hombauer, H., Piribauer, P., Mudrak, I., Zaragoza, K., Juno, C. and Ogris, E. (2003) A novel and essential mechanism determining specificity and activity of protein phosphatase 2A (PP2A) in vivo. Genes Dev. 17, 2138-2150