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Thromb Haemost 1997; 77(01): 150-154
DOI: 10.1055/s-0038-1655923
Platelets
Schattauer GmbH Stuttgart

Protein Tyrosine Phosphatase SHP-1 Fails to Associate with Cytoskeleton but is Normally Phosphorylated upon Thrombin Stimulation of Thrombasthenic Platelets

Ruo Ya Li
1   The Institut Fédératif de Recherche en Immunologie Cellulaire et Moléculaire, Université Paul Sabatier and Centre Hospitalo-Universitaire de Toulouse, INSERM Unité 326, Phospholipides Membranaires, Signalisation Cellulaire et Lipoproteines, Hôpital Purpan, Toulouse, France
,
Frédérique Gaits
1   The Institut Fédératif de Recherche en Immunologie Cellulaire et Moléculaire, Université Paul Sabatier and Centre Hospitalo-Universitaire de Toulouse, INSERM Unité 326, Phospholipides Membranaires, Signalisation Cellulaire et Lipoproteines, Hôpital Purpan, Toulouse, France
,
Jeannie M F Ragab-Thomas
1   The Institut Fédératif de Recherche en Immunologie Cellulaire et Moléculaire, Université Paul Sabatier and Centre Hospitalo-Universitaire de Toulouse, INSERM Unité 326, Phospholipides Membranaires, Signalisation Cellulaire et Lipoproteines, Hôpital Purpan, Toulouse, France
,
Jacques Maclouf
2   INSERM Unite 348, Physiopathologie Cellulaire et Moléculaire des Cellules du Sang et des Vaisseaux, Hôpital Lariboisiére, Paris
,
Jacques P Caen
3   Institut des Vaisseaux et du Sang, Hôpital Lariboisiére, Paris, France
,
Sylviane Lévy-Toledano
2   INSERM Unite 348, Physiopathologie Cellulaire et Moléculaire des Cellules du Sang et des Vaisseaux, Hôpital Lariboisiére, Paris
,
Hugues Chap
1   The Institut Fédératif de Recherche en Immunologie Cellulaire et Moléculaire, Université Paul Sabatier and Centre Hospitalo-Universitaire de Toulouse, INSERM Unité 326, Phospholipides Membranaires, Signalisation Cellulaire et Lipoproteines, Hôpital Purpan, Toulouse, France
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Publication History

Received 08 August 1996

Accepted after revision 08 October 1996

Publication Date:
11 July 2018 (online)

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Summary

SHP-1 is a cytoplasmic protein tyrosine phosphatase predominantly expressed in hematopoietic cells. Upon thrombin stimulation of human platelets, SHP-1 is rapidly phosphorylated on both serine and tyrosine residues, and becomes associated with the cytoskeleton, where it could participate in the formation of multiprotein signalling complexes. In order to discriminate between signalling events occurring downstream of G-protein-coupled thrombin receptor and those subsequent to integrin αIIbβ3engagement, SHP-1 behaviour was examined in platelets from two patients lacking integrin αIIbβ3 (Glanzmann’s thrombasthenia). Upon thrombin stimulation, phosphorylation of SHP-1 occurred normally in thrombasthenic platelets, whereas association with the cytoskeleton was abolished. Moreover, inhibition of normal platelet aggregation with the tetrapeptide arg-gly-asp-ser (RGDS), which impairs fibrinogen binding to integrin aIIb(33, did not alter significantly SHP-1 phosphorylation. It is concluded that SHP-1 phosphorylation is not a consequence of integrin signalling but might rather occur downstream of thrombin receptor and heterotrimeric G-proteins.

 

  • References

  • 1 Clark EA, Shattil SJ, Brugge JS. Regulation of protein tyrosine kinases in platelets. Trends Biochem Sci 1994; 19: 464-469
    CrossrefPubMedGoogle Scholar
  • 2 Golden A, Nemeth S, Brugge JS. Blood platelets express high levels of the pp60c'src-specific protein tyrosine kinase. Proc Natl Acad Sci USA 1986; 83: 852-856
    CrossrefPubMedGoogle Scholar
  • 3 Huang MM, Bolen JB, Barnwell JW, Shattil SJ, Brugge JS. Membrane glycoprotein IV (CD36) is physically associated with the fyn lyn, and yes protein tyrosine kinases in platelets. Proc Natl Acad Sci USA 1991; 88: 7844-7848
    CrossrefPubMedGoogle Scholar
  • 4 Lipfert L, Haimovich B, Schaller MD, Cobb BS, Parsons JT, Brugge J. Integrin-dependent phosphorylation and activation of the protein tyrosine kinase ppl25FAKin platelets. J Cell Biol 1992; 119: 905-909
    CrossrefPubMedGoogle Scholar
  • 5 Shattil S, Haimovitch B, Cunningham M, Lipfert L, Parsons JT, Ginsberg MH, Brugge JS. Tyrosine phosphorylation of ppl25FAKin platelets requires coordinated signalling through integrin and agonist receptors. J Biol Chem 1994; 269: 14738-14745
    PubMedGoogle Scholar
  • 6 Taniguchi T, Kitagawa H, Yanagi S, Sakai K, Asahi M, Ohta S, Takeuchi F, Nakamura SL, Yamamura H. Protein tyrosine kinase p72 syk is activated by thrombin and is negatively regulated through Ca2+ mobilization in platelets. J Biol Chem 1993; 268: 2277-2279
    PubMedGoogle Scholar
  • 7 Bennett DD, Cowley S, Jiang S, London R, Deng B, Grabarek J, Groopman JE, Goeddel DV, Avraham H. Identification and characterization of a novel tyrosine kinase from megakaryocytes. J Biol Chem 1994; 269: 1068-1074
    PubMedGoogle Scholar
  • 8 Turner M, Mee PJ, Costello PS, Williams O, Price AA, Duddy LP, Furlong MT, Geahlen RL, Tybulewicz VLJ. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 1995; 378: 298-302
    CrossrefPubMedGoogle Scholar
  • 9 Cheng AM, Rowley B, Pao W, Hayday A, Bolen JB, Pawson T. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 1995; 378: 303-306
    CrossrefPubMedGoogle Scholar
  • 10 Frangioni JV, Oda A, Smith M, Salzman EW, Neel BG. Calpain-catalyzed cleavage and subcellular relocation of protein tyrosine phosphatase IB (PTP-IB) in human platelets. EMBO J 1993; 12: 4843-4856
    PubMedGoogle Scholar
  • 11 Gu M, York JD, Warshawsky I, Majerus PW. Identification, cloning and expression of a cytosolic megakaryocyte protein-tyrosine phosphatase with sequence homology to cytoskeletal protein 4.1. Proc Natl Acad Sci USA 1991; 88: 5867-5871
    CrossrefPubMedGoogle Scholar
  • 12 Yang Q, Tonks NK. Isolation of a cDNA clone encoding a human protein- tyrosine phosphatase with homology to the cytoskeletal associated proteins band 4.1, ezrin and talin. Proc Natl Acad Sci USA 1991; 88: 5949-5953
    CrossrefPubMedGoogle Scholar
  • 13 Li RY, Gaits F, Ragab A, Ragab-Thomas JMF, Chap H. Translocation of an SH2-containing protein tyrosine phosphatase (SH-PTP1) to the cytoskeleton of thrombin-activated platelets. FEBS Lett 1994; 343: 89-93
    CrossrefPubMedGoogle Scholar
  • 14 Li RY, Gaits F, Ragab A, Ragab-Thomas JMF, Chap H. Tyrosine phosphorylation of an SH2-containing protein tyrosine phosphatase is coupled to platelet thrombin receptor via a pertussis toxin-sensitive heterotrimeric G-protein. EMBO J 1995; 14: 2519-2526
    PubMedGoogle Scholar
  • 15 Ezumi Y, Takayama H, Okuma M. Differential regulation of protein-tyrosine phosphatases by integrinαIIbβ3 through cytoskeletal reorganization and tyrosine phosphorylation in human platelets. J Biol Chem 1995; 270: 11927-11934
    CrossrefPubMedGoogle Scholar
  • 16 Falet H, Ramos-Morales F, Bachelot C, Fischer S, Rendu F. Association of the protein tyrosine phosphatase PTP 1C with the protein tyrosine kinase c-Src in human platelets. FEBS Lett 1996; 383: 165-169
    CrossrefPubMedGoogle Scholar
  • 17 Adachi M, Fischer EJ, Ihle J, Imai K, Jirik F, Neel B, Pawson T, Shen SH, Thomas M, Ullrich A, Zhao Z. Mammalian SH2-containing protein tyrosine phosphatases. Cell 1996; 85: 15
    CrossrefPubMedGoogle Scholar
  • 18 Stone RL, Dixon JE. Protein tyrosine phosphatases. J Biol Chem 1994; 269: 21323-21236
    PubMedGoogle Scholar
  • 19 Shultz LD, Schweitzer PA, Rajan TV, Yi T, Ihle JN, Matthews RJ, Thomas ML, Beier DR. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 1993; 73: 1445-1454
    CrossrefPubMedGoogle Scholar
  • 20 Kozlowski M, Mlinaric-Rascan I, Feng GS, Shen R, Pawson T, Siminovitch KA. Expression and catalytic activity of the tyrosine phosphatase PTP 1C is severely impaired in motheaten and viable motheaten mice. J Exp Med 1993; 178: 2157-2163
    CrossrefPubMedGoogle Scholar
  • 21 Klingmuller U, Lorenz U, Cantley LC, Neel BG, Lodish HF. Specific recruitment of SH-PTP1 to the erythropoietin receptor causes inactivation of JAK2 and termination of proliferative signals. Cell 1995; 80: 729-738
    CrossrefPubMedGoogle Scholar
  • 22 Clark EA, Brugge JS. Redistribution of activated pp60c srcto the integrin- dependent cytoskeletal complexes in thrombin-stimulated platelets. Mol' Cell Biol 1993; 13: 1863-1871
    PubMedGoogle Scholar
  • 23 Grondin P, Plantavid M, Sultan C, Breton M, Mauco G, Chap H. Interaction of pp60c'src, phospholipase inositol-lipid and diacylglycerol kinases with the cytoskeletons of thrombin-stimulated platelets. J Biol Chem 1991; 266: 15705-15709
    PubMedGoogle Scholar
  • 24 Zhang J, Fry MY, Waterfield MD, Jaken S, Liao L, Fox JEB, Ritten- house SE. Activated phosphoinositide 3-kinase associates with membrane skeleton in thrombin-exposed platelets. J Biol Chem 1992; 267: 4686-4692
    PubMedGoogle Scholar
  • 25 Horvath AR, Muszbeck L, Kellie S. Translocation of pp60c-srcto the cytoskeleton during platelet aggregation. EMBO J 1992; 11: 855-861
    PubMedGoogle Scholar
  • 26 Oda A, Druker BY, Smith M, Salzman EW. Association of pp60c-srcwith Triton X-100 insoluble residue in human blood platelets requires platelet aggregation and actin polymerization. J Biol Chem 1992; 267: 20075-20081
    PubMedGoogle Scholar
  • 27 Guinebault C, Payrastre B, Racaud-Sultan C, Mazarguil H, Breton M, Mauco G, Plantavid M, Chap H. Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interaction of p85α with actin filaments and focal adhesion kinase. J Cell Biol 1995; 129: 831-842
    CrossrefPubMedGoogle Scholar
  • 28 Ferrell JE, Martin GS. Tyrosine-specific phosphorylation is regulated by glycoprotein Ilb-IIIa in platelets. Proc Natl Acad Sci USA 1989; 86: 2234-2238
    CrossrefPubMedGoogle Scholar
  • 29 Golden A, Brugge JS, Shattil S. Role of platelet membrane glycoprotein IIb-IIIa in agonist-induced tyrosine phosphorylation of platelet protein. J Cell Biol 1990; 111: 3117-3127
    CrossrefPubMedGoogle Scholar
  • 30 Sultan C, Plantavid M, Bachelot C, Grondin P, Breton M, Mauco G, Lévy-Toledano S, Caen JP, Chap H. Involvement of platelet glycoprotein IIb-IIIa (αIIb β3integrin) in thrombin-induced synthesis of phosphatidylinositol 3’,4’-bisphosphate. J Biol Chem 1991; 266: 23554-23557
    PubMedGoogle Scholar
  • 31 George J, Caen JP, Nurden A. Glanzmann thrombasthenia: the spectrum of clinical disease. Blood 1990; 75: 1383-1395
    CrossrefPubMedGoogle Scholar
  • 32 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685
    CrossrefPubMedGoogle Scholar
  • 33 Pho DB, Vasseur C, Desbruyeres E, Olomucki A. Evidence for the presence of tropomyosin in the cytoskeletons of ADP- and thrombin-stimulated blood platelets. FEBS Lett 1984; 173: 164-168
    CrossrefPubMedGoogle Scholar
  • 34 Gaits F, Li RY, Bigay J, Ragab A, Ragab-Thomas JMF. Chap H: G-protein βϒ subunits mediate specific phosphorylation of the protein tyrosine phosphatase SH-PTP1 induced by lysophosphatidic acid. J Biol Chem 1996; 271: 20151-20155
    PubMedGoogle Scholar
  • 35 Pumiglia KM, Lau LF, Huang CK, Burroughs S, Feinstein MB. Activation of signal transduction in platelets by the tyrosine phosphatase inhibitor pervanadate (vanadyl hydroperoxide). Biochem J 1992; 286: 441-449
    CrossrefPubMedGoogle Scholar
  • 36 Behnke O. Blood platelet heterogeneity: a functional hierarchy in the platelet population. Brit J Haematol 1995; 91: 991-999
    CrossrefPubMedGoogle Scholar