Evidence of SHIP2 Ser132 phosphorylation, its nuclear localization and stability

Biochemical Journal

Volumn 439, Issue 3, 2011, Pages 391-401

  Elong Edimo, William's ^a   Derua, Rita ^b   Janssens, Veerle ^b   Nakamura, Takeshi ^c   Vanderwinden, Jean Marie ^a   Waelkens, Etienne ^a   Erneux, Christophe ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Nuclear speckle; Phosphoinositide; Phosphorylation; SH2 (Src homology 2) domain containing inositol phosphatase 2 (SHIP2)

Indexed keywords

PHOSPHATASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SERINE; SH2 DOMAIN CONTAINING INOSITOL PHOSPHATASE 2; UNCLASSIFIED DRUG; INPPL1 PROTEIN, HUMAN; NUCLEAR PROTEIN;

ARTICLE; ASTROCYTOMA CELL; CELL CYCLE; CELL MEMBRANE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEOMICS; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; COMPARATIVE STUDY; ENZYMOLOGY; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

MAMMALIA;

ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; NUCLEAR PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN STABILITY; SERINE;

EID: 80054028201     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110173     Document Type: Article

References (50)

1. McCrea, H. J. and De Camilli, P. (2009) Mutations in phosphoinositide metabolizing enzymes and human disease. Physiology (Bethesda) 24, 8-16
2. Ooms, L. M., Horan, K. A., Rahman, P., Seaton, G., Gurung, R., Kethesparan, D. S. and Mitchell, C. A. (2009) The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease. Biochem. J. 419, 29-49
3. Bunney, T. D. and Katan, M. (2010) Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat. Rev. Cancer 10, 342-352
4. Blero, D., Payrastre, B., Schurmans, S. and Erneux, C. (2007) Phosphoinositide phosphatases in a network of signalling reactions. Pflügers Arch. 455, 31-44 (Pubitemid 47403989)
5. Damen, J. E., Liu, L., Rosten, P., Humphries, R. K., Jefferson, A. B., Majerus, P. W. and Krystal, G. (1996) The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5- triphosphate 5-phosphatase. Proc. Natl. Acad. Sci. U.S.A. 93, 1689-1693
6. Kavanaugh, W. M., Pot, D. A., Chin, S. M., Deuter-Reinhard, M., Jefferson, A. B., Norris, F. A., Masiarz, F. R., Cousens, L. S., Majerus, P. W. and Williams, L. T. (1996) Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr. Biol. 6, 438-445 (Pubitemid 126656291)
7. Pesesse, X., Deleu, S., De Smedt, F., Drayer, L. and Erneux, C. (1997) Identification of a second SH2-domain-containing protein closely related to the phosphatidylinositol polyphosphate 5-phosphatase SHIP. Biochem. Biophys. Res. Commun. 239, 697-700 (Pubitemid 27504164)
8. Pesesse, X., Dewaste, V., De Smedt, F., Laffargue, M., Giuriato, S., Moreau, C., Payrastre, B. and Erneux, C. (2001) The Src homology 2 domain containing inositol 5-phosphatase SHIP2 is recruited to the epidermal growth factor (EGF) receptor and dephosphorylates phosphatidylinositol 3,4,5-trisphosphate in EGF-stimulated COS-7 cells. J. Biol. Chem. 276, 28348-28355
9. Clement, S., Krause, U., Desmedt, F., Tanti, J. F., Behrends, J., Pesesse, X., Sasaki, T., Penninger, J., Doherty, M., Malaisse, W. et al. (2001) The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409, 92-97 (Pubitemid 32098631)
10. Sleeman, M. W., Wortley, K. E., Lai, K. M., Gowen, L. C., Kintner, J., Kline, W. O., Garcia, K., Stitt, T. N., Yancopoulos, G. D., Wiegand, S. J. and Glass, D. J. (2005) Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity. Nat. Med. 11, 199-205 (Pubitemid 40321356)
11. Jurynec, M. J. and Grunwald, D. J. (2010) SHIP2, a factor associated with diet-induced obesity and insulin sensitivity, attenuates FGF signaling in vivo. Dis. Model Mech. 3, 733-742
12. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
13. Brehme, M., Hantschel, O., Colinge, J., Kaupe, I., Planyavsky, M., Kocher, T., Mechtler, K., Bennett, K. L. and Superti-Furga, G. (2009) Charting the molecular network of the drug target Bcr-Abl. Proc. Natl. Acad. Sci. U.S.A. 106, 7414-7419
14. Prasad, N. K., Tandon, M., Badve, S., Snyder, P. W. and Nakshatri, H. (2008) Phosphoinositol phosphatase SHIP2 promotes cancer development and metastasis coupled with alterations in EGF receptor turnover. Carcinogenesis 29, 25-34 (Pubitemid 351201738)
15. Grempler, R., Leicht, S., Kischel, I., Eickelmann, P. and Redemann, N. (2007) Inhibition of SH2-domain containing inositol phosphatase 2 (SHIP2) in insulin producing INS1E cells improves insulin signal transduction and induces proliferation. FEBS Lett. 581, 5885-5890 (Pubitemid 50009357)
16. Yu, J., Ryan, D. G., Getsios, S., Oliveira-Fernandes, M., Fatima, A. and Lavker, R. M. (2008) MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc. Natl. Acad. Sci. U.S.A. 105, 19300-19305
17. Dyson, J. M., O'Malley, C. J., Becanovic, J., Munday, A. D., Berndt, M. C., Coghill, I. D., Nandurkar, H. H., Ooms, L. M. and Mitchell, C. A. (2001) The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J. Cell Biol. 155, 1065-1079 (Pubitemid 34286256)
18. Paternotte, N., Zhang, J., Vandenbroere, I., Backers, K., Blero, D., Kioka, N., Vanderwinden, J. M., Pirson, I. and Erneux, C. (2005) SHIP2 interaction with the cytoskeletal protein Vinexin. FEBS J. 272, 6052-6066 (Pubitemid 41713695)
19. Raaijmakers, J. H., Deneubourg, L., Rehmann, H., de Koning, J., Zhang, Z., Krugmann, S., Erneux, C. and Bos, J. L. (2007) The PI3K effector Arap3 interacts with the PI(3,4,5)P3 phosphatase SHIP2 in a SAM domain-dependent manner. Cell. Signalling 19, 1249-1257 (Pubitemid 46578336)
20. Vandenbroere, I., Paternotte, N., Dumont, J. E., Erneux, C. and Pirson, I. (2003) The c-Cbl-associated protein and c-Cbl are two new partners of the SH2-containing inositol polyphosphate 5-phosphatase SHIP2. Biochem. Biophys. Res. Commun. 300, 494-500 (Pubitemid 38375836)
21. Prasad, N. K. and Decker, S. J. (2005) SH2-containing 5′-inositol phosphatase, SHIP2, regulates cytoskeleton organization and ligand-dependent down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 280, 13129-13136
22. Habib, T., Hejna, J. A., Moses, R. E. and Decker, S. J. (1998) Growth factors and insulin stimulate tyrosine phosphorylation of the 51C/SHIP2 protein. J. Biol. Chem. 273, 18605-18609 (Pubitemid 28334792)
23. Sasaoka, T., Kikuchi, K., Wada, T., Sato, A., Hori, H., Murakami, S., Fukui, K., Ishihara, H., Aota, R., Kimura, I. and Kobayashi, M. (2003) Dual role of Src homology domain 2-containing inositol phosphatase 2 in the regulation of platelet-derived growth factor and insulin-like growth factor I signaling in rat vascular smooth muscle cells. Endocrinology 144, 4204-4214 (Pubitemid 37088777)
24. Batty, I. H., Van der Kaay, J., Gray, A., Telfer, J. F., Dixon, M. J. and Downes, C. P. (2007) The control of phosphatidylinositol 3,4-bisphosphate concentrations by activation of the Src homology 2 domain containing inositol polyphosphate 5-phosphatase 2, SHIP2. Biochem. J. 407, 255-266
25. Taylor, V., Wong, M., Brandts, C., Reilly, L., Dean, N. M., Cowsert, L. M., Moodie, S. and Stokoe, D. (2000) 5′ phospholipid phosphatase SHIP-2 causes protein kinase B inactivation and cell cycle arrest in glioblastoma cells. Mol. Cell Biol. 20, 6860-6871
26. Wisniewski, D., Strife, A., Swendeman, S., Erdjument-Bromage, H., Geromanos, S., Kavanaugh, W. M., Tempst, P. and Clarkson, B. (1999) A novel SH2-containing phosphatidylinositol 3,4,5-trisphosphate 5- phosphatase (SHIP2) is constitutively tyrosine phosphorylated and associated with src homologous and collagen gene (SHC) in chronic myelogenous leukemia progenitor cells. Blood 93, 2707-2720 (Pubitemid 29181204)
27. Aoki, K., Nakamura, T., Inoue, T., Meyer, T. and Matsuda, M. (2007) An essential role for the SHIP2-dependent negative feedback loop in neuritogenesis of nerve growth factor-stimulated PC12 cells. J. Cell Biol. 177, 817-827 (Pubitemid 46873088)
28. Muraille, E., Pesesse, X., Kuntz, C. and Erneux, C. (1999) Distribution of the src-homology-2-domain-containing inositol 5- phosphatase SHIP-2 in both non-haemopoietic and haemopoietic cells and possible involvement of SHIP-2 in negative signalling of B-cells. Biochem. J. 342, 697-705 (Pubitemid 29452656)
29. Zwaenepoel, K., Goris, J., Erneux, C., Parker, P. J. and Janssens, V. (2010) Protein phosphatase 2A PR130/B″ α1 subunit binds to the SH2 domain-containing inositol polyphosphate 5-phosphatase 2 and prevents epidermal growth factor (EGF)-induced EGF receptor degradation sustaining EGF-mediated signaling. FASEB J. 24, 538-547
30. Vandeput, F., Backers, K., Villeret, V., Pesesse, X. and Erneux, C. (2006) The influence of anionic lipids on SHIP2 phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase activity. Cell. Signalling 18, 2193-2199 (Pubitemid 44636162)
31. Roger, P., Taton, M., Van, S. J. and Dumont, J. E. (1988) Mitogenic effects of thyrotropin and adenosine 3′,5′-monophosphate in differentiated normal human thyroid cells in vitro. J. Clin. Endocrinol. Metab. 66, 1158-1165
32. Blero, D., Zhang, J., Pesesse, X., Payrastre, B., Dumont, J. E., Schurmans, S. and Erneux, C. (2005) Phosphatidylinositol 3,4,5-trisphosphate modulation in SHIP2-deficient mouse embryonic fibroblasts. FEBS J. 272, 2512-2522 (Pubitemid 40705071)
33. Osborne, S. L., Thomas, C. L., Gschmeissner, S. and Schiavo, G. (2001) Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J. Cell Sci. 114, 2501-2511 (Pubitemid 32684804)
34. 2+, ErbB3, and phosphoinositide 3-kinase in 1321N1 astrocytoma cells. J. Biol. Chem. 277, 338-344
35. Lamond, A. I. and Spector, D. L. (2003) Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4, 605-612 (Pubitemid 36934962)
36. Vandeput, F., Combettes, L., Mills, S. J., Backers, K., Wohlkonig, A., Parys, J. B., De Smedt, H., Missiaen, L., Dupont, G., Potter, B. V. and Erneux, C. (2007) Biphenyl 2,3′,4,5′,6-pentakisphosphate, a novel inositol polyphosphate surrogate, modulates Ca2+ responses in rat hepatocytes. FASEB J. 21, 1481-1491 (Pubitemid 46684850)
37. Backers, K., Blero, D., Paternotte, N., Zhang, J. and Erneux, C. (2003) The termination of PI3K signalling by SHIP1 and SHIP2 inositol 5-phosphatases. Adv. Enzyme Regul. 43, 15-28 (Pubitemid 36872819)
38. Suwa, A., Kurama, T. and Shimokawa, T. (2010) SHIP2 and its involvement in various diseases. Expert Opin. Ther. Targets 14, 727-737
39. Deleris, P., Bacqueville, D., Gayral, S., Carrez, L., Salles, J. P., Perret, B. and Breton-Douillon, M. (2003) SHIP-2 and PTEN are expressed and active in vascular smooth muscle cell nuclei, but only SHIP-2 is associated with nuclear speckles. J. Biol. Chem. 278, 38884-38891 (Pubitemid 37221788)
40. Lindsay, Y., McCoull, D., Davidson, L., Leslie, N. R., Fairservice, A., Gray, A., Lucocq, J. and Downes, C. P. (2006) Localization of agonist-sensitive PtdIns(3,4,5)P3 reveals a nuclear pool that is insensitive to PTEN expression. J. Cell Sci. 119, 5160-5168 (Pubitemid 46085194)
41. Barlow, C. A., Laishram, R. S. and Anderson, R. A. (2010) Nuclear phosphoinositides: a signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol. 20, 25-35
42. Keune, W., Bultsma, Y., Sommer, L., Jones, D. and Divecha, N. (2011) Phosphoinositide signalling in the nucleus. Adv. Enzyme Regul. 51, 91-99
43. Mellman, D. L., Gonzales, M. L., Song, C., Barlow, C. A., Wang, P., Kendziorski, C. and Anderson, R. A. (2008) A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 451, 1013-1017 (Pubitemid 351301736)
44. Hendrix, P., Mayer-Jackel, R. E., Cron, P., Goris, J., Hofsteenge, J., Merlevede, W. and Hemmings, B. A. (1993) Structure and expression of a 72-kDa regulatory subunit of protein phosphatase 2A. Evidence for different size forms produced by alternative splicing. J. Biol. Chem. 268, 15267-15276 (Pubitemid 23206684)
45. 2+-binding EF-hand motifs in the B″/PR72 subunit of protein phosphatase 2A. J. Biol. Chem. 278, 10697-10706
46. Marmiroli, S., Bertacchini, J., Beretti, F., Cenni, V., Guida, M., De Pol, A., Maraldi, N. M. and Lattanzi, G. (2009) A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward. J. Cell. Physiol. 220, 553-561
47. Jagatheesan, G., Thanumalayan, S., Muralikrishna, B., Rangaraj, N., Karande, A. A. and Parnaik, V. K. (1999) Colocalization of intranuclear lamin foci with RNA splicing factors. J. Cell Sci. 112, 4651-4661 (Pubitemid 30034813)
48. Ruschmann, J., Ho, V., Antignano, F., Kuroda, E., Lam, V., Ibaraki, M., Snyder, K., Kim, C., Flavell, R. A., Kawakami, T. et al. (2010) Tyrosine phosphorylation of SHIP promotes its proteasomal degradation. Exp. Hematol. 38, 392-402
49. Maccario, H., Perera, N. M., Davidson, L., Downes, C. P. and Leslie, N. R. (2007) PTEN is destabilized by phosphorylation on Thr366. Biochem. J. 405, 439-444
50. Prasad, N. K., Werner, M. E. and Decker, S. J. (2009) Specific tyrosine phosphorylations mediate signal-dependent stimulation of SHIP2 inositol phosphatase activity, while the SH2 domain confers an inhibitory effect to maintain the basal activity. Biochemistry 48, 6285-6287