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Original Article

Mouse podoplanin supports adhesion and aggregation of platelets under arterial shear: A novel mechanism of haemostasis

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Pages 716-722 | Received 26 Apr 2017, Accepted 28 Jun 2017, Published online: 01 Nov 2017

References

  • Suzuki-Inoue K. CLEC-2, the novel platelet activation receptor and its internal ligand, podoplanin. Rinsho Ketsueki 2009;50:389–398.
  • Lowe KL, Navarro-Núñez L, Bénézech C, Nayar S, Kingston BL, Nieswandt B, Barone F, Watson SP, Buckley CD, Desanti GE. The expression of mouse CLEC-2 on leucocyte subsets varies according to their anatomical location and inflammatory state. Eur J Immunol 2015;45:2484–2493. doi:10.1002/eji.201445314.
  • Hughes CE, Sinha U, Pandey A, Eble JA, O’Callaghan CA, Watson SP. Critical role for an acidic amino acid region in platelet signaling by the HemITAM (hemi-immunoreceptor tyrosine-based activation motif) containing receptor CLEC-2 (C-type lectin receptor-2). J Biol Chem 2013;288:5127–5135.
  • Spalton JC, Mori J, Pollitt AY, Hughes CE, Eble JA, Watson SP. The novel Syk inhibitor R406 reveals mechanistic differences in the initiation of GPVI and CLEC-2 signaling in platelets. Jth 2009;7:1192–1199.
  • Severin S, Pollitt AY, Navarro-Nunez L, Nash CA, Mourao-Sa D, Eble JA, Senis YA, Watson SP. Syk-dependent phosphorylation of CLEC-2: a novel mechanism of hem-immunoreceptor tyrosine-based activation motif signaling. J Biol Chem 2011;286:4107–4116.
  • Pollitt AY, Grygielska B, Leblond B, Desire L, Eble JA, Watson SP. Phosphorylation of CLEC-2 is dependent on lipid rafts, actin polymerization, secondary mediators, and Rac. Blood 2010;115:2938–2946.
  • Suzuki-Inoue K, Fuller GL, Garcia A, Eble JA, Pohlmann S, Inoue O, Gartner TK, Hughan SC, Pearce AC, Laing GD, Theakston RD, Schweighoffer E, Zitzmann N, Morita T, Tybulewicz VL, Ozaki Y, Watson SP. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 2006;107:542–549.
  • Suzuki-Inoue K, Kato Y, Inoue O, Kaneko MK, Mishima K, Yatomi Y, Yamazaki Y, Narimatsu H, Ozaki Y. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem 2007;282:25993–26001.
  • Finney BA, Schweighoffer E, Navarro-Nunez L, Benezech C, Barone F, Hughes CE, Langan SA, Lowe KL, Pollitt AY, Mourao-Sa D, Sheardown S, Nash GB, Smithers N, Reis E Sousa C, Tybulewicz VL, Watson SP. CLEC-2 and Syk in the megakaryocytic/platelet lineage are essential for development. Blood 2012;119:1747–1756.
  • Lowe KL, Finney BA, Deppermann C, Hagerling R, Gazit SL, Frampton J, Buckley C, Camerer E, Nieswandt B, Kiefer F, Watson SP. Podoplanin and CLEC-2 drive cerebrovascular patterning and integrity during development. Blood 2015;125:3769–3777.
  • Bertozzi CC, Schmaier AA, Mericko P, Hess PR, Zou Z, Chen M, Chen CY, Xu B, Lu MM, Zhou D, Sebzda E, Santore MT, Merianos DJ, Stadtfeld M, Flake AW, Graf T, Skoda R, Maltzman JS, Koretzky GA, Kahn ML. Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood 2010;116:661–670.
  • Suzuki-Inoue K, Inoue O, Ding G, Nishimura S, Hokamura K, Eto K, Kashiwagi H, Tomiyama Y, Yatomi Y, Umemura K, Shin Y, Hirashima M, Ozaki Y. Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J Biol Chem 2010;285:24494–24507.
  • Ichise H, Ichise T, Ohtani O, Yoshida N. Phospholipase Cgamma2 is necessary for separation of blood and lymphatic vasculature in mice. Development 2009;136:191–195.
  • Herzog BH, Fu J, Wilson SJ, Hess PR, Sen A, McDaniel JM, Pan Y, Sheng M, Yago T, Silasi-Mansat R, McGee S, May F, Nieswandt B, Morris AJ, Lupu F, Coughlin SR, McEver RP, Chen H, Kahn ML, Xia L. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature 2013;502:105–109.
  • Hitchcock JR, Cook CN, Bobat S, Ross EA, Flores-Langarica A, Lowe KL, Khan M, Dominguez-Medina CC, Lax S, Carvalho-Gaspar M, Hubscher S, Rainger GE, Cobbold M, Buckley CD, Mitchell TJ, Mitchell A, Jones ND, Van Rooijen N, Kirchhofer D, Henderson IR, Adams DH, Watson SP, Cunningham AF. Inflammation drives thrombosis after Salmonella infection via CLEC-2 on platelets. J Clin Invest 2015;125:4429–4446.
  • Hughes CE, Navarro-Nunez L, Finney BA, Mourao-Sa D, Pollitt AY, Watson SP. CLEC-2 is not required for platelet aggregation at arteriolar shear. JTH 2010;8:2328–2332.
  • Bender M, May F, Lorenz V, Thielmann I, Hagedorn I, Finney BA, Vogtle T, Remer K, Braun A, Bosl M, Watson SP, Nieswandt B. Combined in vivo depletion of glycoprotein VI and C-type lectin-like receptor 2 severely compromises hemostasis and abrogates arterial thrombosis in mice. Arterioscler Thromb Vasc Biol 2013;33:926–934.
  • Hou TZ, Bystrom J, Sherlock JP, Qureshi O, Parnell SM, Anderson G, Gilroy DW, Buckley CD. A distinct subset of podoplanin (gp38) expressing F4/80+ macrophages mediate phagocytosis and are induced following zymosan peritonitis. FEBS Lett 2010;584:3955–3961.
  • Horbar JD, Badger GJ, Carpenter JH, Fanaroff AA, Kilpatrick S, LaCorte M, Phibbs R, Soll RF. Members of the Vermont Oxford N trends in mortality and morbidity for very low birth weight infants, 1991-1999. Pediatrics 2002;110:143–151.
  • Thrombocytopenia SSJ. bleeding, and use of platelet transfusions in sick neonates. Hematol Am Soc Hematol Educ Program 2012;2012:512–516.
  • Ferrer-Marin F, Stanworth S, Josephson C, Sola-Visner M. Distinct differences in platelet production and function between neonates and adults: implications for platelet transfusion practice. Transfusion 2013;53:2814–2821; quiz 2813.
  • Wang DB, Blocher NC, Spence ME, Rovainen CM, Woolsey TA. Development and remodeling of cerebral blood vessels and their flow in postnatal mice observed with in vivo videomicroscopy. J Cereb Blood Flow Metab 1992;12:935–946.
  • Rovainen CM, Wang DB, Woolsey TA. Strobe epi-illumination of fluorescent beads indicates similar velocities and wall shear rates in brain arterioles of newborn and adult mice. Microvasc Res 1992;43:235–239.
  • Navarro-Nunez L, Pollitt AY, Lowe K, Latif A, Nash GB, Watson SP. Platelet adhesion to podoplanin under flow is mediated by the receptor CLEC-2 and stabilised by Src/Syk-dependent platelet signalling. Thromb Haemost 2015;113:1109–1120.
  • Christou CM, Pearce AC, Watson AA, Mistry AR, Pollitt AY, Fenton-May AE, Johnson LA, Jackson DG, Watson SP, O’Callaghan CA. Renal cells activate the platelet receptor CLEC-2 through podoplanin. Biochem J 2008;411:133–140.
  • Pollitt AY, Poulter NS, Gitz E, Navarro-Nunez L, Wang YJ, Hughes CE, Thomas SG, Nieswandt B, Douglas MR, Owen DM, Jackson DG, Dustin ML, Watson SP. Syk and Src family kinases regulate C-type lectin receptor 2 (CLEC-2)-mediated clustering of podoplanin and platelet adhesion to lymphatic endothelial cells. J Biol Chem 2014;289:35695–35710.
  • Acton Sophie E, Astarita Jillian L, Malhotra D, Lukacs-Kornek V, Franz B, Hess Paul R, Jakus Z, Kuligowski M, Fletcher Anne L, Elpek Kutlu G, Bellemare-Pelletier A, Sceats L, Reynoso Erika D, Gonzalez Santiago F, Graham Daniel B, Chang J, Peters A, Woodruff M, Kim Y-A, Swat W, Morita T, Kuchroo V, Carroll Michael C, Kahn Mark L, Wucherpfennig Kai W, Turley Shannon J. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 2012;37:276–289.
  • Nowak AA, Canis K, Riddell A, Laffan MA, McKinnon TA. O-linked glycosylation of von Willebrand factor modulates the interaction with platelet receptor glycoprotein Ib under static and shear stress conditions. Blood 2012;120:214–222.
  • Borgognone A, Navarro-Nunez L, Correia JN, Pollitt AY, Thomas SG, Eble JA, Pulcinelli FM, Madhani M, Sp W. CLEC-2-dependent activation of mouse platelets is weakly inhibited by cAMP but not by cGMP. Jth 2014;12:550–559.
  • Li Z, Delaney MK, O’Brien KA, Du X. Signaling during platelet adhesion and activation. Arterioscler Thromb Vasc Biol 2010;30:2341–2349.
  • Kaneko MK, Kato Y, Kitano T, Osawa M. Conservation of a platelet activating domain of Aggrus/podoplanin as a platelet aggregation-inducing factor. Gene 2006;378:52–57.
  • Kato Y, Fujita N, Kunita A, Sato S, Kaneko M, Osawa M, Tsuruo T. Molecular identification of Aggrus/T1alpha as a platelet aggregation-inducing factor expressed in colorectal tumors. J Biol Chem 2003;278::51599–51605.
  • Martin-Villar E, Fernandez-Munoz B, Parsons M, Yurrita MM, Megias D, Perez-Gomez E, Jones GE, Quintanilla M. Podoplanin associates with CD44 to promote directional cell migration. Mol Biol Cell 2010;21:4387–4399.
  • Kaneko MK, Kato Y, Kameyama A, Ito H, Kuno A, Hirabayashi J, Kubota T, Amano K, Chiba Y, Hasegawa Y, Sasagawa I, Mishima K, Narimatsu H. Functional glycosylation of human podoplanin: glycan structure of platelet aggregation-inducing factor. FEBS Lett 2007;581:331–336.
  • Savage B, Saldivar E, Ruggeri ZM. Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 1996;84:289–297.
  • Lopez JA, Dong JF. Structure and function of the glycoprotein Ib-IX-V complex. Curr Opin Hematol 1997;4:323–329.
  • Du X. Signaling and regulation of the platelet glycoprotein Ib-IX-V complex. Curr Opin Hematol 2007;14:262–269.
  • Senis YA, Mazharian A, Mori J. Src family kinases: at the forefront of platelet activation. Blood 2014;124:2013–2024.
  • Manne BK, Badolia R, Dangelmaier C, Eble JA, Ellmeier W, Kahn M, Kunapuli SP. Distinct pathways regulate Syk protein activation downstream of immune tyrosine activation motif (ITAM) and hemITAM receptors in platelets. J Biol Chem 2015;290:11557–11568.
  • Ren Q, Ye S. Whiteheart SW The platelet release reaction: just when you thought platelet secretion was simple. Curr Opin Hematol 2008;15:537–541.
  • Reed GL, Fitzgerald ML, Polgar J. Molecular mechanisms of platelet exocytosis: insights into the “secrete” life of thrombocytes. Blood 2000;96:3334–3342.
  • Coller BS, Shattil SJ. The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood 2008;112:3011–3025.
  • Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 2010;11:288–300.
  • Seymour RS, Bosiocic V, Snelling EP. Fossil skulls reveal that blood flow rate to the brain increased faster than brain volume during human evolution. R Soc Open Sci 2016;3:160305.

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