Effect of the hydrogen sulfide donor GYY4137 on platelet activation and microvascular thrombus formation in mice

Platelets

Volumn 25, Issue 3, 2014, Pages 166-174

  Grambow, Eberhard ^a   Mueller Graf, Fabian ^a   Delyagina, Evgenya ^a   Frank, Marcus ^a   Kuhla, Angela ^a   Vollmar, Brigitte ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Alpha granule; Glycoprotein IIb IIIa; Microvascular thrombosis; Platelet exocytosis; S sulfhydration

Indexed keywords

ANTIBODY; ANTICOAGULANT AGENT; CELL ADHESION MOLECULE; DIMETHYL SULFOXIDE; F ACTIN; FERROUS CHLORIDE; GYY 4137; HYDROGEN SULFIDE; N ETHYLMALEIMIDE SENSITIVE FACTOR; P SELECTIN ANTIBODY; PADGEM PROTEIN; THROMBIN RECEPTOR ACTIVATING PEPTIDE; UNCLASSIFIED DRUG; ACID PHOSPHATASE; FIBRINOGEN RECEPTOR; ISOENZYME; MORPHOLINE DERIVATIVE; PHOSPHOROTHIOIC ACID DERIVATIVE; TARTRATE-RESISTANT ACID PHOSPHATASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING TIME; BLOOD CLOTTING; C57BL 6 MOUSE; CELL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ELECTRON MICROSCOPY; EVALUATION STUDY; EXOCYTOSIS; FLOW CYTOMETRY; HUMAN; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN SULFHYDRATION; SUPER RESOLUTION STRUCTURED ILLUMINATION MICROSCOPY; THROMBOCYTE ACTIVATION; THROMBOCYTE STRUCTURE; THROMBUS; ANIMAL; BLOOD; C57BL MOUSE; CHEMISTRY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; THROMBOCYTE; THROMBOSIS; ULTRASTRUCTURE;

ACID PHOSPHATASE; ANIMALS; BLOOD PLATELETS; HUMANS; HYDROGEN SULFIDE; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; MORPHOLINES; ORGANOTHIOPHOSPHORUS COMPOUNDS; P-SELECTIN; PLATELET ACTIVATION; PLATELET GLYCOPROTEIN GPIIB-IIIA COMPLEX; THROMBOSIS;

EID: 84925225522     PISSN: 09537104     EISSN: 13691635     Source Type: Journal    
DOI: 10.3109/09537104.2013.786823     Document Type: Article

References (47)

1. Szabó C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 2007;6:917-935.
2. Calvert JW, Coetzee WA, Lefer DJ. Novel insights into hydrogen sulfide-mediated cytoprotection. Antioxid Redox Signal 2010;12: 1203-1217.
3. Tanizawa K. Production of H2S by 3-mercaptopyruvate. J Biochem 2011;149:357-359.
4. Shibuya N, Koike S, Tanaka M, Ishigami-Yuasa M, Kimura Y, Ogasawara Y, Fukui K, Nagahara N, Kimura H. A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat Commun 2013;4:1366-1372.
5. Whiteman M, Cheung NS, Zhu YZ, Chu SH, Siau JL, Wong BS, Armstrong JS, Moore PK. Hydrogen sulphide: A novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 2005;326:794-798.
6. Whiteman M, Moore PK. Hydrogen sulfide and the vasculature: A novel vasculoprotective entity and regulator of nitric oxide. J Cell Mol Med 2009;13:488-507.
7. Wagner F, Asfar P, Calzia E, Radermacher P, Szabó C. Bench-to-bedside review: Hydrogen sulfide-The third gaseous transmitter: Applications for critical care. Crit Care 2009;13:213-221.
8. Fang L, Zhao J, Chen Y, Ma T, Xu G, Tang C, Liu X, Geng B. Hydrogen sulfide derived from periadventitial adipose tissue is a vasodilator. J Hypertens 2009;27:2174-2185.
9. Mustafa AK, Gadalla MM, Sen N, Kim S, Mu W, Gazi SK, Barrow RK, Yang G, Wang R, Snyder SH. H2S signals through protein S-sulfhydration. Sci Signal 2009;2:72-79.
10. Lowicka E, Beltowski J. Hydrogen sulfide (H2S)-The third gas of interest for pharmacologists. Pharmacol Rep 2007;59:4-24.
11. Zagli G, Patacchini R, Trevisani M, Abbate R, Cinotti S, Gensini GF, Masotti G, Geppetti P. Hydrogen sulfide inhibits human platelet aggregation. Eur J Pharmacol 2007;559:65-68.
12. Morrell CN, Matsushita K, Chiles K, Scharpf RB, Yamakuchi M, Mason RJ, Bergmeier W, Mankowski JL, Baldwin 3rd WM, Faraday N, et al. Regulation of platelet granule exocytosis by S-nitrosylation. Proc Natl Acad Sci USA 2005;102:3782-3787.
13. Polgár J, Reed GL. A critical role for N-ethylmaleimide-sensitive fusion protein (NSF) in platelet granule secretion. Blood 1999;94: 1313-1318.
14. Whiteheart SW, Rossnagel K, Buhrow SA, Brunner M, Jaenicke R, Rothman JE. N-ethylmaleimide-sensitive fusion protein: A trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 1994;126:945-954.
15. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): New insights into the biology of hydrogen sulfide. Circulation 2008; 117:2351-2360.
16. Rivera J, Lozano ML, Navarro-Núñez L, Vicente V. Platelet receptors and signaling in the dynamics of thrombus formation. Haematologica 2009;94:700-711.
17. Weeterings C, Adelmeijer J, Myles T, de Groot PG, Lisman T. Glycoprotein Ib alpha-mediated platelet adhesion and aggregation to immobilized thrombin under conditions of flow. Arterioscler Thromb Vasc Biol 2006;26:670-675.
18. Siljander P, Carpen O, Lassila R. Platelet-derived micro-particles associate with fibrin during thrombosis. Blood 1996;87: 4651-4663.
19. Doré M, Korthuis RJ, Granger DN, Entman ML, Smith CW. P-selectin mediates spontaneous leukocyte rolling in vivo. Blood 1993;82:1308-1316.
20. Merten M, Thiagarajan P. P-selectin expression on platelets determines size and stability of platelet aggregates. Circulation 2000;102:1931-1936.
21. Lehr HA, Leunig M, Menger MD, Nolte D, Messmer K. Dorsal skinfold chamber technique for intravital microscopy in nude mice. Am J Pathol 1993;143:1055-1062.
22. Püschel A, Lindenblatt N, Katzfuß J, Vollmar B, Klar E. Immunosuppressants accelerate microvascular thrombus formation in vivo: Role of endothelial cell activation. Surgery 2012;151: 26-36.
23. Sorg H, Hoffmann JN, Menger MD, Lindenblatt N, Goehring P, Vollmar B. Antithrombin is as effective as heparin and hirudin to prevent formation of microvascular thrombosis in a murine model. Thromb Haemost 2006;96:371-377.
24. Furie B, Furie BC. Thrombus formation in vivo. J Clin Invest 2005; 115:3355-3362.
25. Lindenblatt N, Schareck W, Belusa L, Nickels RM, Menger MD, Vollmar B. Anti-oxidant ebselen delays microvascular thrombus formation in the rat cremaster muscle by inhibiting platelet P-selectin expression. Thromb Haemost 2003;90:882-892.
26. Boulaftali Y, Lamrani L, Rouzaud MC, Loyau S, Jandrot-Perrus M, Bouton MC, Ho-Tin-Noé B. The mouse dorsal skinfold chamber as a model for the study of thrombolysis by intravital microscopy. Thromb Haemost 2012;107:962-971.
27. Herrmann KS. Platelet aggregation induced in the hamster cheek pouch by a photochemical process with excited fluorescein isothiocyanate-dextran. Microvasc Res 1983;26:238-249.
28. Morel A, Malinowska J, Olas B. Antioxidative properties of hydrogen sulfide may involve in its antiadhesive action on blood platelets. Clin Biochem 2012;45:1678-1682.
29. Eckly A, Hechler B, Freund M, Zerr M, Cazenave JP, Lanza F, Mangin PH, Gachet C. Mechanisms underlying FeCl3-induced arterial thrombosis. J Thromb Haemost 2011;9:779-789.
30. Sun Y, Tang C, Jin H, Du J. The vasorelaxing effect of hydrogen sulfide on isolated rat aortic rings versus pulmonary artery rings. Acta Pharmacol Sin 2011;4:456-464.
31. Liang GH, Xi Q, Leffler CW, Jaggar JH. Hydrogen sulfide activates Ca 2 sparks to induce cerebral arteriole dilatation. J Physiol 2012; 590:2709-2720.
32. Jiang B, Tang G, Cao K, Wu L, Wang R. Molecular mechanism for H(2)S-induced activation of K(ATP) channels. Antioxid Redox Signal 2010;12:1167-1178.
33. Subramaniam M, Frenette PS, Saffaripour S, Johnson RC, Hynes RO, Wagner DD. Defects in hemostasis in P-selectin-deficient mice. Blood 1996;87:1238-1242.
34. Furie B, Furie BC, Flaumenhaft R. A journey with platelet P-selectin: The molecular basis of granule secretion, signalling and cell adhesion. Thromb Haemost 2001;86:214-221.
35. André P, Hartwell D, Hrachovinová I, Saffaripour S, Wagner DD. Pro-coagulant state resulting from high levels of soluble P-selectin in blood. Proc Natl Acad Sci USA 2000;97:13835-13840.
36. Ramacciotti E, Myers Jr DD, Wrobleski SK, Deatrick KB, Londy FJ, Rectenwald JE, Henke PK, Schaub RG, Wakefield TW. P-selectin/PSGL-1 inhibitors versus enoxaparin in the resolution of venous thrombosis: A meta-Analysis. Thromb Res 2010;125:138-142.
37. Fijnheer R, Frijns CJ, Korteweg J, Rommes H, Peters JH, Sixma JJ, Nieuwenhuis HK. The origin of P-selectin as a circulating plasma protein. Thromb Haemost 1997;77:1081-1085.
38. Frijns CJ, Kappelle LJ, van Gijn J, Nieuwenhuis HK, Sixma JJ, Fijnheer R. Soluble adhesion molecules reflect endothelial cell activation in ischemic stroke and in carotid atherosclerosis. Stroke 1997;28:2214-2218.
39. Ferroni P, Martini F, Riondino S, La Farina F, Magnapera A, Ciatti F, Guadagni F. Soluble P-selectin as a marker of in vivo platelet activation. Clin Chim Acta 2009;399:88-91.
40. Rink TJ, Smith SW, Tsien RY. Cytoplasmic free Ca2 in human platelets: Ca2 thresholds and Ca-independent activation for shape-change and secretion. FEBS Lett 1982;148:21-26.
41. Hartwig JH, Chambers KA, Stossel TP. Association of gelsolin with actin filaments and cell membranes of macrophages and platelets. J Cell Biol 1989;108:467-479.
42. Klages B, Brandt U, Simon MI, Schultz G, Offermanns S. Activation of G12/G13 results in shape change and Rho/Rho-kinase-mediated myosin light chain phosphorylation in mouse platelets. J Cell Biol 1999;144:745-754.
43. Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bösl M, Stoll G, Nieswandt B. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 2009;113:2056-2063.
44. Munaron L, Avanzato D, Moccia F, Mancardi D. Hydrogen sulfide as a regulator of calcium channels. Cell Calcium 2012;53: 77-84.
45. Li L, Rose P, Moore PK. Hydrogen sulfide and cell signaling. Annu Rev Pharmacol Toxicol 2011;51:169-187.
46. Mustafa AK, Sikka G, Gazi SK, Steppan J, Jung SM, Bhunia AK, Barodka VM, Gazi FK, Barrow RK, Wang R, et al. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ Res 2011;109:1259-1268.
47. Margaritis A, Priora R, Frosali S, Di Giuseppe D, Summa D, Coppo L, Di Stefano A, Di Simplicio P. The role of protein sulfhydryl groups and protein disulfides of the platelet surface in aggregation processes involving thiol exchange reactions. Pharmacol Res 2011; 63:77-84.