Unique biochemical properties of the protein tyrosine phosphatase activity of PTEN-Demonstration of different active site structural requirements for phosphopeptide and phospholipid phosphatase activities of PTEN

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 9, 2010, Pages 1785-1795

  Chia, Joel Yeong Chit ^a   Gajewski, Joanna E ^a   Xiao, Yi ^b   Zhu, Hong Jian ^b   Cheng, Heung Chin ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

Catalytic mechanism; Enzymology; Kinetic analysis; Phosphotransfer reaction; Protein tyrosine phosphatase; PTEN

Indexed keywords

PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PROTEIN TYROSINE PHOSPHATASE; RECOMBINANT PROTEIN; PEPTIDE FRAGMENT; POLYPHOSPHOINOSITIDE; PTEN PROTEIN, HUMAN; TYROSINE;

ALLOSTERISM; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; MUTATION; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS;

CATALYTIC DOMAIN; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN CONFORMATION; PTEN PHOSPHOHYDROLASE; TYROSINE;

EID: 77955093418     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.05.009     Document Type: Article

References (35)

1. Lee J.O., Yang H., Georgescu M.M., Di Cristofano A., Maehama T., Shi Y., Dixon J.E., Pandolfi P., Pavletich N.P. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999, 99:323-334.
2. Maehama T., Taylor G.S., Dixon J.E. PTEN and myotubularin: novel phosphoinositide phosphatases. Annu. Rev. Biochem. 2001, 70:247-279.
3. Myers M.P., Pass I., Batty I.H., Van der Kaay J., Stolarov J.P., Hemmings B.A., Wigler M.H., Downes C.P., Tonks N.K. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13513-13518.
4. Dey N., Crosswell H.E., De P., Parsons R., Peng Q., Su J.D., Durden D.L. The protein phosphatase activity of PTEN regulates SRC family kinases and controls glioma migration. Cancer Res. 2008, 68:1862-1871.
5. Ning K., Pei L., Liao M., Liu B., Zhang Y., Jiang W., Mielke J.G., Li L., Chen Y., El-Hayek M.G., Zhang X., Liu F., Eubanks J., Wang Q. Dual neuroprotective signaling mediated by downregulating two distinct phosphatase activities of PTEN. J. Neurosci. 2004, 24:4052-4060.
6. Okumura K., Zhao M., DePinho R.A., Furnari F.B., Cavenee W.K. PTEN: a novel anti-oncogenic function independent of phosphatase activity. Cell Cycle 2005, 4:540-542.
7. Okumura K., Zhao M., Depinho R.A., Furnari F.B., Cavenee W.K. Cellular transformation by the MSP58 oncogene is inhibited by its physical interaction with the PTEN tumor suppressor. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2703-2706.
8. Shen W.H., Balajee A.S., Wang J., Wu H., Eng C., Pandolfi P.P., Yin Y. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 2007, 128:157-170.
9. Myers M.P., Stolarov J.P., Eng C., Li J., Wang S.I., Wigler M.H., Parsons R., Tonks N.K. P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9052-9057.
10. Xiao Y., Chia J.Y.-C., Gajewski J.E., Sio Seng Lio D., Mulhern T.D., Zhu H.J., Nandurkar H., Cheng H.C. PTEN catalysis of phospholipid dephosphorylation reaction follows a two-step mechanism in which the conserved aspartate-92 does not function as the general acid-mechanistic analysis of a familial Cowden disease-associated PTEN mutation. Cell. Signal. 2007, 19:1434-1445.
11. Zhang Z.Y. Chemical and mechanistic approaches to the study of protein tyrosine phosphatases. Acc. Chem. Res. 2003, 36:385-392.
12. Myers M.P., Pass I., Batty I.H., Van der Kaay J., Stolarov J.P., Hemmings B.A., Wigler M.H., Downes C.P., Tonks N.K. The lipid phosphatase activity of PTEN is critical for its tumor suppressor function. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:13513-13518.
13. Gajewski J.E., Bird M.J., Crowhurst M.O., Sio-Seng Lio D., Liu J., Wettenhall R.E., Zhu H.J., Cheng H.C. Expression, generation, and purification of unphosphorylated and phospho-Ser-380/Thr-382/Thr-383 form of recombinant PTEN phosphatase. Protein Expr. Purif. 2007, 55:334-342.
14. Sotirellis N., Johnson T.M., Hibbs M.L., Stanley I.J., Stanley E., Dunn A.R., Cheng H.C. Autophosphorylation induces autoactivation and a decrease in the Src homology 2 domain accessibility of the Lyn protein kinase. J. Biol. Chem. 1995, 270:29773-29780.
15. Cheung N.S., Choy M.S., Halliwell B., Teo T.S., Bay B.H., Lee A.Y., Qi R.Z., Koh V.H., Whiteman M., Koay E.S., Chiu L.L., Zhu H.J., Wong K.P., Beart P.M., Cheng H.C. Lactacystin-induced apoptosis of cultured mouse cortical neurons is associated with accumulation of PTEN in the detergent-resistant membrane fraction. Cell. Mol. Life Sci. 2004, 61:1926-1934.
16. Johnson T.M., Perich J.W., Bjorge J.D., Fujita D.J., Cheng H.C. Common and differential recognition of structural features in synthetic peptides by the catalytic domain and the Src-homology 2 (SH2) domain of pp 60c-src. J. Pept. Res. 1997, 50:365-371.
17. Foulkes J.G., Howard R.F., Ziemiecki A. Detection of a novel mammalian protein phosphatase with activity for phosphotyrosine. FEBS Lett. 1981, 130:197-200.
18. Layton M.J., Harpur A.G., Panayotou G., Bastiaens P.I., Waterfield M.D. Binding of a diphosphotyrosine-containing peptide that mimics activated platelet-derived growth factor receptor beta induces oligomerization of phosphatidylinositol 3-kinase. J. Biol. Chem. 1998, 273:33379-33385.
19. Tamura M., Gu J., Matsumoto K., Aota S., Parsons R., Yamada K.M. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 1998, 280:1614-1617.
20. Eng C. PTEN: one gene, many syndromes. Hum. Mutat. 2003, 22:183-198.
21. Nassiri I., Faghihi M., Tavassoli M. Pharmacogenomic profiling of the PI3K/PTEN pathway in sporadic breast cancer. Iran. Biomed. J. 2009, 13:79-86.
22. Flint A.J., Tiganis T., Barford D., Tonks N.K. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1680-1685.
23. Keng Y.F., Wu L., Zhang Z.Y. Probing the function of the conserved tryptophan in the flexible loop of the Yersinia protein-tyrosine phosphatase. Eur. J. Biochem. 1999, 259:809-814.
24. Brandao T.A., Robinson H., Johnson S.J., Hengge A.C. Impaired acid catalysis by mutation of a protein loop hinge residue in a YopH mutant revealed by crystal structures. J. Am. Chem. Soc. 2009, 131:778-786.
25. Odriozola L., Singh G., Hoang T., Chan A.M. Regulation of PTEN activity by its carboxyl-terminal autoinhibitory domain. J. Biol. Chem. 2007, 282:23306-23315.
26. Guan K.L., Dixon J.E. Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate. J. Biol. Chem. 1991, 266:17026-17030.
27. Martins A., Shuman S. Mechanism of phosphoanhydride cleavage by baculovirus phosphatase. J. Biol. Chem. 2000, 275:35070-35076.
28. Blume-Jensen P., Hunter T. Two-dimensional phosphoamino acid analysis. Meth. Mol. Biol. 2001, 124:49-65.
29. Al-Khouri A.M., Ma Y., Togo S.H., Williams S., Mustelin T. Cooperative phosphorylation of the tumor suppressor phosphatase and tensin homologue (PTEN) by casein kinases and glycogen synthase kinase 3beta. J. Biol. Chem. 2005, 280:35195-35202.
30. Maccario H., Perera N.M., Davidson L., Downes C.P., Leslie N.R. PTEN is destabilized by phosphorylation on Thr366. Biochem. J. 2007, 405:439-444.
31. Gu J., Tamura M., Pankov R., Danen E.H., Takino T., Matsumoto K., Yamada K.M. Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J. Cell Biol. 1999, 146:389-403.
32. Tonks N.K., Neel B.G. Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol. 2001, 13:182-195.
33. McConnachie G., Pass I., Walker S.M., Downes C.P. Interfacial kinetic analysis of the tumour suppressor phosphatase. PTEN: evidence for activation by anionic phospholipids. Biochem J 2003, 371:947-955.
34. Campbell R.B., Liu F., Ross A.H. Allosteric activation of PTEN phosphatase by phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 2003, 278:33617-33620.
35. Kaplan W., Littlejohn T.G. Swiss-PDB Viewer. Deep View. Brief. Bioinform. 2001, 2:195-197.