Encyclopedia of Signaling Molecules

2018 Edition
| Editors: Sangdun Choi

SHIP2

  • Christophe Erneux
  • Stéphane Schurmans
Reference work entry
DOI: https://doi.org/10.1007/978-3-319-67199-4_101857

Synonyms

Historical Background

Inositol polyphosphate 5-phosphatase or phosphoinositide 5-phosphatases (or PI 5-phosphatases) are enzymes that can act on inositol phosphates and/or phosphoinositides (PIs) as substrates to dephosphorylate the phosphate at 5 position of the inositol ring (Balla 2013). In human, it consists in a family of ten different isoenzymes (Blero et al. 2007). One of the first isoenzyme to be cloned was OCRL1 which is mutated in the Lowe syndrome and Dent-2 disease (Attree et al. 1992). Our interest in the family of PI 5-phosphatases originated from the cloning of INPP5A (i.e., type 1 inositol 1,4,5-trisphosphate 5-phosphatase), a phosphatase that can act on soluble inositol phosphates, i.e., Ins(1,4,5)P3 and Ins(1,3,4,5)P4 as substrate. At that time, its catalytic domain showed some sequence similarity with OCRL1 and another PI 5-phosphatase INPP5B that was identified by the group of Majerus....
This is a preview of subscription content, log in to check access.

References

  1. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  2. Awad A, Sar S, Barre R, Cariven C, Marin M, Salles JP, Erneux C, Samuel D, Gassama-Diagne A. SHIP2 regulates epithelial cell polarity through its lipid product that binds to Dlg1, a pathway subverted by Hepatitis C virus core protein. Mol Biol Cell. 2013;24:2171–85.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Balla T. Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev. 2013;93:1019–137.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Below JE, Earl DL, Shively KM, McMillin MJ, Smith JD, Turner EH, Stephan MJ, Al-Gazali LI, Hertecant JL, Chitayat D, et al. Whole-genome analysis reveals that mutations in inositol polyphosphate phosphatase-like 1 cause opsismodysplasia. Am J Hum Genet. 2013;92:137–43.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Blero D, Zhang J, Pesesse X, Payrastre B, Dumont JE, Schurmans S, Erneux C. Phosphatidylinositol 3,4,5-trisphosphate modulation in SHIP2-deficient mouse embryonic fibroblasts. FEBS J. 2005;272:2512–22.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Blero D, Payrastre B, Schurmans S, Erneux C. Phosphoinositide phosphatases in a network of signalling reactions. Pflugers Arch. 2007;455:31–44.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, et al. The lipid phosphatase SHIP2 controls insulin sensitivity. Nature. 2001;409:92–7.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, et al. Corrigendum: the lipid phosphatase SHIP2 controls insulin sensitivity. Nature. 2005;431:878.CrossRefGoogle Scholar
  9. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  11. Dubois E, Jacoby M, Blockmans M, Pernot E, Schiffmann SN, Foukas LC, Henquin JC, Vanhaesebroeck B, Erneux C, Schurmans S. Developmental defects and rescue from glucose intolerance of a catalytically-inactive novel Ship2 mutant mouse. Cell Signal. 2012;24:1971–80.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Elong Edimo W, Ghosh S, Derua R, Janssens V, Waelkens E, Vanderwinden JM, Robe P, Erneux C. SHIP2 controls plasma membrane PI(4,5)P2 thereby participating in the control of cell migration in 1321 N1 glioblastoma. J Cell Sci. 2016;129:1101–14.PubMedPubMedCentralCrossRefGoogle Scholar
  14. Erneux C, Edimo WE, Deneubourg L, Pirson I. SHIP2 multiple functions: a balance between a negative control of PtdIns(3,4,5)P3 level, a positive control of PtdIns(3,4)P2 production, and intrinsic docking properties. J Cell Biochem. 2011;112:2203–9.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Fradet A, Fitzgerald J. INPPL1 gene mutations in opsismodysplasia. J Hum Genet. 2017;62:135–40.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  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.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Giuriato S, Pesesse X, Bodin S, Sasaki T, Viala C, Marion E, Penninger J, Schurmans S, Erneux C, Payrastre B. SH2-containing inositol 5-phosphatases 1 and 2 in blood platelets: their interactions and roles in the control of phosphatidylinositol 3,4,5-trisphosphate levels. Biochem J. 2003;376:199–207.PubMedPubMedCentralCrossRefGoogle Scholar
  19. Hejna JA, Saito H, Merkens LS, Tittle TV, Jakobs PM, Whitney MA, Grompe M, Friedberg AS, Moses RE. Cloning and characterization of a human cDNA (INPPL1) sharing homology with inositol polyphosphate phosphatases. Genomics. 1995;29:285–7.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Hoekstra E, Das AM, Willemsen M, Swets M, Kuppen PJ, van der Woude CJ, Bruno M J, Shah JP, Ten Hagen TL, Chisholm JD, et al. Lipid phosphatase SHIP2 functions as oncogene in colorectal cancer by regulating PKB activation. Oncotarget. 2016;7:73525–40.Google Scholar
  21. Huber C, Faqeih EA, Bartholdi D, Bole-Feysot C, Borochowitz Z, Cavalcanti DP, Frigo A, Nitschke P, Roume J, Santos HG, et al. Exome sequencing identifies INPPL1 mutations as a cause of opsismodysplasia. Am J Hum Genet. 2013;92:144–9.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Jurynec MJ, Grunwald DJ. SHIP2, a factor associated with diet-induced obesity and insulin sensitivity, attenuates FGF signaling in vivo. Dis Model Mech. 2010;3:733–42.PubMedPubMedCentralCrossRefGoogle Scholar
  23. Nakatsu F, Perera RM, Lucast L, Zoncu R, Domin J, Gertler FB, Toomre D, De Camilli P. The inositol 5-phosphatase SHIP2 regulates endocytic clathrin-coated pit dynamics. J Cell Biol. 2010;190(3):307–15.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Oikawa T, Takenawa T. PtdIns(3,4)P2 instigates focal adhesions to generate podosomes. Cell Adhes Migr. 2009;3:195–7.CrossRefGoogle Scholar
  25. 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.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Pesesse X, Moreau C, Drayer AL, Woscholski R, Parker P, Erneux C. The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5- tetrakisphosphate 5-phosphatase activity. FEBS Lett. 1998;437:301–3.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Prasad NK, Tandon M, Handa A, Moore GE, Babbs CF, Snyder PW, Bose S. High expression of obesity-linked phosphatase SHIP2 in invasive breast cancer correlates with reduced disease-free survival. Tumour Biol. 2008;29:330–41.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Rajadurai CV, Havrylov S, Coelho PP, Ratcliffe CD, Zaoui K, Huang BH, Monast A, Chughtai N, Sangwan V, Gertler FB, et al. 5’-Inositol phosphatase SHIP2 recruits Mena to stabilize invadopodia for cancer cell invasion. J Cell Biol. 2016;214:719–34.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Sasaoka T, Wada T, Tsuneki H. Lipid phosphatases as a possible therapeutic target in cases of type 2 diabetes and obesity. Pharmacol Ther. 2006;112:799–809.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Sharma VP, Eddy R, Entenberg D, Kai M, Gertler FB, Condeelis J. Tks5 and SHIP2 regulate invadopodium maturation, but not initiation, in breast carcinoma cells. Curr Biol. 2013;23:2079–89.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Sleeman MW, Wortley KE, Lai KMV, Gowen LC, Kintner J, Kline WO, Garcia K, Stitt TN, Yancopoulos GD, Wiegand SJ, et al. Absence of the lipid phosphatase SHIP2 confers resistance to diary obesity. Nat Med. 2005;11:199–205.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Taylor V, Wong M, Brandts C, Reilly L, Dean NM, Cowsert LM, Moodie S, Stokoe D. 5’ phospholipid phosphatase SHIP-2 causes protein kinase B inactivation and cell cycle arrest in glioblastoma cells. Mol Cell Biol. 2000;20:6860–71.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 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.PubMedPubMedCentralGoogle Scholar
  34. Xie J, Vandenbroere I, Pirson I. SHIP2 associates with intersectin and recruits it to the plasma membrane in response to EGF. FEBS Lett. 2008;582:3011–7.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Xie J, Erneux C, Pirson I. How does SHIP1/2 balance PtdIns(3,4)P2 and does it signal independently of its phosphatase activity? BioEssays. 2013;35:733–43.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM)Université Libre de Bruxelles (ULB)BrusselsBelgium
  2. 2.Laboratoire de Génétique Fonctionnelle, GIGA-Research CentreUniversité de Liège (ULg)LiègeBelgium