The intrinsically disordered tails of PTEN and PTEN-L have distinct roles in regulating substrate specificity and membrane activity

Biochemical Journal

Volumn 473, Issue 2, 2016, Pages 135-144

  Masson, Glenn R ^a   Perisic, Olga ^a   Burke, John E ^a,b   Williams, Roger L ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

(PTEN L); Hydrogen deuterium exchange mass spectrometry (HDX MS); Interfacial catalysis; Intrinsically disordered protein regions; Phosphatase and tensin homologue deleted on chromosome 10 (PTEN)

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE LONG; UNCLASSIFIED DRUG; PTEN PROTEIN, HUMAN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME SPECIFICITY; LIPID VESICLE; MASS SPECTROMETRY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPODOPTERA FRUGIPERDA; AMINO ACID SEQUENCE; ANIMAL; CELL MEMBRANE; CHEMISTRY; GENETICS; INSECT; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SPODOPTERA;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; INSECTS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PTEN PHOSPHOHYDROLASE; SPODOPTERA; SUBSTRATE SPECIFICITY;

EID: 84955515031     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150931     Document Type: Article

References (58)

1. Liaw, D., Marsh, D.J., Li, J., Dahia, P.L.M., Wang, S.I., Zheng, Z., Bose, S., Call, K.M., Tsou, H.C., Peacoke, M. et al. (1997) Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat. Genet. 16, 64-67 CrossRef PubMed
2. Steck, P.A., Pershouse, M.A., Jasser, S.A., Yung, W.K.A., Lin, H., Ligon, A.H., Langford, L.A., Baumgard, M.L., Hattier, T., Davis, T. et al. (1997) Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 15, 356-362 CrossRef PubMed
3. Yuan, T.L. and Cantley, L.C. (2008) PI3K pathway alterations in cancer: variations on a theme. Oncogene 27, 5497-5510 CrossRef PubMed
4. 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 CrossRef PubMed
5. 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 CrossRef PubMed
6. 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 CrossRef PubMed
7. Cantley, L.C. and Neel, B.G. (1999) New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc. Natl. Acad. Sci. U.S.A. 96, 4240-4245 CrossRef PubMed
8. Shi, Y., Wang, J., Chandarlapaty, S., Cross, J., Thompson, C., Rosen, N. and Jiang, X. (2014) PTEN is a protein tyrosine phosphatase for IRS1. Nat. Struct. Mol. Biol. 21, 522-527 CrossRef PubMed
9. Suzuki, A., la Pompa, de, J.L., Stambolic, V., Elia, A.J., Sasaki, T., Barrantes, I.D.B., Ho, A., Wakeham, A., ltie, A., Khoo, W. et al. (1998) High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr. Biol. 8, 1169-1178 CrossRef PubMed
10. Salmena, L., Carracedo, A. and Pandolfi, P.P. (2008) Tenets of PTEN tumor suppression. Cell 133, 403-414 CrossRef PubMed
11. Berger, A.H., Knudson, A.G. and Pandolfi, P.P. (2011) A continuum model for tumour suppression. Nature 476, 163-169 CrossRef PubMed
12. Papa, A., Wan, L., Bonora, M., Salmena, L., Song, M.S., Hobbs, R.M., Lunardi, A., Webster, K., Ng, C., Newton, R.H. et al. (2014) Cancer-associated PTEN mutants act in a dominant-negative manner to suppress PTEN protein function. Cell 157, 595-610 CrossRef PubMed
13. 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. Cell 99, 323-334 CrossRef PubMed
14. Walker, S.M., Leslie, N.R., Perera, N.M., BATTY, I.H. and Downes, C.P. (2004) The tumour-suppressor function of PTEN requires an N-terminal lipid-binding motif. Biochem. J. 379, 301-307 CrossRef PubMed
15. Yang, J., Niu, T., Zhang, A., Mishra, A.K., Zhao, Z.J. and Zhou, G.W. (2001) Relation between the flexibility of the WPD loop and the activity of the catalytic domain of protein tyrosine phosphatase SHP-1. J. Cell. Biochem. 84, 47-55 CrossRef PubMed
16. Rodriguez-Escudero, I., Oliver, M.D., Andres-Pons, A., Molina, M., Cid, V.J. and Pulido, R. (2011) A comprehensive functional analysis of PTEN mutations: implications in tumorand autism-related syndromes. Hum. Mol. Genet. 20, 4132-4142 CrossRef PubMed
17. Brandão, T.A.S., Johnson, S.J. and Hengge, A.C. (2012) The molecular details of WPD-loop movement differ in the protein-tyrosine phosphatases YopH and PTP1B. Arch. Biochem. Biophys. 525, 53-59 CrossRef PubMed
18. Xiao, Y., Yeong Chit Chia, J., Gajewski, J.E., Sio Seng Lio, D., Mulhern, T.D., Zhu, H.-J., Nandurkar, H. and Cheng, H.-C. (2007) 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. 19, 1434-1445 CrossRef PubMed
19. Lu, J., Jeong, H., Kong, N., Yang, Y., Carroll, J., Luo, H.R., Silberstein, L.E. and YupoMa and Chai, L. (2009) Stem cell factor SALL4 represses the transcriptions of PTEN and SALL1 through an epigenetic repressor complex. PLoS One 4, e5577 CrossRef PubMed
20. Song, M.S., Salmena, L. and Pandolfi, P.P. (2012) The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell. Bio. 13, 283-296
21. 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 CrossRef PubMed
22. 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 CrossRef PubMed
23. Okumura, K. (2006) PCAF modulates PTEN activity. J. Biol. Chem. 281, 26562-26568 CrossRef PubMed
24. Lee, S.R., Yang, K.S., Kwon, J., Lee, C., Jeong, W. and Rhee, S.G. (2002) Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 277, 20336-20342 CrossRef PubMed
25. Wang, X., Trotman, L.C., Koppie, T., Alimonti, A., Chen, Z., Gao, Z., Wang, J., Erdjument-Bromage, H., Tempst, P., Cordon-Cardo, C. et al. (2007) NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128, 129-139 CrossRef PubMed
26. Huang, J., Yan, J., Zhang, J., Zhu, S., Wang, Y., Shi, T., Zhu, C., Chen, C., Liu, X., Cheng, J. et al. (2012) SUMO1 modification of PTEN regulates tumorigenesis by controlling its association with the plasma membrane. Nat. Commun. 3, 911 CrossRef PubMed
27. Putz, U., Howitt, J., Doan, A., Goh, C.P., Low, L.H., Silke, J. and Tan, S.S. (2012) The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci. Signal. 5, ra70 CrossRef PubMed
28. Pulido, R., Baker, S.J., Barata, J.T., Carracedo, A., Cid, V.J., Chin-Sang, I.D., Dave, V., Hertog, den, J., Devreotes, P., Eickholt, B.J. et al. (2014) A unified nomenclature and amino acid numbering for human PTEN. Sci. Signal. 7, pe15 CrossRef PubMed
29. Hopkins, B.D., Fine, B., Steinbach, N., Dendy, M., Rapp, Z., Shaw, J., Pappas, K., Yu, J.S., Hodakoski, C., Mense, S. et al. (2013) A secreted PTEN phosphatase that enters cells to alter signaling and survival. Science 341, 399-402 CrossRef PubMed
30. Liang, H., He, S., Yang, J., Jia, X., Wang, P., Chen, X., Zhang, Z., Zou, X., McNutt, M.A., Shen, W.H. et al. (2014) PTENα, a PTEN isoform translated through alternative initiation, regulates mitochondrial function and energy metabolism. Cell Metab. 19, 836-848 CrossRef PubMed
31. Malaney, P., Uversky, V.N. and Davé, V. (2013) The PTEN Long N-tail is intrinsically disordered: increased viability for PTEN therapy. Mol. BioSyst. 9, 2877 CrossRef PubMed
32. Johnston, S.B. and Raines, R.T. (2015) Catalysis by the tumor-suppressor enzymes PTEN and PTEN-L. PLoS One 10, e0116898 CrossRef PubMed
33. Al-Khouri, A.M., Ma, Y., Togo, S.H., Williams, S. and Mustelin, T. (2005) Cooperative phosphorylation of the tumor suppressor phosphatase and tensin homologue (PTEN) by casein kinases and glycogen synthase kinase 3β. J. Biol. Chem. 280, 35195-35202 CrossRef PubMed
34. Cordier, F., Chaffotte, A., Terrien, E., Préhaud, C., Theillet, F.-X., Delepierre, M., Lafon, M., Buc, H. and Wolff, N. (2012) Ordered phosphorylation events in two independent cascades of the PTEN C-tail revealed by NMR. J. Am. Chem. Soc. 134, 20533-20543 CrossRef PubMed
35. Bolduc, D., Rahdar, M., Tu-Sekine, B., Sivakumaren, S.C., Raben, D., Amzel, L.M., Devreotes, P., Gabelli, S.B. and Cole, P. (2013) Phosphorylation-mediated PTEN conformational closure and deactivation revealed with protein semisynthesis. Elife 2, e00691 CrossRef PubMed
36. 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 CrossRef PubMed
37. 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 CrossRef PubMed
38. Tibarewal, P., Zilidis, G., Spinelli, L., Schurch, N., Maccario, H., Gray, A., Perera, N.M., Davidson, L., Barton, G.J. and Leslie, N.R. (2012) PTEN protein phosphatase activity correlates with control of gene expression and invasion, a tumor-suppressing phenotype, but not with AKT activity. Sci. Signal. 5, ra18 CrossRef PubMed
39. Maccario, H., Perera, N.M., Davidson, L., Downes, C.P. and Leslie, N.R. (2007) PTEN is destabilized by phosphorylation on Thr 366. Biochem. J. 405, 439-444 CrossRef PubMed
40. Nalefski, E.A., Slazas, M.M. and Falke, J.J. (1997) Ca 2+-signaling cycle of a membrane-docking C2 domain. Biochemistry 36, 12011-12018 CrossRef PubMed
41. Vance, J. and Steenbergen, R. (2005) Metabolism and functions of phosphatidylserine. Prog. Lipid Res. 44, 207-234 CrossRef PubMed
42. Burke, J.E., Perisic, O., Masson, G.R., Vadas, O. and Williams, R.L. (2012) Oncogenic mutations mimic and enhance dynamic events in the natural activation of phosphoinositide 3-kinase p110α (PIK3CA). Proc. Natl. Acad. Sci. U.S.A. 109, 15259-15264 CrossRef PubMed
43. Jain, M.K. and Berg, O.G. (1989) The kinetics of interfacial catalysis by phospholipase A2 and regulation of interfacial activation: hopping versus scooting. Biochim Biophys Acta 1002, 127-156 CrossRef PubMed
44. McConnachie, G., Pass, I., Walker, S.M. and Downes, C.P. (2003) Interfacial kinetic analysis of the tumour suppressor phosphatase, PTEN: evidence for activation by anionic phospholipids. Biochem. J. 371, 947-955 CrossRef PubMed
45. Vanhaesebroeck, B. (1999) Autophosphorylation of p110delta phosphoinositide 3-kinase: a new paradigm for the regulation of lipid kinases in vitro and in vivo. EMBO J. 18, 1292-1302 CrossRef PubMed
46. 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 CrossRef PubMed
47. Gu, T., Zhang, Z., Wang, J., Guo, J., Shen, W.H. and Yin, Y. (2011) CREB is a novel nuclear target of PTEN phosphatase. Cancer Res. 71, 2821-2825; CrossRef PubMed
48. Schneider, E., Keppler, R., Prawitt, D., Steinwender, C., Roos, F.C., Thüroff, J.W., Lausch, E. and Brenner, W. (2011) Migration of renal tumor cells depends on dephosphorylation of Shc by PTEN. Int. J. Oncol. 38, 823-831 PubMed
49. Nakdimon, I., Walser, M., Fröhli, E. and Hajnal, A. (2012) PTEN Negatively Regulates MAPK Signaling during Caenorhabditis elegans vulval development. PLoS Genet. 8, e1002881 CrossRef PubMed
50. Shnitsar, I., Bashkurov, M., Masson, G.R., Ogunjimi, A.A., Mosessian, S., Cabeza, E.A., Hirsch, C.L., Trcka, D., Gish, G., Jiao, J. et al. (2015) PTEN regulates cilia through Dishevelled. Nat. Commun. 6, 8388 CrossRef PubMed
51. Blind, R.D., Suzawa, M. and Ingraham, H.A. (2012) Direct modification and activation of a nuclear receptor-PIP2 complex by the inositol lipid kinase IPMK. Sci. Signal. 5, ra44 CrossRef PubMed
52. Nguyen, H.N., Afkari, Y., Senoo, H., Sesaki, H., Devreotes, P.N. and Iijima, M. (2013) Mechanism of human PTEN localization revealed by heterologous expression in Dictyostelium. Oncogene 33, 5688-5696 CrossRef PubMed
53. Yasui, M., Matsuoka, S. and Ueda, M. (2014) PTEN hopping on the cell membrane is regulated via a positively-charged C2 domain. PLoS Comput. Biol. 10, e1003817 CrossRef PubMed
54. Lumb, C.N. and Sansom, M.S. P. (2013) Defining the membrane-associated state of the PTEN tumor suppressor protein. Biophys. J. 104, 613-621 CrossRef PubMed
55. Li, Q., Wanderling, S., Paduch, M., Medovoy, D., Singharoy, A., McGreevy, R., Villalba-Galea, C.A., Hulse, R.E., Roux, B., Schulten, K. et al. (2014) Structural mechanism of voltage-dependent gating in an isolated voltage-sensing domain. Nat. Struct. Mol. Biol. 21, 244-252 CrossRef PubMed
56. Hobiger, K., Utesch, T., Mroginski, M.A., Seebohm, G. and Friedrich, T. (2013) The linker pivot in Ci-VSP: the key to unlock catalysis. PLoS One 8, e70272 CrossRef PubMed
57. Wei, Y., Stec, B., Redfield, A.G., Weerapana, E. and Roberts, M.F. (2015) Phospholipid-binding sites of phosphatase and tensin homolog (PTEN). J. Biol. Chem. 290, 1592-1606 CrossRef PubMed
58. Dowler, S., Kular, G. and Alessi, D.R. (2002) Protein lipid overlay assay. Sci. Signal. 2002, pl6 CrossRef