Cyclophilin A affects inflammation, virus elimination and myocardial fibrosis in coxsackievirus B3-induced myocarditis

Journal of Molecular and Cellular Cardiology

Volumn 53, Issue 1, 2012, Pages 6-14

  Seizer, Peter ^a   Klingel, Karin ^a   Sauter, Martina ^a   Westermann, Dirk ^b   Ochmann, Carmen ^a   Schönberger, Tanja ^a   Schleicher, Rebecca ^a   Stellos, Konstantinos ^a   Schmidt, Eva Maria ^a   Borst, Oliver ^a   Bigalke, Boris ^a,c   Kandolf, Reinhard ^a   Langer, Harald ^a   Gawaz, Meinrad ^a   May, Andreas E ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

Cyclophilin a; Fibrosis; Inflammation; Myocarditis

Indexed keywords

CD147 ANTIGEN; CYCLOPHILIN A; CYCLOSPORIN A [4 N METHYLISOLEUCINE]; GELATINASE A; GELATINASE B; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS B3; DRUG ACTIVITY; DRUG EFFICACY; DRUG PROTEIN BINDING; HEART MUSCLE FIBROSIS; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; T LYMPHOCYTE; UPREGULATION; VIRUS REPLICATION; ZYMOGRAPHY;

ANIMALS; ANTIGENS, CD147; CELL LINE; COXSACKIEVIRUS INFECTIONS; CYCLOPHILIN A; CYCLOSPORINE; ENDOMYOCARDIAL FIBROSIS; ENTEROVIRUS B, HUMAN; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASE 9; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MONOCYTES; MYOCARDITIS; T-LYMPHOCYTES; VENTRICULAR REMODELING;

COXSACKIEVIRUS; MURINAE; MUS;

EID: 84861963152     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.03.004     Document Type: Article

References (45)

1. Kindermann I., Kindermann M., Kandolf R., Klingel K., Bultmann B., Muller T., et al. Predictors of outcome in patients with suspected myocarditis. Circulation Aug 5 2008, 118(6):639-648.
2. Mahrholdt H., Wagner A., Deluigi C.C., Kispert E., Hager S., Meinhardt G., et al. Presentation, patterns of myocardial damage, and clinical course of viral myocarditis. Circulation Oct 10 2006, 114(15):1581-1590.
3. Henke A., Huber S., Stelzner A., Whitton J.L. The role of CD8+ T lymphocytes in coxsackievirus B3-induced myocarditis. J Virol Nov 1995, 69(11):6720-6728.
4. Chow L.H., Beisel K.W., McManus B.M. Enteroviral infection of mice with severe combined immunodeficiency. Evidence for direct viral pathogenesis of myocardial injury. Lab Invest Jan 1992, 66(1):24-31.
5. Sallusto F., Mackay C.R., Lanzavecchia A. The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 2000, 18:593-620.
6. Shen Y., Xu W., Chu Y.W., Wang Y., Liu Q.S., Xiong S.D. Coxsackievirus group B type 3 infection upregulates expression of monocyte chemoattractant protein 1 in cardiac myocytes, which leads to enhanced migration of mononuclear cells in viral myocarditis. J Virol Nov 2004, 78(22):12548-12556.
7. Yuan J., Liu Z., Lim T., Zhang H., He J., Walker E., et al. CXCL10 inhibits viral replication through recruitment of natural killer cells in coxsackievirus B3-induced myocarditis. Circ Res Mar 13 2009, 104(5):628-638.
8. Fairweather D., Frisancho-Kiss S., Yusung S.A., Barrett M.A., Davis S.E., Gatewood S.J., et al. Interferon-gamma protects against chronic viral myocarditis by reducing mast cell degranulation, fibrosis, and the profibrotic cytokines transforming growth factor-beta 1, interleukin-1 beta, and interleukin-4 in the heart. Am J Pathol Dec 2004, 165(6):1883-1894.
9. Weinzierl A.O., Szalay G., Wolburg H., Sauter M., Rammensee H.G., Kandolf R., et al. Effective chemokine secretion by dendritic cells and expansion of cross-presenting CD4-/CD8+ dendritic cells define a protective phenotype in the mouse model of coxsackievirus myocarditis. J Virol Aug 2008, 82(16):8149-8160.
10. Sherry B., Yarlett N., Strupp A., Cerami A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci U S A Apr 15 1992, 89(8):3511-3515.
11. Fischer G., Schmid F.X. The mechanism of protein folding. Implications of in vitro refolding models for de novo protein folding and translocation in the cell. Biochemistry Mar 6 1990, 29(9):2205-2212.
12. Handschumacher R.E., Harding M.W., Rice J., Drugge R.J., Speicher D.W. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science Nov 2 1984, 226(4674):544-547.
13. Ponticelli C., Scolari M.P. Calcineurin inhibitors in renal transplantation still needed but in reduced doses: a review. Transplant Proc Jul 2010, 42(6):2205-2208.
14. Steinkasserer A., Harrison R., Billich A., Hammerschmid F., Werner G., Wolff B., et al. Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus type 1 (HIV-1): interference with early and late events in HIV-1 replication. J Virol Feb 1995, 69(2):814-824.
15. Fischer G., Gallay P., Hopkins S. Cyclophilin inhibitors for the treatment of HCV infection. Curr Opin Investig Drugs Aug 2010, 11(8):911-918.
16. Nigro P., Satoh K., O'Dell M.R., Soe N.N., Cui Z., Mohan A., et al. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med Jan 17 2011, 208(1):53-66.
17. Satoh K., Matoba T., Suzuki J., O'Dell M.R., Nigro P., Cui Z., et al. Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation Jun 17 2008, 117(24):3088-3098.
18. Satoh K., Nigro P., Matoba T., O'Dell M.R., Cui Z., Shi X., et al. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med Jun 2009, 15(6):649-656.
19. Seizer P., Ochmann C., Schonberger T., Zach S., Rose M., Borst O., et al. Disrupting the EMMPRIN (CD147)-cyclophilin A interaction reduces infarct size and preserves systolic function after myocardial ischemia and reperfusion. Arterioscler Thromb Vasc Biol Jun 2011, 31(6):1377-1386.
20. Arora K., Gwinn W.M., Bower M.A., Watson A., Okwumabua I., MacDonald H.R., et al. Extracellular cyclophilins contribute to the regulation of inflammatory responses. J Immunol Jul 1 2005, 175(1):517-522.
21. Gwinn W.M., Damsker J.M., Falahati R., Okwumabua I., Kelly-Welch A., Keegan A.D., et al. Novel approach to inhibit asthma-mediated lung inflammation using anti-CD147 intervention. J Immunol Oct 1 2006, 177(7):4870-4879.
22. Seizer P., Geisler T., Bigalke B., Schneider M., Klingel K., Kandolf R. EMMPRIN and its ligand cyclophilin A as novel diagnostic markers in inflammatory cardiomyopathy. Int J Cardiol Jul 1 2011.
23. Rosenwirth B., Billich A., Datema R., Donatsch P., Hammerschmid F., Harrison R., et al. Inhibition of human immunodeficiency virus type 1 replication by SDZ NIM 811, a nonimmunosuppressive cyclosporine analog. Antimicrob Agents Chemother 1994, 38(8):1763-1772.
24. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int 2009, 11(7):36-42.
25. Kandolf R., Hofschneider P.H. 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 U S A Jul 1985, 82(14):4818-4822.
26. Szalay G., Sauter M., Haberland M., Zuegel U., Steinmeyer A., Kandolf R., et al. Osteopontin: a fibrosis-related marker molecule in cardiac remodeling of enterovirus myocarditis in the susceptible host. Circ Res Apr 10 2009, 104(7):851-859.
27. Szalay G., Sauter M., Hald J., Weinzierl A., Kandolf R., Klingel K. Sustained nitric oxide synthesis contributes to immunopathology in ongoing myocarditis attributable to interleukin-10 disorders. Am J Pathol Dec 2006, 169(6):2085-2093.
28. Seizer P., Schonberger T., Schott M., Lang M.R., Langer H.F., Bigalke B., et al. EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis Mar 2010, 209(1):51-57.
29. Klingel K., Hohenadl C., Canu A., Albrecht M., Seemann M., Mall G., et al. Ongoing enterovirus-induced myocarditis is associated with persistent heart muscle infection: quantitative analysis of virus replication, tissue damage, and inflammation. Proc Natl Acad Sci U S A Jan 1 1992, 89(1):314-318.
30. Colgan J., Asmal M., Neagu M., Yu B., Schneidkraut J., Lee Y., et al. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity Aug 2004, 21(2):189-201.
31. Ma S., Boerner J.E., TiongYip C., Weidmann B., Ryder N.S., Cooreman M.P., et al. NIM811, a cyclophilin inhibitor, exhibits potent in vitro activity against hepatitis C virus alone or in combination with alpha interferon. Antimicrob Agents Chemother Sep 2006, 50(9):2976-2982.
32. Rosado J.A., Pariente J.A., Salido G.M., Redondo P.C. SERCA2b activity is regulated by cyclophilins in human platelets. Arterioscler Thromb Vasc Biol Mar 2010, 30(3):419-425.
33. Yurchenko V., Constant S., Bukrinsky M. Dealing with the family: CD147 interactions with cyclophilins. Immunology Mar 2006, 117(3):301-309.
34. Damsker J.M., Okwumabua I., Pushkarsky T., Arora K., Bukrinsky M.I., Constant S.L. Targeting the chemotactic function of CD147 reduces collagen-induced arthritis. Immunology Jan 2009, 126(1):55-62.
35. Piot C., Croisille P., Staat P., Thibault H., Rioufol G., Mewton N., et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med Jul 31 2008, 359(5):473-481.
36. Wang H., Zhang Y., Wang T., You H., Jia J. N-methyl-4-isoleucine cyclosporine attenuates CCl -induced liver fibrosis in rats by interacting with cyclophilin B and D. J Gastroenterol Hepatol Mar 2011, 26(3):558-567.
37. Spinale F.G., Coker M.L., Heung L.J., Bond B.R., Gunasinghe H.R., Etoh T., et al. A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure. Circulation Oct 17 2000, 102(16):1944-1949.
38. Rutschow S., Leschka S., Westermann D., Puhl K., Weitz A., Ladyszenskij L., et al. Left ventricular enlargement in coxsackievirus-B3 induced chronic myocarditis-ongoing inflammation and an imbalance of the matrix degrading system. Eur J Pharmacol Mar 25 2010, 630(1-3):145-151.
39. Ducharme A., Frantz S., Aikawa M., Rabkin E., Lindsey M., Rohde L.E., et al. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest Jul 2000, 106(1):55-62.
40. Romanic A.M., Harrison S.M., Bao W., Burns-Kurtis C.L., Pickering S., Gu J., et al. Myocardial protection from ischemia/reperfusion injury by targeted deletion of matrix metalloproteinase-9. Cardiovasc Res Jun 2002, 54(3):549-558.
41. Cheung C., Marchant D., Walker E.K., Luo Z., Zhang J., Yanagawa B., et al. Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation Mar 25 2008, 117(12):1574-1582.
42. Jin Z.G., Melaragno M.G., Liao D.F., Yan C., Haendeler J., Suh Y.A., et al. Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res Oct 27 2000, 87(9):789-796.
43. Liao D.F., Jin Z.G., Baas A.S., Daum G., Gygi S.P., Aebersold R., et al. Purification and identification of secreted oxidative stress-induced factors from vascular smooth muscle cells. J Biol Chem Jan 7 2000, 275(1):189-196.
44. Coppinger J.A., Cagney G., Toomey S., Kislinger T., Belton O., McRedmond J.P., et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood Mar 15 2004, 103(6):2096-2104.
45. Balsley M.A., Malesevic M., Stemmy E.J., Gigley J., Jurjus R.A., Herzog D., et al. A cell-impermeable cyclosporine A derivative reduces pathology in a mouse model of allergic lung inflammation. J Immunol Dec 15 2010, 185(12):7663-7670.