The termination of PI3K signalling by SHIP1 and SHIP2 inositol 5-phosphatases

Advances in Enzyme Regulation

Volumn 43, Issue 1, 2003, Pages 15-28

  Backers, Katrien ^a   Blero, Daniel ^a   Paternotte, Nathalie ^a   Zhang, Jing ^a   Erneux, Christophe ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; MAMMALIA;

EID: 0037702455     PISSN: 00652571     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2571(02)00043-2     Document Type: Conference Paper

References (67)

1. Asano T, Mochizuki Y, Matsumoto K, Takenawa T, Endo T. Pharbin. A novel inositol polyphosphate 5-phosphatase induces dendritic appearances in fibroblasts. Biochem Biophys Res Commun 1999;261:188-95.
2. Attree O, Olivos IM, Okabe I, Bailey LC, Nelson DL, Lewis RA, McInnes RR, Nussbaum RL. The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 1992;358:239-42.
3. Blero D, De Smedt F, Pesesse X, Paternotte N, Moreau C, Payrastre B, Erneux C. The SH2 domain containing inositol 5-phosphatase SHIP2 controls phosphatidylinositol 3,4,5-trisphosphate levels in CHO-IR cells stimulated by insulin. Biochem Biophys Res Commun 2001;282:839-43.
4. Brauweiler A, Tamir I, Dal Porto J, Benschop RJ, Helgason CD, Humphries RK, Freed JH, Cambier JC. Differential regulation of B cell development, activation, and death by the src homology 2 domain-containing 5′ inositol phosphatase (SHIP). J Exp Med 2000;191:1545-54.
5. Choi Y, Zhang J, Murga C, Yu H, Koller E, Monia BP, Gutkind JS, Li W. PTEN, but not SHIP and SHIP2, suppresses the PI3K/Akt pathway and induces growth inhibition and apoptosis of myeloma cells. Oncogene 2002;21:5289-300.
6. Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, Dumont JE, Marchand-Brustel Y, Erneux C, Hue L, Schurmans S. The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 2001;409:92-7.
7. Communi D, Lecocq R, Erneux C. Arginine 343 and 350 are two active residues involved in substrate binding by human Type I D-myo-inositol 1,4,5,-trisphosphate 5- phosphatase. J Biol Chem 1996; 271:11676-83.
8. Damen JE, Liu L, Rosten P, Humphries RK, Jefferson AB, Majerus PW, Krystal G. 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 USA 1996;93:1689-93.
9. De Smedt F, Missiaen L, Parys JB, Vanweyenberg Y, De Smedt H, Erneux C. Isoprenylated human brain type I inositol 1,4,5-trisphosphate 5-phosphatase controls Ca2+ oscillations induced by ATP in Chinese hamster ovary cells. J Biol Chem 1997;272:17367-75.
10. De Smedt F, Verjans B, Mailleux P, Erneux C. Cloning and expression of human brain type I inositol 1,4,5-trisphosphate 5-phosphatase High levels of mRNA in cerebellar Purkinje cells. FEBS Lett 1994;347:69-72.
11. Dlakic M. Functionally unrelated signalling proteins contain a fold similar to Mg2+-dependent endonucleases. Trends Biochem Sci 2000;25:272-3.
12. Downes CP, Mussat MC, Michell RH. The inositol trisphosphate phosphomonoesterase of the human erythrocyte membrane. Biochem J 1982;203:169-77.
13. Drayer AL, Pesesse X, De Smedt F, Woscholski R, Parker P, Erneux C. Cloning and expression of a human placenta inositol 1,3,4,5- tetrakisphosphate and phosphatidylinositol 3,4,5-trisphosphate 5- phosphatase. Biochem Biophys Res Commun 1996;225:243-9.
14. Dyson JM, O'Malley CJ, Becanovic J, Munday AD, Berndt MC, Coghill ID, Nandurkar HH, Ooms LM, Mitchell CA. The SH2-containing inositol polyphosphate 5-phosphatase, SHIP-2, binds filamin and regulates submembraneous actin. J Cell Biol 2001;155:1065-79.
15. Erneux C, Govaerts C, Communi D, Pesesse X. The diversity and possible functions of the inositol polyphosphate 5- phosphatases. Biochim Biophys Acta 1998;1436:185-99.
16. Giallourakis C, Kashiwada M, Pan PY, Danial N, Jiang H, Cambier J, Coggeshall KM, Rothman P. Positive regulation of interleukin-4-mediated proliferation by the SH2-containing inositol-5′-phosphatase. J Biol Chem 2000;275:29275-82.
17. Giuriato S, Blero D, Robaye B, Bruyns C, Payrastre B, Erneux C. SHIP2 overexpression strongly reduces the proliferation rate of K562 erythroleukemia cell line. Biochem Biophys Res Commun 2002;296:106-10.
18. Giuriato S, Payrastre B, Drayer AL, Plantavid M, Woscholski R, Parker P, Erneux C, Chap H. Tyrosine phosphorylation and relocation of SHIP are integrin-mediated in thrombin-stimulated human blood platelets. J Biol Chem 1997;272:26857-63.
19. Habib T, Hejna JA, Moses RE, Decker SJ. Growth factors and insulin stimulate tyrosine phosphorylation of the 51C/SHIP2 protein. J Biol Chem 1998;273:18605-9.
20. Harmer SL, DeFranco AL. The src homology domain 2-containing inositol phosphatase SHIP forms a ternary complex with Shc and Grb2 in antigen receptor-stimulated B lymphocytes. J Biol Chem 1999;274:12183-91.
21. Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM, Borowski A, Jirik F, Krystal G, Humphries RK. Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev 1998;12:1610-20.
22. Hori H, Sasaoka T, Ishihara H, Wada T, Murakami S, Ishiki M, Kobayashi M. Association of SH2-containing inositol phosphatase 2 with the insulin resistance of diabetic db/db mice. Diabetes 2002;51:2387-94.
23. Huber M, Helgason CD, Damen JE, Liu L, Humphries RK, Krystal G. The src homology 2-containing inositol phosphatase (SHIP) is the gatekeeper of mast cell degranulation. Proc Natl Acad Sci USA 1998;95:11330-5.
24. Huber M, Helgason CD, Damen JE, Scheid M, Duronio V, Liu L, Ware MD, Humphries RK, Krystal G. The role of SHIP in growth factor induced signalling. Prog Biophys Mol Biol 1997;71:423-34.
25. Ijuin T, Mochizuki Y, Fukami K, Funaki M, Asano T, Takenawa T. Identification and characterization of a novel inositol polyphosphate 5-phosphatase. J Biol Chem 2000;275:10870-5.
26. Jefferson AB, Majerus PW. Mutation of the conserved domains of two inositol polyphosphate 5-phosphatases. Biochemistry 1996;35:7890-4.
27. Kavanaugh WM, Pot DA, Chin SM, Deuter-Reinhard M, Jefferson AB, Norris FA, Masiarz FR, Cousens LS, Majerus PW, Williams LT. Multiple forms of an inositol polyphosphate 5-phosphatase form signaling complexes with Shc and Grb2. Curr Biol 1996;6:438-45.
28. Kay BK, Williamson MP, Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 2000;14:231-41.
29. Kisseleva MV, Wilson MP, Majerus PW. The isolation and characterization of a cDNA encoding phospholipid- specific inositol polyphosphate 5-phosphatase. J Biol Chem 2000;275:20110-6.
30. Kong AM, Speed CJ, O'Malley CJ, Layton MJ, Meehan T, Loveland KL, Cheema S, Ooms LM, Mitchell CA. Cloning and characterization of a 72-kDa inositol-polyphosphate 5-phosphatase localized to the Golgi network. J Biol Chem 2000;275:24052-64.
31. Lin T, Orrison BM, Leahey AM, Suchy SF, Bernard DJ, Lewis RA, Nussbaum RL. Spectrum of mutations in the OCRL1 gene in the Lowe oculocerebrorenal syndrome. Am J Hum Genet 1997;60:1384-8.
32. Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold A, Rohrschneider LR. P150SHIP, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev 1996;10:1084-95.
33. Liu Q, Oliveira-Dos-Santos A J, Mariathasan S, Bouchard D, Jones J, Sarao R, Kozieradzki I, Ohashi PS, Penninger JM, Dumont DJ. The inositol polyphosphate 5-phosphatase SHIP is a crucial negative regulator of B cell antigen receptor signaling. J Exp Med 1998a;188:1333-42.
34. Liu Q, Shalaby F, Jones J, Bouchard D, Dumont DJ. The SH2-containing inositol polyphosphate 5-phosphatase ship is expressed during hematopoiesis and spermatogenesis. Blood 1998b;91:2753-9.
35. Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998;273:13375-8.
36. Majerus PW, Kisseleva MY, Norris FA. The role of phosphatases in inositol signaling reactions. J Biol Chem 1999;274:10669-72.
37. Marion E, Kaisaki PJ, Pouillon V, Gueydan C, Levy JC, Bodson A, Krzentowski G, Daubresse JC, Mockel J, Behrends J, Servais G, Szpirer C, Kruys V, Gauguier D, Schurmans S. The gene INPPL1, encoding the lipid phosphatase SHIP2, is a candidate for type 2 diabetes in rat and man. Diabetes 2002;51:2012-7.
38. Matzaris M, O'Malley CJ, Badger A, Speed CJ, Bird PI, Mitchell CA. Distinct membrane and cytosolic forms of inositol polyphosphate 5-phosphatase II. Efficient membrane localization requires two discrete domains. J Biol Chem 1998;273:8256-67.
39. McPherson PS, Garcia EP, Slepnev VI, David C, Zhang X, Grabs D, Sossin WS, Bauerfeind R, Nemoto Y, De Camilli P. A presynaptic inositol-5-phosphatase. Nature 1996;379:353-7.
40. Minagawa T, Ijuin T, Mochizuki Y, Takenawa T. Identification and characterization of a sac domain-containing phosphoinositide 5-phosphatase. J Biol Chem 2001;276:22011-5.
41. Mitchell CA, Gurung R, Kong AM, Dyson JM, Tan A, Ooms LM. Inositol polyphosphate 5-phosphatases: lipid phosphatases with flair. IUBMB Life 2002;53:25-36.
42. Mochizuki Y, Takenawa T. Novel inositol polyphosphate 5-phosphatase localizes at membrane ruffles. J Biol Chem 1999;274:36790-5.
43. Muraille E, Bruhns P, Pesesse X, Daeron M, Erneux C. The SH2 domain containing inositol 5-phosphatase SHIP2 associates to the immunoreceptor tyrosine-based inhibition motif of Fc gamma RIIB in B cells under negative signaling. Immunol Lett 2000;72:7-15.
44. Muraille E, Pesesse X, Kuntz C, Erneux C. 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 1999;342Pt3:697-705.
45. Nemoto Y, Arribas M, Haffner C, DeCamilli P. Synaptojanin 2, a novel synaptojanin isoform with a distinct targeting domain and expression pattern. J Biol Chem 1997;272:30817-21.
46. Ono M, Bolland S, Tempst P, Ravetch JV. Role of the inositol phosphatase SHIP in negative regulation of the immune system by the receptor Fc(gamma)RIIB. Nature 1996;383:263-6.
47. Pesesse X, Deleu S, De Smedt F, Drayer L, Erneux C. Identification of a second SH2-domain-containing protein closely related to the phosphatidylinositol polyphosphate 5-phosphatase SHIP. Biochem Biophys Res Commun 1997;239:697-700.
48. Pesesse X, Dewaste V, De Smedt F, Laffargue M, Giuriato S, Moreau C, Payrastre B, Erneux C. 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 2001;276:28348-55.
49. Phee H, Jacob A, Coggeshall KM. Enzymatic activity of the Src homology 2 domain-containing inositol phosphatase is regulated by a plasma membrane location. J Biol Chem 2000;275:19090-7.
50. Poe JC, Fujimoto M, Jansen PJ, Miller AS, Tedder TF. CD22 forms a quaternary complex with SHIP, Grb2, and Shc. A pathway for regulation of B lymphocyte antigen receptor-induced calcium flux. J Biol Chem 2000;275:17420-7.
51. Prasad N, Topping RS, Decker SJ. SH2-containing inositol 5′-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading. Mol Cell Biol 2001;21:1416-28.
52. Rameh LE, Tolias KF, Duckworth BC, Cantley LC. A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 1997;390:192-6.
53. Rechsteiner M, Rogers SW. Pest sequences and regulation by proteolysis. Trends Biochem Sci 1996;21:267-71.
54. Rohrschneider LR, Fuller JF, Wolf I, Liu Y, Lucas DM. Structure, function, and biology of SHIP proteins. Genes Dev 2000;14:505-20.
55. Sasaoka T, Hori H, Wada T, Ishiki M, Haruta T, Ishihara H, Kobayashi M. SH2-containing inositol phosphatase 2 negatively regulates insulin- induced glycogen synthesis in L6 myotubes. Diabetologia 2001;44:1258-67.
56. Scheid MP, Huber M, Damen JE, Hughes M, Kang V, Neilsen P, Prestwich GD, Krystal G, Duronio V. Phosphatidylinositol (3,4,5)P3 is essential but not sufficient for protein kinase B (PKB) activation; phosphatidylinositol (3,4)P2 is required for PKB phosphorylation at Ser-473: studies using cells from SH2-containing inositol-5-phosphatase knockout mice. J Biol Chem 2002;277:9027-35.
57. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 1998;95:29-39.
58. Stapleton D, Balan I, Pawson T, Sicheri F. The crystal structure of an Eph receptor SAM domain reveals a mechanism for modular dimerization. Nat Struct Biol 1999;6:44-9.
59. Stein E, Cerretti DP, Daniel TO. Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J Biol Chem 1996;271:23588-93.
60. Taylor V, Wong M, Brandts C, Reilly L, Dean NM, Cowsert LM, Moodie S, Stokoe D. Phospholipid phosphatase SHIP-2 causes protein kinase B inactivation and cell cycle arrest in glioblastoma cells. Mol Cell Biol 2000;20:6860-71.
61. Thanos CD, Faham S, Goodwill KE, Cascio D, Phillips M, Bowie JU. Monomeric structure of the human EphB2 sterile alpha motif domain. J Biol Chem 1999;274:37301-6.
62. Torres R, Firestein BL, Dong H, Staudinger J, Olson EN, Huganir RL, Bredt DS, Gale NW, Yancopoulos GD. PDZ proteins bind, cluster, and synaptically colocalize with Eph receptors and their ephrin ligands. Neuron 1998;21:1453-63.
63. Tsujishita Y, Guo S, Stolz LE, York JD, Hurley JH. Specificity determinants in phosphoinositide dephosphorylation: crystal structure of an archetypal inositol polyphosphate 5-phosphatase. Cell 2001;105:379-89.
64. Wada T, Sasaoka T, Funaki M, Hori H, Murakami S, Ishiki M, Haruta T, Asano T, Ogawa W, Ishihara H, Kobayashi M. Overexpression of SH2-containing inositol phosphatase 2 results in negative regulation of insulin-induced metabolic actions in 3T3-L1 adipocytes via its 5′-phosphatase catalytic activity. Mol Cell Biol 2001;21:1633-46.
65. Wisniewski D, Strife A, Swendeman S, Erdjument-Bromage H, Geromanos S, Kavanaugh WM, Tempst P, Clarkson B. 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 1999;93:2707-20.
66. Woscholski R, Parker PJ. Inositol lipid 5-phosphatases-traffic signals and signal traffic. Trends Biochem Sci 1997;22:427-31.
67. York JD, Odom AR, Murphy R, Ives EB, Wente SR. A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 1999;285:96-100.