IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR

Circulation Research

Volumn 104, Issue 2, 2009, Pages

  Krishnamurthy, Prasanna ^a   Rajasingh, Johnson ^a   Lambers, Erin ^a   Qin, Gangjian ^a   Losordo, Douglas W ^a   Kishore, Raj ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cardiac remodeling; Cytokines; IL 10; Inflammation; Myocardial infarction

Indexed keywords

GELATINASE B; HUR PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; RECOMBINANT INTERLEUKIN 10; SMALL INTERFERING RNA; SODIUM CHLORIDE; STAT3 PROTEIN; ANTIINFLAMMATORY AGENT; AUTACOID; ELAV-LIKE PROTEIN 1; INTERLEUKIN 10; MEMBRANE ANTIGEN; MMP9 PROTEIN, MOUSE; RECOMBINANT PROTEIN; RNA BINDING PROTEIN; STAT3 PROTEIN, MOUSE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE; HEART MUSCLE FIBROSIS; HEART VENTRICLE REMODELING; INFLAMMATION; INFLAMMATORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANGIOGENESIS; ANIMAL; APOPTOSIS; ARTERIOLE; C57BL MOUSE; CAPILLARY; CELL STRAIN 3T3; DISEASE MODEL; DRUG EFFECT; FIBROSIS; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; TIME;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, SURFACE; APOPTOSIS; ARTERIOLES; CAPILLARIES; DISEASE MODELS, ANIMAL; FIBROSIS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-10; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; MYOCARDIAL INFARCTION; MYOCARDIUM; NEOVASCULARIZATION, PHYSIOLOGIC; NIH 3T3 CELLS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 59849089688     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.188243     Document Type: Article

References (43)

1. Bujak M, Ren G, Kweon HJ, Dobaczewski M, Reddy A, Taffet G, Wang XF, Frangogiannis NG. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation. 2007;116: 2127-2138.
2. Frangogiannis NG. Targeting the inflammatory response in healing myo-cardial infarcts. Curr Med Chem. 2006;13:1877-1893.
3. Huebener P, Abou-Khamis T, Zymek P, Bujak M, Ying X, Chatila K, Haudek S, Thakker G, Frangogiannis NG. CD44 is critically involved in infarct healing by regulating the inflammatory and fibrotic response. J Immunol. 2008;180:2625-2633.
4. Timmers L, Sluijter JP, van Keulen JK, Hoefer IE, Nederhoff MG, Goumans MJ, Doevendans PA, van Echteld CJ, Joles JA, Quax PH, Piek JJ, Pasterkamp G, de Kleijn DP. Toll-like receptor 4 mediates mal-adaptive left ventricular remodeling and impairs cardiac function after myocardial infarction. Circ Res. 2008;102:257-264.
5. Tao ZY, Cavasin MA, Yang F, Liu YH, Yang XP. Temporal changes in matrix metalloproteinase expression and inflammatory response associated with cardiac rupture after myocardial infarction in mice. Life Sci. 2004;74:1561-1572.
6. Matsumura S, Iwanaga S, Mochizuki S, Okamoto H, Ogawa S, Okada Y. Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice. J Clin Invest. 2005; 115:599-609.
7. Sun M, Dawood F, Wen WH, Chen M, Dixon I, Kirshenbaum LA, Liu PP. Excessive tumor necrosis factor activation after infarction contributes to susceptibility of myocardial rupture and left ventricular dysfunction. Circulation. 2004;110:3221-3228.
8. Frangogiannis NG, Mendoza LH, Lindsey ML, Ballantyne CM, Michael LH, Smith CW, Entman ML. IL-10 is induced in the reperfused myocardium and may modulate the reaction to injury. J Immunol. 2000;165: 2798-2808.
9. Yao L, Huang K, Huang D, Wang J, Guo H, Liao Y. Acute myocardial infarction induced increases in plasma tumor necrosis factor-alpha and interleukin-10 are associated with the activation of poly(ADP-ribose) polymerase of circulating mononuclear cell. Int J Cardiol. 2008;123: 366-368.
10. Rajasingh J, Bord E, Luedemann C, Asai J, Hamada H, Thorne T, Qin G, Goukassian D, Zhu Y, Losordo DW, Kishore R. IL-10-induced TNF-alpha mRNA destabilization is mediated via IL-10 suppression of p38 MAP kinase activation and inhibition of HuR expression. FASEB J. 2006;20:2112-2114.
11. Bellahcene M, Jacquet S, Cao XB, Tanno M, Haworth RS, Layland J, Kabir AM, Gaestel M, Davis RJ, Flavell RA, Shah AM, Avkiran M, Marber MS. Activation of p38 mitogen-activated protein kinase contributes to the early cardiodepressant action of tumor necrosis factor. J Am Coll Cardiol. 2006;48:545-555.
12. Li Z, Ma JY, Kerr I, Chakravarty S, Dugar S, Schreiner G, Protter AA. Selective inhibition of p38alpha MAPK improves cardiac function and reduces myocardial apoptosis in rat model of myocardial injury. Am J Physiol Heart Circ Physiol. 2006;291:H1972-H1977.
13. Wang M, Tsai BM, Turrentine MW, Mahomed Y, Brown JW, Meldrum DR. p38 mitogen activated protein kinase mediates both death signaling and functional depression in the heart. Ann Thorac Surg. 2005;80: 2235-2241.
14. Hilfiker-Kleiner D, Hilfiker A, Fuchs M, Kaminski K, Schaefer A, Schieffer B, Hillmer A, Schmiedl A, Ding Z, Podewski E, Podewski E, Poli V, Schneider MD, Schulz R, Park JK, Wollert KC, Drexler H. Signal transducer and activator of transcription 3 is required for myocardial capillary growth, control of interstitial matrix deposition, and heart protection from ischemic injury. Circ Res. 2004;95:187-195.
15. Jacoby JJ, Kalinowski A, Liu MG, Zhang SS, Gao Q, Chai GX, Ji L, Iwamoto Y, Li E, Schneider M, Russell KS, Fu XY. Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc Natl Acad Sci U S A. 2003;100:12929-12934.
16. Krishnamurthy P, Subramanian V, Singh M, Singh K. Deficiency of beta1 integrins results in increased myocardial dysfunction after myo-cardial infarction. Heart. 2006;92:1309-1315.
17. Finsen AV, Christensen G, Sjaastad I. Echocardiographic parameters discriminating myocardial infarction with pulmonary congestion from myocardial infarction without congestion in the mouse. J Appl Physiol. 2005;98:680-689.
18. Ii M, Nishimura H, Iwakura A, Wecker A, Eaton E, Asahara T, Losordo DW. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation. 2005;111:1114-1120.
19. Qin G, Kishore R, Dolan CM, Silver M, Wecker A, Luedemann CN, Thorne T, Hanley A, Curry C, Heyd L, Dinesh D, Kearney M, Martelli F, Murayama T, Goukassian DA, Zhu Y, Losordo DW. Cell cycle regulator E2F1 modulates angiogenesis via p53-dependent transcriptional control of VEGF. Proc Natl Acad Sci U S A. 2006;103:11015-11020.
20. Goukassian DA, Qin G, Dolan C, Murayama T, Silver M, Curry C, Eaton E, Luedemann C, Ma H, Asahara T, Zak V, Mehta S, Burg A, Thorne T, Kishore R, Losordo DW. Tumor necrosis factor-alpha receptor p75 is required in ischemia-induced neovascularization. Circulation. 2007;115: 752-762.
21. Luo D, Luo Y, He Y, Zhang H, Zhang R, Li X, Dobrucki WL, Sinusas AJ, Sessa WC, Min W. Differential functions of tumor necrosis factor receptor 1 and 2 signaling in ischemia-mediated arteriogenesis and angio-genesis. Am J Pathol. 2006;169:1886-1898.
22. Higuchi Y, McTiernan CF, Frye CB, McGowan BS, Chan TO, Feldman AM. Tumor necrosis factor receptors 1 and 2 differentially regulate survival, cardiac dysfunction, and remodeling in transgenic mice with tumor necrosis factor-alpha-induced cardiomyopathy. Circulation. 2004; 109:1892-1897.
23. Huwiler A, Akool el S, Aschrafi A, Hamada FM, Pfeilschifter J, Eberhardt W. ATP potentiates interleukin-1 beta-induced MMP-9 expression in mesangial cells via recruitment of the ELAV protein HuR. J Biol Chem. 2003;278:51758- 51769.
24. Ono K, Matsumori A, Shioi T, Furukawa Y, Sasayama S. Cytokine gene expression after myocardial infarction in rat hearts: possible implication in left ventricular remodeling. Circulation. 1998;98:149-156.
25. Li Y, Takemura G, Okada H, Miyata S, Maruyama R, Li L, Higuchi M, Minatoguchi S, Fujiwara T, Fujiwara H. Reduction of inflammatory cytokine expression and oxidative damage by erythropoietin in chronic heart failure. Cardiovasc Res. 2006;71:684-694.
26. Mayer B, Holmer SR, Hengstenberg C, Lieb W, Pfeifer M, Schunkert H. Functional improvement in heart failure patients treated with beta-blockers is associated with a decline of cytokine levels. Int J Cardiol. 2005;103:182-186.
27. Suzuki K, Murtuza B, Smolenski RT, Sammut IA, Suzuki N, Kaneda Y, Yacoub MH. Overexpression of interleukin-1 receptor antagonist provides cardioprotection against ischemia-reperfusion injury associated with reduction in apoptosis. Circulation. 2001;104:I308-I303.
28. Yeh CH, Chen TP, Wu YC, Lin YM, Jing Lin P. Inhibition of NFkappaB activation with curcumin attenuates plasma inflammatory cytokines surge and cardiomyocytic apoptosis following cardiac ischemia/reperfusion. J Surg Res. 2005;125:109-116.
29. Sun M, Chen M, Dawood F, Zurawska U, Li JY, Parker T, Kassiri Z, Kirshenbaum LA, Arnold M, Khokha R, Liu PP. Tumor necrosis factor-alpha mediates cardiac remodeling and ventricular dysfunction after pressure overload state. Circulation. 2007;115:1398-1407.
30. Aukrust P, Yndestad A, Damas JK, Gullestad L. Inflammation and chronic heart failure-potential therapeutic role of intravenous immuno-globulin. Autoimmun Rev. 2004;3:221-227.
31. Duncan DJ, Hopkins PM, Harrison SM. Negative inotropic effects of tumour necrosis factor-alpha and interleukin-1beta are ameliorated by alfentanil in rat ventricular myocytes. Br J Pharmacol. 2007;150: 720-726.
32. Sugishita K, Kinugawa K, Shimizu T, Harada K, Matsui H, Takahashi T, Serizawa T, Kohmoto O. Cellular basis for the acute inhibitory effects of IL-6 and TNF-alpha on excitation-contraction coupling. J Mol Cell Cardiol. 1999;31:1457-1467.
33. Burchfield JS, Iwasaki M, Koyanagi M, Urbich C, Rosenthal N, Zeiher AM, Dimmeler S. Interleukin-10 from transplanted bone marrow mono-nuclear cells contributes to cardiac protection after myocardial infarction. Circ Res. 2008;103:203-211.
34. Ahmed SH, Clark LL, Pennington WR, Webb CS, Bonnema DD, Leonardi AH, McClure CD, Spinale FG, Zile MR. Matrix metallopro-teinases/tissue inhibitors of metalloproteinases: relationship between changes in proteolytic determinants of matrix composition and structural, functional, and clinical manifestations of hypertensive heart disease. Circulation. 2006;113:2089-2096.
35. Mori S, Gibson G, McTiernan CF. Differential expression of MMPs and TIMPs in moderate and severe heart failure in a transgenic model. J Card Fail. 2006;12:314-325.
36. Brown RD, Jones GM, Laird RE, Hudson P, Long CS. Cytokines regulate matrix metalloproteinases and migration in cardiac fibroblasts. Biochem Biophys Res Commun. 2007;362:200-205.
37. Frangogiannis NG. The role of the chemokines in myocardial ischemia and reperfusion. Curr Vasc Pharmacol. 2004;2:163-174.
38. Heba G, Krzeminski T, Porc M, Grzyb J, Ratajska A, Dembinska-Kiec A. The time course of tumor necrosis factor-alpha, inducible nitric oxide synthase and vascular endothelial growth factor expression in an experimental model of chronic myocardial infarction in rats. J Vasc Res. 2001;38:288-300.
39. Lindsey ML, Escobar GP, Dobrucki LW, Goshorn DK, Bouges S, Mingoia JT, McClister DM Jr, Su H, Gannon J, MacGillivray C, Lee RT, Sinusas AJ, Spinale FG. Matrix metalloproteinase-9 gene deletion facilitates angiogenesis after myocardial infarction. Am J Physiol Heart Circ Physiol. 2006;290:H232-H239.
40. Lindsey ML, Gannon J, Aikawa M, Schoen FJ, Rabkin E, Lopresti-Morrow L, Crawford J, Black S, Libby P, Mitchell PG, Lee RT. Selective matrix metalloproteinase inhibition reduces left ventricular remodeling but does not inhibit angiogenesis after myocardial infarction. Circulation. 2002;105:753-758.
41. Cornelius LA, Nehring LC, Harding E, Bolanowski M, Welgus HG, Kobayashi DK, Pierce RA, Shapiro SD. Matrix metalloproteinases generate angiostatin: effects on neovascularization. J Immunol. 1998;161: 6845-6852.
42. Ing DJ, Zang J, Dzau VJ, Webster KA, Bishopric NH. Modulation of cytokine-induced cardiac myocyte apoptosis by nitric oxide, Bak, and Bcl-x. Circ Res. 1999;84:21-33.
43. Asadullah K, Sterry W, Volk HD. Interleukin-10 therapy-review of a new approach. Pharmacol Rev. 2003;55:241-269.