Vascular smooth muscle cells stimulate platelets and facilitate thrombus formation through platelet CLEC-2: Implications in atherothrombosis

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Inoue, Osamu ^a   Hokamura, Kazuya ^b   Shirai, Toshiaki ^a   Osada, Makoto ^a   Tsukiji, Nagaharu ^a   Hatakeyama, Kinta ^c   Umemura, Kazuo ^b   Asada, Yujiro ^c   Suzuki Inoue, Katsue ^a   Ozaki, Yukio ^a  

^a UNIVERSITY OF YAMANASHI   (Japan)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CLEC 2 PROTEIN; FERRIC CHLORIDE; PODOPLANIN; PROTEIN S 100; PROTEIN S 100A13; THROMBOCYTE RECEPTOR; UNCLASSIFIED DRUG; CLEC-2 PROTEIN, MOUSE; CLEC2B PROTEIN, HUMAN; LECTIN; LIGAND; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN; PROTEIN BINDING; S100A13 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; BLOOD CLOTTING; CONTROLLED STUDY; CORONARY ARTERY MUSCLE; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HAMSTER; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VIVO STUDY; LIGAND BINDING; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; RABBIT; SURFACE PLASMON RESONANCE; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE COUNT; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPOIESIS; THROMBOSIS; VASCULAR SMOOTH MUSCLE CELL; WESTERN BLOTTING; ANIMAL; ARTERIOSCLEROSIS; C57BL MOUSE; CELL CULTURE; CHO CELL LINE; CRICETULUS; CYTOLOGY; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; SMOOTH MUSCLE CELL; THROMBOCYTE; TRANSGENIC MOUSE; VASCULAR SMOOTH MUSCLE;

ANIMALS; ARTERIOSCLEROSIS; BLOOD PLATELETS; BLOTTING, WESTERN; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; LECTINS, C-TYPE; LIGANDS; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PLATELET AGGREGATION; PROTEIN BINDING; S100 PROTEINS; THROMBOSIS;

EID: 84947928655     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0139357     Document Type: Article

References (42)

1. Suzuki-Inoue K, Fuller GL, Garcia A, Eble JA, Pohlmann S, Inoue O, et al. A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood. 2006; 107(2):542-9. Epub 2005/09/22. 2005-05-1994 [pii] doi: 10.1182/blood-2005-05-1994 PMID: 16174766.
2. Suzuki-Inoue K, Kato Y, Inoue O, Kaneko MK, Mishima K, Yatomi Y, et al. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem. 2007; 282(36):25993-6001. Epub 2007/07/10. M702327200 [pii] doi: 10.1074/jbc.M702327200 PMID: 17616532.
3. Kato Y, Kaneko MK, Kunita A, Ito H, Kameyama A, Ogasawara S, et al. Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci. 2008; 99(1):54-61. Epub 2007/10/20. CAS634 [pii] doi: 10.1111/j.1349-7006.2007.00634.x PMID: 17944973.
4. Tsuruo T, Fujita N. Platelet aggregation in the formation of tumor metastasis. Proc Jpn Acad Ser B Phys Biol Sci. 2008; 84(6):189-98. Epub 2008/10/23. JST.JSTAGE/pjab/84.189 [pii]. PMID: 18941298.
5. Bertozzi CC, Schmaier AA, Mericko P, Hess PR, Zou Z, Chen M, et al. Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood. 2010; 116(4):661-70. Epub 2010/04/07. blood-2010-02-270876 [pii] doi: 10.1182/blood-2010-02-270876 PMID: 20363774.
6. Suzuki-Inoue K, Inoue O, Ding G, Nishimura S, Hokamura K, Eto K, et al. 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(32):24494-507. Epub 2010/06/08. M110.130575 [pii] doi: 10.1074/jbc.M110.130575 PMID: 20525685; PubMed Central PMCID: PMC2915686.
7. 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. Journal of thrombosis and haemostasis: JTH. 2010; 8(10):2328-32. Epub 2010/08/11. JTH4006 [pii] doi: 10.1111/j.1538-7836.2010.04006.x PMID: 20695981.
8. Finney BA, Schweighoffer E, Navarro-Nunez L, Benezech C, Barone F, Hughes CE, et al. CLEC-2 and Syk in the megakaryocytic/platelet lineage are essential for development. Blood. 2012; 119(7):1747-56. Epub 2011/12/22. blood-2011-09-380709 [pii] doi: 10.1182/blood-2011-09-380709 PMID: 22186994.
9. Osada M, Inoue O, Ding G, Shirai T, Ichise H, Hirayama K, et al. Platelet Activation Receptor CLEC-2 Regulates Blood/Lymphatic Vessel Separation by Inhibiting Proliferation, Migration, and Tube Formation of Lymphatic Endothelial Cells. Journal of Biological Chemistry. 2012; 287(26):22241-52. Epub 2012/05/05. M111.329987 [pii] doi: 10.1074/jbc.M111.329987 PMID: 22556408.
10. May F, Hagedorn I, Pleines I, Bender M, Vogtle T, Eble J, et al. CLEC-2 is an essential platelet-activating receptor in hemostasis and thrombosis. Blood. 2009; 114(16):3464-72. Epub 2009/07/31. blood-2009-05-222273 [pii] doi: 10.1182/blood-2009-05-222273 PMID: 19641185.
11. Bender M, May F, Lorenz V, Thielmann I, Hagedorn I, Finney BA, et al. Combined in vivo depletion of glycoprotein VI and C-type lectin-like receptor 2 severely compromises hemostasis and abrogates arterial thrombosis in mice. ArteriosclerThromb Vasc Biol. 2013; 33(5):926-34. doi: 10.1161/ATVBAHA. 112.300672 PMID: 23448972.
12. Morton LF, Hargreaves PG, Farndale RW, Young RD, Barnes MJ. Integrin alpha 2 beta 1-independent activation of platelets by simple collagen-like peptides: collagen tertiary (triple-helical) and quaternary (polymeric) structures are sufficient alone for alpha 2 beta 1-independent platelet reactivity. Biochem J. 1995; 306 (Pt2):337-44. Epub 1995/03/01. PMID: 7534064; PubMed Central PMCID: PMC1136526.
13. Shin Y, Morita T. Rhodocytin, afunctional novel platelet agonist belonging to the heterodimericC-type lectin family, induces platelet aggregation independently of glycoprotein Ib. Biochem Biophys Res Commun. 1998; 245(3):741-5. Epub 1998/05/20. S0006-291X(98)98516-3 [pii] doi: 10.1006/bbrc.1998.8516 PMID: 9588185.
14. Hatakeyama K, Asada Y, Marutsuka K, Sato Y, Kamikubo Y, Sumiyoshi A. Localization and activity of tissue factor in human aortic atherosclerotic lesions. Atherosclerosis. 1997; 133(2):213-9. PMID: 9298681.
15. Ishikawa T, Hatakeyama K, Imamura T, Ito K, Hara S, Date H, et al. Increased adrenomedullin immunoreactivity and mRNA expression in coronary plaques obtained from patients with unstable angina. Heart. 2004; 90(10):1206-10. doi: 10.1136/hrt.2003.017921 PMID: 15367525; PubMed Central PMCID: PMC1768472.
16. Sharmin S, Sakata K, Kashiwagi K, Ueda S, Iwasaki S, Shirahata A, et al. Polyamine cytotoxicity in the presence of bovine serum amine oxidase. Biochem Biophys Res Commun. 2001; 282(1):228-35. doi: 10.1006/bbrc.2001.4569 PMID: 11263996.
17. Suzuki-Inoue K, Inoue O, Frampton J, Watson SP. Murine GPVI stimulates weak integrin activation in PLCgamma2-/- platelets: involvement of PLCgamma1 and PI3-kinase. Blood. 2003; 102(4):1367-73. Epub 2003/05/06. doi: 10.1182/blood-2003-01-0029 2003-01-0029 [pii]. PMID: 12730118.
18. Kikuchi S, Umemura K, Kondo K, Saniabadi AR, Nakashima M. Photochemically induced endothelial injury in the mouse as a screening model for inhibitors of vascular intimal thickening. Arterioscler Thromb Vasc Biol. 1998; 18(7):1069-78. PMID: 9672067.
19. Inoue O, Suzuki-Inoue K, McCarty OJ, Moroi M, Ruggeri ZM, Kunicki TJ, et al. Laminin stimulates spreading of platelets through integrin alpha6beta1-dependent activation of GPVI. Blood. 2006; 107(4):1405-12. Epub 2005/10/13. 2005-06-2406 [pii] doi: 10.1182/blood-2005-06-2406 PMID: 16219796; PubMed Central PMCID: PMC1895394.
20. Suzuki-Inoue K, Yatomi Y, Asazuma N, Kainoh M, Tanaka T, Satoh K, et al. Rac, a small guanosinetriphosphate-binding protein, and p21-activated kinase are activated during platelet spreading on collagen-coated surfaces: roles of integrin alpha(2)beta(1). Blood. 2001; 98(13):3708-16. Epub 2001/12/12. PMID: 11739176.
21. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr., et al. Adefinition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995; 92(5):1355-74. PMID: 7648691.
22. Munnix IC, Strehl A, Kuijpers MJ, Auger JM, van der Meijden PE, van Zandvoort MA, et al. The glycoprotein VI-phospholipase Cgamma2 signaling pathway controls thrombus formation induced by collagen and tissue factor in vitro and in vivo. Arteriosclerosis, Thrombosis, and Vascular Biology. 2005; 25(12):2673-8. Epub 2005/10/29. 01.ATV.0000193568.71980.4a [pii] doi: 10.1161/01.ATV.0000193568.71980.4a PMID: 16254207.
23. Morowski M, Vogtle T, Kraft P, Kleinschnitz C, Stoll G, Nieswandt B. Only severe thrombocytopenia results in bleeding and defective thrombus formation in mice. Blood. 2013; 121(24):4938-47. doi: 10.1182/blood-2012-10-461459 PMID: 23584880.
24. Hirata Y, Umemura K, Kondoh K, Uematsu T, Nakashima M. Experimental intimal thickening studies using the photochemically induced thrombosis model in the guinea-pig femoral artery. Atherosclerosis. 1994; 107(1):117-24. PMID: 7945554.
25. Mohan SK, Yu C. The IL1alpha-S100A13 heterotetrameric complex structure: a component in the non-classical pathway for interleukin 1alpha secretion. J BiolChem. 2011; 286(16):14608-17. doi: 10.1074/jbc.M110.201954 PMID: 21270123; PubMed Central PMCID: PMC3077658.
26. MoutaCarreira C, LaVallee TM, Tarantini F, Jackson A, Lathrop JT, Hampton B, et al. S100A13is involved in the regulation of fibroblast growth factor-1 and p40 synaptotagmin-1 release in vitro. J Biol Chem. 1998; 273(35):22224-31. PMID: 9712836.
27. Mandinova A, Soldi R, Graziani I, Bagala C, Bellum S, Landriscina M, et al. S100A13 mediates the copper-dependent stress-induced release of IL-1alpha from both human U937and murine NIH 3T3 cells. J Cell Sci. 2003; 116(Pt 13):2687-96. doi: 10.1242/jcs.00471 PMID: 12746488.
28. Ridinger K, Schafer BW, Durussel I, Cox JA, Heizmann CW. S100A13. Biochemical characterization and subcellular localization in different cell lines. J BiolChem. 2000; 275(12):8686-94. PMID: 10722710.
29. Kathir KM, Gao L, Rajalingam D, Daily AE, Brixey S, Liu H, et al. NMR characterization of copper and lipid interactions of the C2B domain of synaptotagmin I-relevance to the non-classical secretion of the human acidic fibroblast growth factor (hFGF-1). BiochimBiophysActa. 2010; 1798(2):297-302. doi: 10.1016/j.bbamem.2009.09.024 PMID: 19835837; PubMed Central PMCID: PMC3628535.
30. Matsunaga H, Ueda H. Stress-induced non-vesicular release of prothymosin-alpha initiated by an interaction with S100A13, and its blockade by caspase-3 cleavage. Cell Death Differ. 2010; 17(11):1760-72. doi: 10.1038/cdd.2010.52 PMID: 20467443.
31. Blanc A, Pandey NR, Srivastava AK. Synchronous activation of ERK 1/2, p38 mapkand PKB/Akt signaling by H2O2 in vascular smooth muscle cells: potential involvement in vascular disease (review). Int J Mol Med. 2003; 11(2):229-34. PMID: 12525883.
32. Hatakeyama K, Kaneko MK, Kato Y, Ishikawa T, Nishihira K, Tsujimoto Y, et al. Podoplaninexpression in advanced atherosclerotic lesions of human aortas. Thrombosis Research. 2012; 129(4):e70-6. Epub 2012/01/31. S0049-3848(12)00007-2 [pii] doi: 10.1016/j.thromres.2012.01.003 PMID: 22283975.
33. Hayashi K, Saga H, Chimori Y, Kimura K, Yamanaka Y, Sobue K. Differentiated phenotype of smooth muscle cells depends on signaling pathways through insulin-like growth factors and phosphatidylinositol 3-kinase. Journal of Biological Chemistry. 1998; 273(44):28860-7. Epub 1998/10/24. PMID: 9786887.
34. Cosemans JM, Angelillo-Scherrer A, Mattheij NJ, Heemskerk JW. The effects of arterial flow on platelet activation, thrombus growth, and stabilization. Cardiovasc Res. 2013; 99(2):342-52. doi: 10.1093/cvr/cvt110 PMID: 23667186.
35. Massi D, Landriscina M, Piscazzi A, Cosci E, Kirov A, Paglierani M, et al. S100A13 is a new angiogenic marker in human melanoma. Mod Pathol. 2010; 23(6):804-13. doi: 10.1038/modpathol.2010.54 PMID: 20208480; PubMed Central PMCID: PMC2882157.
36. Li C, Zhang F, Wang Y. S100A proteins in the pathogenesis of experimental corneal neovascularization. Mol Vis. 2010; 16:2225-35. PMID: 21139687; PubMed Central PMCID: PMC2994359.
37. Landriscina M, Schinzari G, Di Leonardo G, Quirino M, Cassano A, D'Argento E, et al. S100A13, anew marker of angiogenesis in human astrocytic gliomas. J Neurooncol. 2006; 80(3):251-9. doi: 10.1007/s11060-006-9189-y PMID: 16773219.
38. Pierce A, Barron N, Linehan R, Ryan E, O'Driscoll L, Daly C, et al. Identification of a novel, functional roleforS100A13 in invasive lung cancer cell lines. Eur J Cancer. 2008; 44(1):151-9. doi: 10.1016/j.ejca.2007.10.017 PMID: 18061437.
39. Lambros MP, Parsa C, Mulamalla H, Orlando R, Lau B, Huang Y, et al. Identifying cell and molecular stress after radiation in a three-dimensional (3-D) model of oral mucositis. Biochem Biophys Res Commun. 2011; 405(1):102-6. doi: 10.1016/j.bbrc.2010.12.135 PMID: 21216227.
40. Mandinov L, Mandinova A, Kyurkchiev S, Kyurkchiev D, Kehayov I, Kolev V, et al. Copper chelation represses the vascular response to injury. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100(11):6700-5. doi: 10.1073/pnas.1231994100 PMID: 12754378; PubMed Central PMCID: PMC164510.
41. Siddiqi OK, Faxon DP. Very late stent thrombosis: current concepts. CurrOpin Cardiol. 2012; 27(6):634-41. Epub 2012/10/19. doi: 10.1097/HCO.0b013e3283587c7e 00001573-201211000-00012 [pii]. PMID: 23075822.
42. Farb A, Burke AP, Tang AL, Liang TY, Mannan P, Smialek J, et al. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996; 93(7):1354-63. PMID: 8641024.