Functional analysis of the protein phosphatase activity of PTEN

Biochemical Journal

Volumn 444, Issue 3, 2012, Pages 457-464

  Zhang, Xiaoqun Catherine ^a   Piccini, Antonella ^a,b   Myers, Michael P ^a,b   Van Aelst, Linda ^a   Tonks, Nicholas K ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Organotypic hippocampal slice culture; PDZ domain; Phosphatase and tensin homologue deleted on chromosome 10 (PTEN); Protein phosphatase; Spine density; Two photon laser scanning microscopy

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; SERINE; THREONINE;

ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; LASER MICROSCOPY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RAT;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; DENDRITIC SPINES; ENZYME ACTIVATION; HIPPOCAMPUS; MOLECULAR SEQUENCE DATA; ORGAN CULTURE TECHNIQUES; PHOSPHOPROTEIN PHOSPHATASES; PTEN PHOSPHOHYDROLASE; RATS;

EID: 84862208776     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120098     Document Type: Article

References (50)

1. Salmena, L., Carracedo, A. and Pandolfi, P. P. (2008) Tenets of PTEN tumor suppression. Cell 133, 403-414 (Pubitemid 351622014)
2. Hollander, M. C., Blumenthal, G. M. and Dennis, P. A. (2011) PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Nat. Rev. Cancer 11, 289-301
3. Leslie, N. R. and Foti, M. (2011) Non-genomic loss of PTEN function in cancer: not in my genes. Trends Pharmacol. Sci. 32, 131-140
4. Chang, N., El-Hayek, Y. H., Gomez, E. and Wan, Q. (2007) Phosphatase PTEN in neuronal injury and brain disorders. Trends Neurosci. 30, 581-586 (Pubitemid 350051425)
5. Endersby, R. and Baker, S. J. (2008) PTEN signaling in brain: neuropathology and tumorigenesis. Oncogene 27, 5416-5430
6. Lee, J. O., Yang, H., Georgescu, M. M., Di Cristofano, A., Maehama, T., Shi, Y., Dixon, J. E., Pandolfi, P. and Pavletich, N. P. (1999) Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 99, 323-334 (Pubitemid 29519911)
7. Gericke, A., Munson, M. and Ross, A. H. (2006) Regulation of the PTEN phosphatase. Gene 374, 1-9 (Pubitemid 43737118)
8. Bonifant, C. L., Kim, J. S. and Waldman, T. (2007) NHERFs, NEP, MAGUKs, and more: interactions that regulate PTEN. J. Cell. Biochem. 102, 878-885 (Pubitemid 350036928)
9. Nardella, C., Carracedo, A., Salmena, L. and Pandolfi, P. P. (2010) Faithfull modeling of PTEN loss driven diseases in the mouse. Curr. Top. Microbiol. Immunol. 347, 135-168
10. Kwon, C. H., Luikart, B. W., Powell, C. M., Zhou, J., Matheny, S. A., Zhang, W., Li, Y., Baker, S. J. and Parada, L. F. (2006) Pten regulates neuronal arborization and social interaction in mice. Neuron 50, 377-388
11. Fraser, M. M., Bayazitov, I. T., Zakharenko, S. S. and Baker, S. J. (2008) Phosphatase and tensin homolog, deleted on chromosome 10 deficiency in brain causes defects in synaptic structure, transmission and plasticity, and myelination abnormalities. Neuroscience 151, 476-488
12. Myers, M. P., Stolarov, J. P., Eng, C., Li, J., Wang, S. I., Wigler, M. H., Parsons, R. and Tonks, N. K. (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. U.S.A. 94, 9052-9057
13. Maehama, T. and Dixon, J. E. (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378 (Pubitemid 28268370)
14. Myers, M. P., Pass, I., Batty, I. H., Van der Kaay, J., Stolarov, J. P., Hemmings, B. A., Wigler, M. H., Downes, C. P. and Tonks, N. K. (1998) The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc. Natl. Acad. Sci. U.S.A. 95, 13513-13518 (Pubitemid 28523003)
15. Shi, S., Hayashi, Y., Esteban, J. A. and Malinow, R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343 (Pubitemid 32455340)
16. Arnold, D., Feng, L., Kim, J. and Heintz, N. (1994) A strategy for the analysis of gene expression during neural development. Proc. Natl. Acad. Sci. U.S.A. 91, 9970-9974 (Pubitemid 24311930)
17. Zito, K., Knott, G., Shepherd, G. M., Shenolikar, S. and Svoboda, K. (2004) Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44, 321-334 (Pubitemid 39346255)
18. Kopec, C. D., Li, B., Wei, W., Boehm, J. and Malinow, R. (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26, 2000-2009
19. Li, B., Woo, R. S., Mei, L. and Malinow, R. (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54, 583-597 (Pubitemid 46756136)
20. Davidson, L., Maccario, H., Perera, N. M., Yang, X., Spinelli, L., Tibarewal, P., Glancy, B., Gray, A., Weijer, C. J., Downes, C. P. and Leslie, N. R. (2010) Suppression of cellular proliferation and invasion by the concerted lipid and protein phosphatase activities of PTEN. Oncogene 29, 687-697
21. Raftopoulou, M., Etienne-Manneville, S., Self, A., Nicholls, S. and Hall, A. (2004) Regulation of cell migration by the C2 domain of the tumor suppressor PTEN. Science 303, 1179-1181 (Pubitemid 38233580)
22. Maier, D., Jones, G., Li, X., Schonthal, A. H., Gratzl, O., Van Meir, E. G. and Merlo, A. (1999) The PTEN lipid phosphatase domain is not required to inhibit invasion of glioma cells. Cancer Res. 59, 5479-5482 (Pubitemid 29526461)
23. Freeman, D. J., Li, A. G., Wei, G., Li, H. H., Kertesz, N., Lesche, R., Whale, A. D., Martinez-Diaz, H., Rozengurt, N., Cardiff, R. D., Liu, X. and Wu, H. (2003) PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 3, 117-130 (Pubitemid 37443385)
24. Yuan, X. J. and Whang, Y. E. (2002) PTEN sensitizes prostate cancer cells to death receptor-mediated and drug-induced apoptosis through a FADD-dependent pathway. Oncogene 21, 319-327
25. Ramaswamy, S., Nakamura, N., Vazquez, F., Batt, D. B., Perera, S., Roberts, T. M. and Sellers, W. R. (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 2110-2115 (Pubitemid 29117876)
26. Steelman, L. S., Navolanic, P. M., Sokolosky, M. L., Taylor, J. R., Lehmann, B. D., Chappell, W. H., Abrams, S. L., Wong, E. W., Stadelman, K. M., Terrian, D. M. et al. (2008) Suppression of PTEN function increases breast cancer chemotherapeutic drug resistance while conferring sensitivity to mTOR inhibitors. Oncogene 27, 4086-4095 (Pubitemid 351931994)
27. Cai, X. M., Tao, B. B., Wang, L. Y., Liang, Y. L., Jin, J. W., Yang, Y., Hu, Y. L. and Zha, X. L. (2005) Protein phosphatase activity of PTEN inhibited the invasion of glioma cells with epidermal growth factor receptor mutation type III expression. Int. J. Cancer 117, 905-912 (Pubitemid 41688564)
28. Dey, N., Crosswell, H. E., De, P., Parsons, R., Peng, Q., Su, J. D. and Durden, D. L. (2008) The protein phosphatase activity of PTEN regulates SRC family kinases and controls glioma migration. Cancer Res. 68, 1862-1871 (Pubitemid 351416572)
29. Leslie, N. R., Yang, X., Downes, C. P. and Weijer, C. J. (2007) PtdIns(3,4,5)P3-dependent and -independent roles for PTEN in the control of cell migration. Curr. Biol. 17, 115-125 (Pubitemid 46107842)
30. Ning, K., Pei, L., Liao, M., Liu, B., Zhang, Y., Jiang, W., Mielke, J. G., Li, L., Chen, Y., El-Hayek, Y. H. et al. (2004) Dual neuroprotective signaling mediated by downregulating two distinct phosphatase activities of PTEN. J. Neurosci. 24, 4052-4060 (Pubitemid 38544231)
31. Tamura, M., Gu, J., Takino, T. and Yamada, K. M. (1999) Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: differential involvement of focal adhesion kinase and p130Cas. Cancer Res. 59, 442-449 (Pubitemid 29048881)
32. Mahimainathan, L. and Choudhury, G. G. (2004) Inactivation of platelet-derived growth factor receptor by the tumor suppressor PTEN provides a novel mechanism of action of the phosphatase. J. Biol. Chem. 279, 15258-15268 (Pubitemid 38618922)
33. Torres, J. and Pulido, R. (2001) The tumor suppressor PTEN is phosphorylated by the protein kinase CK2 at its C terminus. Implications for PTEN stability to proteasome-mediated degradation. J. Biol. Chem. 276, 993-998 (Pubitemid 32096519)
34. Ning, K., Miller, L. C., Laidlaw, H. A., Burgess, L. A., Perera, N. M., Downes, C. P., Leslie, N. R. and Ashford, M. L. (2006) A novel leptin signalling pathway via PTEN inhibition in hypothalamic cell lines and pancreatic β-cells. EMBO J. 25, 2377-2387 (Pubitemid 44012221)
35. Ning, K., Miller, L. C., Laidlaw, H. A., Watterson, K. R., Gallagher, J., Sutherland, C. and Ashford, M. L. (2009) Leptin-dependent phosphorylation of PTEN mediates actin restructuring and activation of ATP-sensitive K+ channels. J. Biol. Chem. 284, 9331-9340
36. Birle, D., Bottini, N., Williams, S., Huynh, H., deBelle, I., Adamson, E. and Mustelin, T. (2002) Negative feedback regulation of the tumor suppressor PTEN by phosphoinositide-induced serine phosphorylation. J. Immunol. 169, 286-291 (Pubitemid 34686147)
37. Cheong, J. W., Eom, J. I., Maeng, H. Y., Lee, S. T., Hahn, J. S., Ko, Y. W. and Min, Y. H. (2003) Phosphatase and tensin homologue phosphorylation in the C-terminal regulatory domain is frequently observed in acute myeloid leukaemia and associated with poor clinical outcome. Br. J. Haematol. 122, 454-456 (Pubitemid 36951630)
38. Vazquez, F., Ramaswamy, S., Nakamura, N. and Sellers, W. R. (2000) Phosphorylation of the PTEN tail regulates protein stability and function. Mol. Cell. Biol. 20, 5010-5018 (Pubitemid 30431555)
39. Torres, J., Rodriguez, J., Myers, M. P., Valiente, M., Graves, J. D., Tonks, N. K. and Pulido, R. (2003) Phosphorylation-regulated cleavage of the tumor suppressor PTEN by caspase-3: implications for the control of protein stability and PTEN-protein interactions. J. Biol. Chem. 278, 30652-30660 (Pubitemid 36994570)
40. Das, S., Dixon, J. E. and Cho, W. (2003) Membrane-binding and activation mechanism of PTEN. Proc. Natl. Acad. Sci. U.S.A. 100, 7491-7496 (Pubitemid 36759997)
41. Odriozola, L., Singh, G., Hoang, T. and Chan, A. M. (2007) Regulation of PTEN activity by its carboxyl-terminal autoinhibitory domain. J. Biol. Chem. 282, 23306-23315 (Pubitemid 47311930)
42. Rahdar, M., Inoue, T., Meyer, T., Zhang, J., Vazquez, F. and Devreotes, P. N. (2009) A phosphorylation-dependent intramolecular interaction regulates the membrane association and activity of the tumor suppressor PTEN. Proc. Natl. Acad. Sci. U.S.A. 106, 480-485
43. Merlot, S. and Firtel, R. A. (2003) Leading the way: directional sensing through phosphatidylinositol 3-kinase and other signaling pathways. J. Cell Sci. 116, 3471-3478 (Pubitemid 37063391)
44. Tolkacheva, T., Boddapati, M., Sanfiz, A., Tsuchida, K., Kimmelman, A. C. and Chan, A. M. (2001) Regulation of PTEN binding to MAGI-2 by two putative phosphorylation sites at threonine 382 and 383. Cancer Res. 61, 4985-4989 (Pubitemid 32681524)
45. Vazquez, F., Grossman, S. R., Takahashi, Y., Rokas, M. V., Nakamura, N. and Sellers, W. R. (2001) Phosphorylation of the PTEN tail acts as an inhibitory switch by preventing its recruitment into a protein complex. J. Biol. Chem. 276, 48627-48630
46. Okahara, F., Ikawa, H., Kanaho, Y. and Maehama, T. (2004) Regulation of PTEN phosphorylation and stability by a tumor suppressor candidate protein. J. Biol. Chem. 279, 45300-45303 (Pubitemid 39491510)
47. Valiente, M., Andres-Pons, A., Gomar, B., Torres, J., Gil, A., Tapparel, C., Antonarakis, S. E. and Pulido, R. (2005) Binding of PTEN to specific PDZ domains contributes to PTEN protein stability and phosphorylation by microtubule-associated serine/threonine kinases. J. Biol. Chem. 280, 28936-28943 (Pubitemid 41161339)
48. Jurado, S., Benoist, M., Lario, A., Knafo, S., Petrok, C. N. and Esteban, J. A. (2010) PTEN is recruited to the postsynaptic terminal for NMDA receptor-dependent long-term depression. EMBO J. 29, 2827-2840
49. Vanhaesebroeck, B., Higashi, K., Raven, C., Welham, M., Anderson, S., Brennan, P., Ward, S. G. and Waterfield, M. D. (1999) Autophosphorylation of p110δ phosphoinositide 3-kinase: a new paradigm for the regulation of lipid kinases in vitro and in vivo. EMBO J. 18, 1292-1302 (Pubitemid 29110313)
50. Kim, E. and Sheng, M. (2004) PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771-781 (Pubitemid 39336214)