Inhibition of coagulation factor xa improves myocardial function during CVB3-induced myocarditis

Cardiovascular Therapeutics

Volumn 32, Issue 3, 2014, Pages 113-119

  Malz, Ronny ^a   Weithauser, Alice ^a   Tschöpe, Carsten ^a   Schultheiss, Heinz Peter ^a   Rauch, Ursula ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Factor Xa; Fondaparinux; Inflammation; Myocarditis; Remodeling

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 10A INHIBITOR; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COMPLEMENTARY DNA; CYTOKINE; FONDAPARINUX; GELATINASE A; MESSENGER RNA; RNA; AUTACOID; MMP2 PROTEIN, MOUSE; POLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING DISORDER; CONTROLLED STUDY; COXSACKIE VIRUS B3; COXSACKIE VIRUS INFECTION; CYTOKINE PRODUCTION; DRUG EFFECT; HEART LEFT VENTRICLE FUNCTION; HEART VENTRICLE REMODELING; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; VIRUS LOAD; VIRUS MYOCARDITIS; ANIMAL; BLOOD; C57BL MOUSE; COXSACKIEVIRUS INFECTIONS; DISEASE MODEL; DRUG EFFECTS; ENTEROVIRUS; GENETICS; MALE; METABOLISM; PATHOGENICITY; PATHOPHYSIOLOGY; VIROLOGY;

ANIMALS; COXSACKIEVIRUS INFECTIONS; CYTOKINES; DISEASE MODELS, ANIMAL; ENTEROVIRUS B, HUMAN; FACTOR XA; FACTOR XA INHIBITORS; INFLAMMATION MEDIATORS; MALE; MATRIX METALLOPROTEINASE 2; MICE, INBRED C57BL; MYOCARDITIS; POLYSACCHARIDES; RNA, MESSENGER; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING; VIRAL LOAD;

EID: 84899087567     PISSN: 17555914     EISSN: 17555922     Source Type: Journal    
DOI: 10.1111/1755-5922.12069     Document Type: Article

References (33)

1. Klingel K, Stephan S, Sauter M, Zell R, McManus BM, Bultmann B, Kandolf R. Pathogenesis of murine enterovirus myocarditis: Virus dissemination and immune cell targets. J Virol 1996;70:8888-8895.
2. Schultheiss HP, Kuhl U. Why is diagnosis of infectious myocarditis such a challenge? Expert Rev Anti-Infect Ther 2011;9:1093-1095.
3. Antoniak S, Boltzen U, Riad A, et al. Viral myocarditis and coagulopathy: Increased tissue factor expression and plasma thrombogenicity. J Mol Cell Cardiol 2008;45:118-126.
4. Funderburg NT, Mayne E, Sieg SF, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: Relationship to in vivo coagulation and immune activation. Blood 2010;115:161-167.
5. Antoniak S, Boltzen U, Eisenreich A, Stellbaum C, Poller W, Schultheiss HP, Rauch U. Regulation of cardiomyocyte full-length tissue factor expression and microparticle release under inflammatory conditions in vitro. J Thromb Haemost 2009;7:871-878.
6. Antoniak S, Rojas M, Spring D, et al. Protease-activated receptor 2 deficiency reduces cardiac ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 2010;30:2136-2142.
7. Barnes JA, Singh S, Gomes AV. Protease activated receptors in cardiovascular function and disease. Mol Cell Biochem 2004;263:227-239.
8. Pepke W, Eisenreich A, Jaster M, et al. Bivalirudin inhibits periprocedural platelet function and tissue factor expression of human smooth muscle cells. Cardiovasc Ther 2013;31:115-123.
9. Rauch U, Nemerson Y. Circulating tissue factor and thrombosis. Curr Opin Hematol 2000;7:273-277.
10. Szotowski B, Antoniak S, Rauch U. Alternatively spliced tissue factor: A previously unknown piece in the puzzle of hemostasis. Trends Cardiovasc Med 2006;16:177-182.
11. Golino P, Ragni M, Cimmino G, Forte L. Role of tissue factor pathway inhibitor in the regulation of tissue factor-dependent blood coagulation. Cardiovasc Drug Rev 2002;20:67-80.
12. Borensztajn K, Peppelenbosch MP, Spek CA. Factor Xa: At the crossroads between coagulation and signaling in physiology and disease. Trends Mol Med 2008;14:429-440.
13. Borensztajn K, Peppelenbosch MP, Spek CA. Coagulation factor Xa signaling: The link between coagulation and inflammatory bowel disease? Trends Pharmacol Sci 2009;30:8-16.
14. Pejler G, Lunderius C, Tomasini-Johansson B. Macrophages synthesize factor X and secrete factor X/Xa-containing prothrombinase activity into the surrounding medium. Thromb Haemost 2000;84:429-435.
15. Rauch BH, Bretschneider E, Braun M, Schror K. Factor Xa releases matrix metalloproteinase-2 (MMP-2) from human vascular smooth muscle cells and stimulates the conversion of pro-MMP-2 to MMP-2: Role of MMP-2 in factor Xa-induced DNA synthesis and matrix invasion. Circ Res 2002;90:1122-1127.
16. Li J, Leschka S, Rutschow S, et al. Immunomodulation by interleukin-4 suppresses matrix metalloproteinases and improves cardiac function in murine myocarditis. Eur J Pharmacol 2007;554:60-68.
17. Okamoto H, Imanaka-Yoshida K. Matricellular proteins: New molecular targets to prevent heart failure. Cardiovasc Ther 2012;30:e198-e209.
18. Apostolakis S, Lip GY, Lane DA, Shantsila E. The quest for new anticoagulants: From clinical development to clinical practice. Cardiovasc Ther 2011;29:e12-e22.
19. Kandolf R, Hofschneider PH. Molecular cloning of the genome of a cardiotropic Coxsackie B3 virus: Full-length reverse-transcribed recombinant cDNA generates infectious virus in mammalian cells. Proc Natl Acad Sci USA 1985;82:4818-4822.
20. Szalay G, Meiners S, Voigt A, et al. Ongoing coxsackievirus myocarditis is associated with increased formation and activity of myocardial immunoproteasomes. Am J Pathol 2006;168:1542-1552.
21. Ebermann L, Wika S, Klumpe I, et al. The mitochondrial respiratory chain has a critical role in the antiviral process in Coxsackievirus B3-induced myocarditis. Lab Invest. 2012;92:125-134.
22. Szotowski B, Goldin-Lang P, Antoniak S, et al. Alterations in myocardial tissue factor expression and cellular localization in dilated cardiomyopathy. J Am Coll Cardiol 2005;45:1081-1089.
23. Noutsias M, Pauschinger M, Kuhl U, Schultheiss HP. [Myocarditis and dilated cardiomyopathy. New methods in diagnosis and therapy]. MMW Fortschr Med. 2002;144:36-40. Myokarditis und dilatative Kardiomyopathie. Neue Wege in Diagnostik und Therapie.
24. Pauschinger M, Phan MD, Doerner A, et al. Enteroviral RNA replication in the myocardium of patients with left ventricular dysfunction and clinically suspected myocarditis. Circulation 1999;99:889-895.
25. Li J, Schwimmbeck PL, Tschope C, et al. Collagen degradation in a murine myocarditis model: Relevance of matrix metalloproteinase in association with inflammatory induction. Cardiovasc Res 2002;56:235-247.
26. Frizelle S, Schwarz J, Huber SA, Leslie K. Evaluation of the effects of low molecular weight heparin on inflammation and collagen deposition in chronic coxsackievirus B3-induced myocarditis in A/J mice. Am J pathol 1992;141:203-209.
27. Zucker S, Conner C, DiMassmo BI, Ende H, Drews M, Seiki M, Bahou WF. Thrombin induces the activation of progelatinase A in vascular endothelial cells. Physiologic regulation of angiogenesis. J Biol Chem 1995;270:23730-23738.
28. Marchant D, McManus BM. Matrix metalloproteinases in the pathogenesis of viral heart disease. Trends Cardiovasc Med 2009;19:21-26.
29. Westermann D, Savvatis K, Lindner D, et al. Reduced degradation of the chemokine MCP-3 by matrix metalloproteinase-2 exacerbates myocardial inflammation in experimental viral cardiomyopathy. Circulation 2011;124:2082-2093.
30. Matsusaka H, Ikeuchi M, Matsushima S, et al. Selective disruption of MMP-2 gene exacerbates myocardial inflammation and dysfunction in mice with cytokine-induced cardiomyopathy. Am J Physiol Heart Circ Physiol 2005;289:H1858-H1864.
31. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011;11:723-737.
32. Dayan V, Yannarelli G, Billia F, Filomeno P, Wang XH, Davies JE, Keating A. Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction. Basic Res Cardiol 2011;106:1299-1310.
33. Weithauser A, Bobbert P, Antoniak S, et al. Protease-activated receptor 2 regulates the innate immune response to viral infection in a CVB3-induced myocarditis. J Am Coll Cardiol 2013;62;1737-1745.