SH2 domain containing inositol 5-phosphatases 1 and 2 in blood platelets: interaction and respective role in the control of phosphatidylinositol 3,4,5-trisphosphate levels
[en] Src homology domain 2-containing inositol 5-phosphatases 1 and 2 (SHIP1 and SHIP2) are capable of dephosphorylating the second messenger PtdIns(3,4,5) P3 (phosphatidylinositol 3,4,5-trisphosphate) and interacting with several signalling proteins. SHIP1 is essentially expressed in haematopoietic cells, whereas SHIP2, a closely related enzyme, is ubiquitous. In the present study, we show that SHIP1 and SHIP2 are expressed as functional PtdIns(3,4,5) P3 5-phosphatases in human blood platelets and are capable of interacting when these two lipid phosphatases are co-expressed, either naturally (platelets and A20 B lymphoma cells) or artificially (COS-7 cells). Using COS-7 cells transfected with deletion mutants of SHIP2, we demonstrate that the Src homology domain 2 of SHIP2 is the minimal and sufficient protein motif responsible for the interaction between the two phosphatases. These results prompted us to investigate the relative importance of SHIP1 and SHIP2 in the control of PtdIns(3,4,5) P3 levels in platelets using homozygous or heterozygous SHIP1- or SHIP2-deficient mice. Our results strongly suggest that SHIP1, rather than SHIP2, plays a major role in controlling PtdIns(3,4,5) P3 levels in response to thrombin or collagen activation of mouse blood platelets
Giuriato, S.; INSERM U563, Hôpital Purpan, 31059 Toulouse Cedex, France > Department of Oncogenesis and Signaling in Hematopoietic Cells, IFR30, Hˆopital Purpan, 31059 Toulouse Cedex, France
Pesesse, X.; Université Libre de Bruxelles - ULB > IRIBHM
Bodin, S.; INSERM U563, Hôpital Purpan, 31059 Toulouse Cedex, France > Department of Oncogenesis and Signaling in Hematopoietic Cells, IFR30
Sasaki, T.; Akita University School of Medicine, 1-1-1 Hondo, 010-8543, Akita, Japan, > The 21st Century Center of Excellence (COE) Program
Viala, C.; INSERM U563, Hôpital Purpan, 31059 Toulouse Cedex, France > Department of Oncogenesis and Signaling in Hematopoietic Cells, IFR30
Marion, E.; Université Libre de Bruxelles - ULB > Centre de Recherche en Biotechnologie, Interdisciplinary Research Institute (IRIBHM)
Penninger, J.; Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Dr Bohr Gasse 7, 1030 Vienna, Austria
Schurmans, Stéphane ; Université de Liège - ULiège > Département de sciences fonctionnelles > Biochimie métabolique vétérinaire
Erneux, C.; Université Libre de Bruxelles - ULB > IRIBHM
Payrastre, B.; INSERM U563, Hôpital Purpan, 31059 Toulouse Cedex, France > Department of Oncogenesis and Signaling in Hematopoietic Cells, IFR30
Language :
English
Title :
SH2 domain containing inositol 5-phosphatases 1 and 2 in blood platelets: interaction and respective role in the control of phosphatidylinositol 3,4,5-trisphosphate levels
Publication date :
2003
Journal title :
Biochemical Journal
ISSN :
0264-6021
eISSN :
1470-8728
Publisher :
Portland Press, London, United Kingdom
Volume :
376
Pages :
199-207
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
FRSM - Fonds de la Recherche Scientifique Médicale INSERM - Institut National de la Santé et de la Recherche Médicale CFB - Communauté française de Belgique Fondation ARC pour la Recherche sur le Cancer
Funding text :
This work was supported by the CEE BIOMED 2 contract no. PL962609, by grants from Action de Recherche Concertée (Communauté française de Belgique Wallonie, Bruxelles, Belgium), Fonds de la Recherche Scientifique Médicale, Association pour la Recherche sur le Cancer (Villejuif, France; contract no. 4794 and ARECA-Toulouse) and the INSERM–Communauté française de Belgique exchange contract.
Erneux, C., Govaerts, C., Communi, D. and Pesesse, X. (1998) The diversity and possible functions of the inositol polyphosphate 5-phosphatases. Biochim. Biophys. Acta 1436, 185-199
Drayer, A. L., Pesesse, X., De Smedt, F., Woscholski, R., Parker, P. and Erneux, C. (1996) 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. 225, 243-249
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
Rohrschneider, L. R., Fuller, J. F., Wolf, I., Liu, Y. and Lucas, D. M. (2000) Structure, function, and biology of SHIP proteins. Genes Dev. 14, 505-520
Liu, Q., Oliveira-Dos-Santos, A. J., Mariathasan, S., Bouchard, D., Jones, J., Sarao, R., Kozieradzki, I., Ohashi, P. S., Penninger, J. M. and Dumont, D. J. (1998) The inositol polyphosphate 5-phosphatase ship is a crucial negative regulator of B cell antigen receptor signaling. J. Exp. Med. 188, 1333-1342
Liu, Q., Sasaki, T., Kozieradzki, I., Wakeham, A., Itie, A., Dumont, D. J. and Penninger, J. M. (1999) SHIP is a negative regulator of growth factor receptor-mediated PKB/Akt activation and myeloid cell survival. Genes Dev. 13, 786-791
Huber, M., Helgason, C. D., Scheid, M. P., Duronio, V., Humphries, R. K. and Krystal, G. (1998) Targeted disruption of SHIP leads to Steel factor-induced degranulation of mast cells. EMBO J. 17, 7311-7319
Valderrama-Carvajal, H., Cocolakis, E., Lacerte, A., Lee, E. H., Krystal, G., Ali, S. and Lebrun, J. J. (2002) Activin/TGF-β induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nat. Cell Biol. 4, 963-969
Helgason, C. D., Damen, J. E., Rosten, P., Grewal, R., Sorensen, P., Chappel, S. M., Borowski, A., Jirik, F., Krystal, G. and Humphries, R. K. (1998) Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 12, 1610-1620
Huber, M., Helgason, C. D., Damen, J. E., Scheid, M., Duronio, V., Liu, L., Ware, M. D., Humphries, R. K. and Krystal, G. (1999) The role of SHIP in growth factor induced signalling. Prog. Biophys. Mol. Biol. 71, 423-434
Luo, J. M., Yoshida, H., Komura, S., Ohishi, N., Pan, L., Shigeno, K., Hanamura, I., Miura, K., Iida, S., Ueda, R. et al. (2003) Possible dominant-negative mutation of the SHIP gene in acute myeloid leukemia. Leukemia 17, 1-8
Sattler, M., Verma, S., Byrne, C. H., Shrikhande, G., Winkler, T., Algate, P. A., Rohrschneider, L. R. and Griffin, J. D. (1999) BCR/ABL directly inhibits expression of SHIP, an SH2-containing polyinositol-5-phosphatase involved in the regulation of hematopoiesis. Mol. Cell. Biol. 19, 7473-7480
Rey-Ladino, J. A., Huber, M., Liu, L., Damen, J. E., Krystal, G. and Takei, F. (1999) The SH2-containtng inositol-5′-phosphatase enhances LFA-1-mediated cell adhesion and defines two signaling pathways for LFA-1 activation. J. Immunol. 162, 5792-5799
Mancini, A., Koch, A., Wilms, R. and Tamura, T. (2002) The SH2-containing inositol 5-phosphatase (SHIP)-1 is implicated in the control of cell-cell junction and induces dissociation and dispersion of MDCK cells. Oncogene 21, 1477-1484
Wang, J. W., Howson, J. M., Ghansah, T., Desponts, C., Ninos, J. M., May, S. L., Nguyen, K. H., Toyama-Sorimachi, N. and Kerr, W. G. (2002) Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science 295, 2094-2097
Takeshita, S., Namba, N., Zhao, J. J., Jiang, Y., Genant, H. K., Silva, M. J., Brodt, M. D., Helgason, C. D., Kalesnikoff, J., Rauh, M. J. et al. (2002) SHIP-deficient mice are severely osteoporotic due to increased numbers of hyper-resorptive osteoclasts. Nat. Med. (Tokyo) 8, 943-949
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
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
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
Giuriato, S., Blero, D., Robaye, B., Bruyns, C., Payrastre, B. and Erneux, C. (2002) SHIP2 overexpression strongly reduces the proliferation rate of K562 erythroleukemia cell line. Biochem. Biophys. Res. Commun. 296, 106-110
Prasad, N., Topping, R. S. and Decker, S. J. (2001) SH2-containing inositol 5′-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading. Mol. Cell. Biol, 21, 1416-1428
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
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 (London) 409, 92-97
Giuriato, S., Payrastre, B., Drayer, A. L., Plantavid, M., Woscholski, R., Parker, P., Erneux, C. and Chap, H. (1997) Tyrosine phosphorylation and relocation of SHIP are integrin-mediated in thrombin-stimulated human blood platelets. J. Biol. Chem. 272, 26857-26863
Giuriato, S., Bodin, S., Erneux, C., Woscholski, R., Plantavid, M., Chap, H. and Payrastre, B. (2000) pp60c-src associates with the SH2-containing inositol-5-phosphatase SHIP1 and is involved in its tyrosine phosphorylation downstream of αIIbβ3 integrin in human platelets. Biochem. J. 348, 107-112
Trumel, C., Payrastre, B., Plantavid, M., Hechler, B., Viala, C., Presek, P., Martinson, E. A., Cazenave, J. P., Chap, H. and Cachet, C. (1999) A key role of adenosine diphosphate in the irreversible platelet aggregation induced by the PAR1-activating peptide through the late activation of phosphoinositide 3-kinase. Blood 94, 4156-4165
Pasquet, J. M., Quek, L., Stevens, C., Bobe, R., Huber, M., Duronio, V., Krystal, G. and Watson, S. P. (2000) Phosphatidylinositol 3,4,5-trisphosphate regulates Ca2+ entry via btk in platelets and megakaryocytes without increasing phospholipase C activity. EMBO J. 19, 2793-2802
Bruyns, C., Pesesse, X., Moreau, C., Blero, D. and Erneux, C. (1999) The two SH2-domain-containing inositol 5-phosphatases SHIP1 and SHIP2 are coexpressed in human T lymphocytes. Biol. Chem. 380, 969-974
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
Muraille, E., Bruhns, P., Pesesse, X., Daeron, M. and Erneux, C. (2000) The SH2 domain containing inositol 5-phosphatase SHIP2 associates to the immunoreceptor tyrosine-based inhibition motif of Fcγ RIIB in B cells under negative signaling. Immunol. Lett. 72, 7-15
Bruhns, P., Vely, F., Malbec, O., Fridman, W. H., Vivier, E. and Daeron, M. (2000) Molecular basis ot the recruitment of the SH2 domain-containing inositol 5-phosphatases SHIP1 and SHIP2 by fcγ RIIB. J. Biol. Chem. 275, 37357-37364
Brauweiler, A., Tamir, I., Marschner, S., Helgason, C. D. and Cambier, J. C. (2001) Partially distinct molecular mechanisms mediate inhibitory FcγRIIB signaling in resting and activated B cells. J. Immunol. 167, 204-211
Scheid, M. P., Huber, M., Damen, J. E., Hughes, M., Kang, V., Neilsen, P., Prestwich, G. D., Krystal, G. and Duronio, V. (2002) 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. 277, 9027-9035
Cazenave, J. P., Hemmendinger, S., Beretz, A., Sutter-Bay, A. and Launay, J. (1983) Platelet aggregation: a tool for clinical investigation and pharmacological study. Methodology. Ann. Biol. Clin. (Paris) 41, 167-179
Bligh, E. G. and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
Gratacap, M. P., Payrastre, B., Viala, C., Mauco, G., Plantavid, M. and Chap, H. (1998) Phosphatidylinositol 3,4,5-trisphosphate-dependent stimulation of phospholipase C-γ2 is an early key event in FcγRIIA-mediated activation of human platelets. J. Biol. Chem. 273, 24314-24321
Pesesse, X., Moreau, C., Drayer, A. L., Woscholski, R., Parker, P. and Erneux, C. (1998) The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosptiate 5-phosphatase activity. FEBS Lett. 437, 301-303
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
Payrastre, B., Missy, K., Giuriato, S., Bodin, S., Plantavid, M. and Gratacap, M. (2001) Phosphoinositides: key players in cell signalling, in time and space. Cell. Signal. 13, 377-387
Damen, J. E., Liu, L., Ware, M. D., Ermolaeva, M., Majerus, P. W. and Krystal, G. (1998) Multiple forms of the SH2-containing inositol phosphatase, SHIP, are generated by C-terminal truncation. Blood 92, 1199-1205
Horn, S., Meyer, J., Heukeshoven, J., Fehse, B, Schulze, C., Li, S., Frey, J., Poll, S., Stocking, C. and Jucker, M. (2001) The inositol 5-phosphatase SHIP is expressed as 145 and 135 kDa proteins in blood and bone marrow cells in vivo, whereas carboxyltruncated forms of SHIP are generated by proteolytic cleavage in vitro. Leukemia 15, 112-120
Dyson, J. M., Munday, A. D., Kong, A. M., Huysmans, R. D., Matzaris, M., Layton, M. J., Nandurkar, H. H., Berndt, M. C. and Mitchell, C. A. (2003) SHIP-2 forms a tetrameric complex with filamin, actin, and GPIb-IX-V: localization of SHIP-2 to the activated platelet actin cytoskeleton. Blood 102, 940-948
Osborne, M. A., Zenner, G., Lubinus, M., Zhang, X., Songyang, Z., Cantley, L. C., Majerus, P., Burn, P. and Kochan, J. P. (1996) The inositol 5′-phosphatase SHIP binds to immunoreceptor signaling motifs and responds to high affinity IgE receptor aggregation. J. Biol. Chem. 271, 29271-29278
Tridandapani, S., Pradhan, M., LaDine, J. R., Garber, S., Anderson, C. L. and Coggeshall, K. M. (1999) Protein interactions of Src homology 2 (SH2) domain-containing inositol phosphatase (SHIP): association with Shc displaces SHIP from FcγRIIb in B cells. J. Immunol. 162, 1408-1414
Hinchliffe, K. A., Giudici, M. L., Letcher, A. J. and Irvine, R. F. (2002) Type IIα phosphatidylinositol phosphate kinase associates with the plasma membrane via interaction with type I isoforms. Biochem. J. 363, 563-570
Jackson, S. P., Schoenwaelder, S. M., Matzaris, M., Brown, S. and Mitchell, C. A. (1995) Phosphatidylinositol 3,4,5-trisphosphate is a substrate for the 75 kDa inositol polyphosphate 5-phosphatase and a novel 5-phosphatase which forms a complex with the p85/p110 form of phosphoinositide 3-kinase. EMBO J. 14, 4490-4500
Zhang, J., Banfic, H., Straforini, F., Tosi, L., Volinia, S. and Rittenhouse, S. E. (1998) A type II phosphoinositide 3-kinase is stimulated via activated integrin in platelets. A source of phosphatidylinositol 3-phosphate. J. Biol. Chem. 273, 14081-14084