Locally targeted cytoprotection with dextran sulfate attenuates experimental porcine myocardial ischaemia/reperfusion injury

European Heart Journal

Volumn 26, Issue 21, 2005, Pages 2334-2343

  Banz, Yara ^a   Hess, Otto M ^b   Robson, Simon C ^c   Mettler, Daniel ^a   Meier, Pascal ^b   Haeberli, André ^a   Csizmadia, Eva ^c   Korchagina, Elena Y ^d   Bovin, Nicolai V ^d   Rieben, Robert ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b BERN UNIVERSITY HOSPITAL   (Switzerland)

^c HARVARD UNIVERSITY   (United States)

^d SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

Cytoprotection; Dextran sulfate; Endothelium; Ischaemia reperfusion injury

Indexed keywords

CREATINE KINASE; DEXTRAN SULFATE; FLUORESCEIN; HEART ENZYME; PROTEOHEPARAN SULFATE; THROMBOPLASTIN; TROPONIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL PROTECTION; CONTROLLED STUDY; CORRELATION ANALYSIS; HEART INFARCTION SIZE; HEART LEFT VENTRICLE; HEART MUSCLE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; STAINING; STATISTICAL SIGNIFICANCE; SWINE;

ANIMALS; BIOLOGICAL MARKERS; BLOOD PRESSURE; COMPLEMENT ACTIVATION; CREATINE KINASE; DEXTRAN SULFATE; IMMUNOHISTOCHEMISTRY; ISCHEMIC PRECONDITIONING, MYOCARDIAL; LIGATION; MYOCARDIAL REPERFUSION INJURY; PLASMA SUBSTITUTES; RANDOM ALLOCATION; SWINE; TROPONIN I;

EID: 27544469830     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehi421     Document Type: Article

References (59)

1. Matsumura K, Jeremy RW, Schaper J, Becker LC. Progression of myocardial necrosis during reperfusion of ischemic myocardium. Circulation 1998;97:795-804.
2. Kilgore KS, Friedrichs GS, Homeister JW, Lucchesi BR. The complement system in myocardial ischaemia/reperfusion injury. Cardiovasc Res 1994;28:437-444.
3. Zhou W, Farrar CA, Abe K, Pratt JR, Marsh JE, Wang Y, Stahl GL, Sacks SH. Predominant role for C5b-9 in renal ischemia/reperfusion injury. J Clin Invest 2000;105:1363-1371.
4. Mathey D, Schofer J, Schafer HJ, Hamdoch T, Joachim HC, Ritgen A, Hugo F, Bhakdi S. Early accumulation of the terminal complement-complex in the ischaemic myocardium after reperfusion. Eur Heart J 1994;15:418-423.
5. Adler S, Baker PJ, Johnson RJ, Ochi RF, Pritzl P, Couser WG. Complement membrane attack complex stimulates production of reactive oxygen metabolites by cultured rat mesangial cells. J Clin Invest 1986;77:762-767.
6. Kilgore KS, Park JL, Tanhehco EJ, Booth EA, Marks RM, Lucchesi BR. Attenuation of interleukin-8 expression in C6-deficient rabbits after myocardial ischemia/reperfusion. J Mol Cell Cardiol 1998;30:75-85.
7. Amsterdam EA, Stahl GL, Pan HL, Rendig SV, Fletcher MP, Longhurst JC. Limitation of reperfusion injury by a monoclonal antibody to C5a during myocardial infarction in pigs. Am J Physiol 1995;268:H448-H457.
8. Horstick G, Berg O, Heimann A, Gotze O, Loos M, Hafner G, Bierbach B, Petersen S, Bhakdi S, Darius H, Horstick M, Meyer J, Kempski O. Application of C1-esterase inhibitor during reperfusion of ischemic myocardium: dose-related beneficial versus detrimental effects. Circulation 2001;104:3125-3131.
9. Granger CB, Mahaffey KW, Weaver WD, Theroux P, Hochman JS, Filloon TG, Rollins S, Todaro TG, Nicolau JC, Ruzyllo W, Armstrong PW. Pexelizumab, an anti-C5 complement antibody, as adjunctive therapy to primary percutaneous coronary intervention in acute myocardial infarction: the COMplement inhibition in Myocardial infarction treated with Angioplasty (COMMA) trial. Circulation 2003;108:1184-1190.
10. Golino P, Ragni M, Cirillo P, Avvedimento VE, Feliciello A, Esposito N, Scognamiglio A, Trimarco B, Iaccarino G, Condorelli M, Chiariello M, Ambrosio G. Effects of tissue factor induced by oxygen free radicals on coronary flow during reperfusion. Nat Med 1996;2:35-40.
11. Koo DD, Welsh KI, Roake JA, Morris PJ, Fuggle SV. Ischemia/reperfusion injury in human kidney transplantation: an immunohistochemical analysis of changes after reperfusion. Am J Pathol 1998;153:557-566.
12. Erlich JH, Boyle EM, Labriola J, Kovacich JC, Santucci RA, Fearns C, Morgan EN, Yun W, Luther T, Kojikawa O, Martin TR, Pohlman TH, Verrier ED, Mackman N. Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischemia-reperfusion injury by reducing inflammation. Am J Pathol 2000;157:1849-1862.
13. Czarnowska E, Karwatowska-Prokopczuk E. Ultrastructural demonstration of endothelial glycocalyx disruption in the reperfused rat heart. Involvement of oxygen free radicals. Basic Res Cardiol 1995;90:357-364.
14. Mulivor AW, Lipowsky HH. Inflammation and ischemia induced shedding of the venular glycocalyx. Am J Physiol Heart Circ Physiol 2004;286:H1672-1680.
15. Platts SH, Linden J, Duling BR. Rapid modification of the glycocalyx caused by ischemia-reperfusion is inhibited by adenosine A2A receptor activation. Am J Physiol Heart Circ Physiol 2003;284:H2360-H2367.
16. Ihrcke NS, Wrenshall LE, Lindman BJ, Platt JL. Role of heparan sulfate in immunesystem-blood vessel interactions. Immunol Today 1993;14:500-505.
17. Constantinescu AA, Vink H, Spaan JA. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler Thromb Vasc Biol 2003;23:1541-1547.
18. Hirsh J, Levine MN. Low molecular weight heparin. Blood 1992;79:1-17.
19. Ho G, Broze GJ Jr, Schwartz AL. Role of heparan sulfate proteoglycans in the uptake and degradation of tissue factor pathway inhibitor-coagulation factor Xa complexes. J Biol Chem 1997;272:16838-16844.
20. Meri S, Pangburn MK. Regulation of alternative pathway complement activation by glycosaminoglycans: specificity of the polyanion binding site on factor H. Biochem Biophys Res Commun 1994;198:52-59.
21. Wuillemin WA, te Velthuis H, Lubbers YT, de Ruig CP, Eldering E, Hack CE. Potentiation of C1 inhibitor by glycosaminoglycans: dextran sulfate species are effective inhibitors of in vitro complement activation in plasma. J Immunol 1997;159:1953-1960.
22. Laumonier T, Walpen A, Maurus C, Mohacsi PJ, Matozan K, Korchagina E, Bovin N, Vanhove B, Seebach JD, Rieben R. Dextran sulfate acts as an endothelial cell protectant and inhibits human complement and NK cell-mediated cytotoxicity against porcine cells. Transplantation 2003 2003;76:838-843.
23. Zeerleder S, Mauron T, Lammle B, Wuillemin WA. Effect of low-molecular weight dextran sulfate on coagulation and platelet function tests. Thromb Res 2002;105:441-446.
24. Dodge HT, Sandler H, Ballew DW, Lord JD Jr. The use of biplane angiocardigraphy for the measurement of left ventricular volume in man. Am Heart J 1960;60:762-776.
25. Klein HH, Puschmann S, Schaper J, Schaper W. The mechanisms of the tetrazolium reaction in identifying experimental myocardial infarction. Virchows Arch 1981;393:287-297.
26. Daha MR, Van Es LA. Enhanced alternative complement pathway-dependent degradation of soluble immunoglobulin aggregates by macrophages. Immunology 1981;43:513-518.
27. Thiruvikraman SV, Guha A, Roboz J, Taubman MB, Nemerson Y, Fallon JT. In situ localization of tissue factor in human atherosclerotic plaques by binding of digoxigenin-labeled factors VIIa and X. Lab Invest 1996;75:451-461.
28. Gollackner B, Goh SK, Qawi I, Buhler L, Knosalla C, Daniel S, Kaczmarek E, Awwad M, Cooper DK, Robson SC. Acute vascular rejection of xenografts: roles of natural and elicited xenoreactive antibodies in activation of vascular endothelial cells and induction of procoagulant activity. Transplantation 2004;77:1735-1741.
29. Friedrichs GS, Kilgore KS, Manley PJ, Gralinski MR, Lucchesi BR. Effects of heparin and N-acetyl heparin on ischemia/reperfusion-induced alterations in myocardial function in the rabbit isolated heart. Circ Res 1994;75:701-710.
30. Lauver DA, Booth EA, White AJ, Poradosu E, Lucchesi BR. Sulodexide (KRX-101) attenuates myocardial ischemia/reperfusion injury and the deposition of C-reactive protein in areas of infarction without affecting hemostasis. J Pharmacol Exp Ther 2005;312:794-800.
31. Black SC, Gralinski MR, Friedrichs GS, Kilgore KS, Driscoll EM, Lucchesi BR. Cardioprotective effects of heparin or N-acetylheparin in an in vivo model of myocardial ischaemic and reperfusion injury. Cardiovasc Res 1995;29:629-636.
32. Pinckard RN, O'Rourke RA, Crawford MH, Grover FS, McManus LM, Ghidoni JJ, Storrs SB, Olson MS. Complement localization and mediation of ischemic injury in baboon myocardium. J Clin Invest 1980;66:1050-1056.
33. Weisman HF, Bartow T, Leppo MK, Marsh HC Jr., Carson GR, Concino MF, Boyle MP, Roux KH, Weisfeldt ML, Fearon DT. Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing postischemic myocardial inflammation and necrosis. Science 1990;249:146-151.
34. Pratt JR, Jones ME, Dong J, Zhou W, Chowdhury P, Smith RA, Sacks SH. Nontransgenic hyperexpression of a complement regulator in donor kidney modulates transplant ischemia/reperfusion damage, acute rejection, and chronic nephropathy. Am J Pathol 2003;163:1457-1465.
35. de Zwaan C, Kleine AH, Diris JH, Glatz JF, Wellens HJ, Strengers PF, Tissing M, Hack CE, van Dieijen-Visser MP, Hermens WT. Continuous 48-h C1-inhibitor treatment, following reperfusion therapy, in patients with acute myocardial infarction. Eur Heart J 2002;23:1670-1677.
36. Rossen RD, Swain JL, Michael LH, Weakley S, Giannini E, Entman ML. Selective accumulation of the first component of complement and leukocytes in ischemic canine heart muscle. A possible initiator of an extra myocardial mechanism of ischemic injury. Circ Res 1985;57:119-130.
37. Kagiyama A, Savage HE, Michael LH, Hanson G, Entman ML, Rossen RD. Molecular basis of complement activation in ischemic myocardium: identification of specific molecules of mitochondrial origin that bind human C1q and fix complement. Circ Res 1989;64:607-615.
38. Birdsall HH, Green DM, Trial J, Youker KA, Burns AR, MacKay CR, LaRosa GJ, Hawkins HK, Smith CW, Michael LH, Entman ML, Rossen RD. Complement C5a, TGF-beta 1, and MCP-1, in sequence, induce migration of monocytes into ischemic canine myocardium within the first one to five hours after reperfusion. Circulation 1997;95:684-692.
39. de Vries B, Walter SJ, Peutz-Kootstra CJ, Wolfs TG, van Heurn LW, Buurman WA. The mannose-binding lectin-pathway is involved in complement activation in the course of renal ischemia-reperfusion injury. Am J Pathol 2004;165:1677-1688.
40. Jordan JE, Montalto MC, Stahl GL. Inhibition of mannose-binding lectin reduces postischemic myocardial reperfusion injury. Circulation 2001;104:1413-1418.
41. Esmon CT. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. Faseb J 1995;9:946-955.
42. Marcum JA, Atha DH, Fritze LM, Nawroth P, Stern D, Rosenberg RD. Cloned bovine aortic endothelial cells synthesize anticoagulantly active heparan sulfate proteoglycan. J Biol Chem 1986;261:7507-7517.
43. Chen D, Giannopoulos K, Shiels PG, Webster Z, McVey JH, Kemball-Cook G, Tuddenham E, Moore M, Lechler R, Dorling A. Inhibition of intravascular thrombosis in murine endotoxemia by targeted expression of hirudin and tissue factor pathway inhibitor analogs to activated endothelium. Blood 2004;104:1344-1349.
44. Chou J, Mackman N, Merrill-Skoloff G, Pedersen B, Furie BC, Furie B. Hematopoietic cell-derived microparticle tissue factor contributes to fibrin formation during thrombus propagation. Blood 2004;104:3190-3197.
45. Ruf W, Edgington TS. Structural biology of tissue factor, the initiator of thrombogenesis in vivo. Faseb J 1994;8:385-390.
46. Golino P, Ragni M, Cirillo P, Scognamiglio A, Ravera A, Buono C, Guarino A, Piro O, Lambiase C, Botticella F, Ezban M, Condorelli M, Chiariello M. Recombinant human, active site-blocked factor VIIa reduces infarct size and no-reflow phenomenon in rabbits. Am J Physiol Heart Circ Physiol 2000;278:H1507-H1516.
47. Horstick G, Heimann A, Gotze O, Hafner G, Berg O, Boehmer P, Becker P, Darius H, Rupprecht HJ, Loos M, Bhakdi S, Meyer J, Kempski O. Intracoronary application of C1 esterase inhibitor improves cardiac function and reduces myocardial necrosis in an experimental model of ischemia and reperfusion. Circulation 1997;95:701-708.
48. Vakeva AP, Agah A, Rollins SA, Matis LA, Li L, Stahl GL. Myocardial infarction and apoptosis after myocardial ischemia and reperfusion: role of the terminal complement components and inhibition by anti-C5 therapy. Circulation 1998;97:2259-2267.
49. Solomon SD, Glynn RJ, Greaves S, Ajani U, Rouleau JL, Menapace F, Arnold JM, Hennekens C, Pfeffer MA. Recovery of ventricular function after myocardial infarction in the reperfusion era: the healing and early afterload reducing therapy study. Ann Intern Med 2001;134:451-458.
50. Antoniucci D, Valenti R, Migliorini A, Moschi G, Trapani M, Buonamici P, Cerisano G, Bolognese L, Santoro GM. Relation of time to treatment and mortality in patients with acute myocardial infarction undergoing primary coronary angioplasty. Am J Cardiol 2002;89:1248-1252.
51. De Luca G, van't Hof AW, de Boer MJ, Ottervanger JP, Hoorntje JC, Gosselink AT, Dambrink JH, Zijlstra F, Suryapranata H. Time-to-treatment significantly affects the extent of ST-segment resolution and myocardial blush in patients with acute myocardial infarction treated by primary angioplasty. Eur Heart J 2004;25:1009-1013.
52. Garcia-Dorado D, Theroux P, Elizaga J, Galinanes M, Solares J, Riesgo M, Gomez MJ, Garcia-Dorado A, Fernandez Aviles F. Myocardial reperfusion in the pig heart model: infarct size and duration of coronary occlusion. Cardiovasc Res 1987;21:537-544.
53. Reimer KA, Vander Heide RS, Richard VJ. Reperfusion in acute myocardial infarction: effect of timing and modulating factors in experimental models. Am J Cardiol 1993;72:13G-21G.
54. Maxwell MP, Hearse DJ, Yellon DM. Species variation in the coronary collateral circulation during regional myocardial ischaemia: a critical determinant of the rate of evolution and extent of myocardial infarction. Cardiovasc Res 1987;21:737-746.
55. Schaper W, Frenzel H, Hort W. Experimental coronary artery occlusion. I. Measurement of infarct size. Basic Res Cardiol 1979;74:46-53.
56. Ito WD, Schaarschmidt S, Klask R, Hansen S, Schafer HJ, Mathey D, Bhakdi S. Infarct size measurement by triphenyltetrazolium chloride staining versus in vivo injection of propidium iodide. J Mol Cell Cardiol 1997;29:2169-2175.
57. Wolff RA, Chien GL, van Winkle DM. Propidium iodide compares favorably with histology and triphenyl tetrazolium chloride in the assessment of experimentally-induced infarct size. J Mol Cell Cardiol 2000;32:225-232.
58. van den Berg BM, Vink H, Spaan JA. The endothelial glycocalyx protects against myocardial edema. Circ Res 2003;92:592-594.
59. Mulivor AW, Lipowsky HH. Role of glycocalyx in leukocyte-endothelial cell adhesion. Am J Physiol Heart Circ Physiol 2002;283:H1282-H1291.