Regulatory T cells are recruited in the infarcted mouse myocardium and may modulate fibroblast phenotype and function

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 8, 2014, Pages H1233-H1242

  Saxena, Amit ^a   Dobaczewski, Marcin ^a   Rai, Vikrant ^a   Haque, Zaffar ^a   Chen, Wei ^a   Li, Na ^a   Frangogiannis, Nikolaos G ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Fibroblast; Inflammation; Lymphocyte; Myocardial infarction; Remodeling

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; MONOCYTE CHEMOTACTIC PROTEIN 1; STROMELYSIN; TRANSCRIPTION FACTOR FOXP3; ACTIN; ALPHA-SMOOTH MUSCLE ACTIN, MOUSE; COLLAGEN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MMP3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL THERAPY; CONTROLLED STUDY; DENDRITIC CELL; EFFECTOR CELL; FIBROBLAST; GENE EXPRESSION REGULATION; HEART DILATATION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE REPERFUSION; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; GENETICS; HEART CONTRACTION; HEART MUSCLE; HEART VENTRICLE REMODELING; METABOLISM; MYOFIBROBLAST; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REPERFUSION INJURY;

ACTINS; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL3; COLLAGEN; MATRIX METALLOPROTEINASE 3; MICE; MICE, INBRED C57BL; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOFIBROBLASTS; PHENOTYPE; T-LYMPHOCYTES, REGULATORY; VENTRICULAR REMODELING;

EID: 84908110191     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00328.2014     Document Type: Article

References (39)

1. Bujak M, Dobaczewski M, Gonzalez-Quesada C, Xia Y, Leucker T, Zymek P, Veeranna V, Tager AM, Luster AD, Frangogiannis NG. Induction of the CXC chemokine interferon-γ-inducible protein 10 regulates the reparative response following myocardial infarction. Circ Res 105: 973-983, 2009.
2. 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 116: 2127-2138, 2007.
3. Chandrasekar B, Smith JB, Freeman GL. Ischemia-reperfusion of rat myocardium activates nuclear factor-κB and induces neutrophil infiltration via lipopolysaccharide-induced CXC chemokine. Circulation 103: 2296-2302, 2001.
4. Chaudhry A, Rudensky AY. Control of inflammation by integration of environmental cues by regulatory T cells. J Clin Invest 123: 939-944, 2013.
5. Chen W, Saxena A, Li N, Sun J, Gupta A, Lee DW, Tian Q, Dobaczewski M, Frangogiannis NG. Endogenous IRAK-M attenuates postinfarction remodeling through effects on macrophages and fibroblasts. Arterioscler Thromb Vasc Biol 32: 2598-2608, 2012.
6. Christia P, Bujak M, Gonzalez-Quesada C, Chen W, Dobaczewski M, Reddy A, Frangogiannis NG. Systematic characterization of myocardial inflammation, repair, and remodeling in a mouse model of reperfused myocardial infarction. J Histochem Cytochem 61: 555-570, 2013.
7. Christia P, Frangogiannis NG. Targeting inflammatory pathways in myocardial infarction. Eur J Clin Invest 43: 986-995, 2013.
8. Collison LW, Workman CJ, Kuo TT, Boyd K, Wang Y, Vignali KM, Cross R, Sehy D, Blumberg RS, Vignali DA. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 450: 566-569, 2007.
9. Courties G, Heidt T, Sebas M, Iwamoto Y, Jeon D, Truelove J, Tricot B, Wojtkiewicz G, Dutta P, Sager HB, Borodovsky A, Novobrantseva T, Klebanov B, Fitzgerald K, Anderson DG, Libby P, Swirski FK, Weissleder R, Nahrendorf M. In vivo silencing of the transcription factor IRF5 reprograms the macrophage phenotype and improves infarct healing. J Am Coll Cardiol 63: 1556-1566, 2014.
10. D'Alessio FR, Tsushima K, Aggarwal NR, West EE, Willett MH, Britos MF, Pipeling MR, Brower RG, Tuder RM, McDyer JF, King LS. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J Clin Invest 119: 2898-2913, 2009.
11. Dewald O, Ren G, Duerr GD, Zoerlein M, Klemm C, Gersch C, Tincey S, Michael LH, Entman ML, Frangogiannis NG. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am J Pathol 164: 665-677, 2004.
12. Dewald O, Zymek P, Winkelmann K, Koerting A, Ren G, Abou-Khamis T, Michael LH, Rollins BJ, Entman ML, Frangogiannis NG. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ Res 96: 881-889, 2005.
13. Dobaczewski M, Bujak M, Li N, Gonzalez-Quesada C, Mendoza LH, Wang XF, Frangogiannis NG. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ Res 107: 418-428, 2010.
14. Dobaczewski M, Xia Y, Bujak M, Gonzalez-Quesada C, Frangogiannis NG. CCR5 signaling suppresses inflammation and reduces adverse remodeling of the infarcted heart, mediating recruitment of regulatory T cells. Am J Pathol 176: 2177-2187, 2010.
15. Fishbein MC, Maclean D, Maroko PR. The histopathologic evolution of myocardial infarction. Chest 73: 843-849, 1978.
16. Frangogiannis NG. The inflammatory response in myocardial injury, repair, and remodelling. Nat Rev Cardiol 11: 255-265, 2014.
17. Frangogiannis NG. Regulation of the inflammatory response in cardiac repair. Circ Res 110: 159-173, 2012.
18. 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 165: 2798-2808, 2000.
19. Fullerton JN, O'Brien AJ, Gilroy DW. Pathways mediating resolution of inflammation: when enough is too much. J Pathol 231: 8-20, 2013.
20. Hofmann U, Beyersdorf N, Weirather J, Podolskaya A, Bauersachs J, Ertl G, Kerkau T, Frantz S. Activation of CD4+ T lymphocytes improves wound healing and survival after experimental myocardial infarction in mice. Circulation 125: 1652-1663, 2012.
21. Houot R, Perrot I, Garcia E, Durand I, Lebecque S. Human CD4+CD25high regulatory T cells modulate myeloid but not plasmacytoid dendritic cells activation. J Immunol 176: 5293-5298, 2006.
22. Kong P, Christia P, Saxena A, Su Y, Frangogiannis NG. Lack of specificity of fibroblast-specific protein 1 in cardiac remodeling and fibrosis. Am J Physiol Heart Circ Physiol 305: H1363-H1372, 2013.
23. Lin J, Li M, Wang Z, He S, Ma X, Li D. The role of CD4+CD25+ regulatory T cells in macrophage-derived foam-cell formation. J Lipid Res 51: 1208-1217, 2010.
24. Ma Y, Halade GV, Zhang J, Ramirez TA, Levin D, Voorhees A, Jin YF, Han HC, Manicone AM, Lindsey ML. Matrix metalloproteinase-28 deletion exacerbates cardiac dysfunction and rupture after myocardial infarction in mice by inhibiting M2 macrophage activation. Circ Res 112: 675-688, 2013.
25. Matsumoto K, Ogawa M, Suzuki J, Hirata Y, Nagai R, Isobe M. Regulatory T lymphocytes attenuate myocardial infarction-induced ventricular remodeling in mice. Int Heart J 52: 382-387, 2011.
26. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo JL, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 204: 3037-3047, 2007.
27. O'Garra A, Vieira PL, Vieira P, Goldfeld AE. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 114: 1372-1378, 2004.
28. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 133: 775-787, 2008.
29. Saxena A, Chen W, Su Y, Rai V, Uche OU, Li N, Frangogiannis NG. IL-1 induces proinflammatory leukocyte infiltration and regulates fibroblast phenotype in the infarcted myocardium. J Immunol 191: 4838-4848, 2013.
30. Shinde AV, Frangogiannis NG. Fibroblasts in myocardial infarction: a role in inflammation and repair. J Mol Cell Cardiol 70C: 74-82, 2014.
31. Silvestre JS, Mallat Z, Tamarat R, Duriez M, Tedgui A, Levy BI. Regulation of matrix metalloproteinase activity in ischemic tissue by interleukin-10: role in ischemia-induced angiogenesis. Circ Res 89: 259-264, 2001.
32. Sobirin MA, Kinugawa S, Takahashi M, Fukushima A, Homma T, Ono T, Hirabayashi K, Suga T, Azalia P, Takada S, Taniguchi M, Nakayama T, Ishimori N, Iwabuchi K, Tsutsui H. Activation of natural killer T cells ameliorates postinfarct cardiac remodeling and failure in mice. Circ Res 111: 1037-1047, 2012.
33. Tang TT, Yuan J, Zhu ZF, Zhang WC, Xiao H, Xia N, Yan XX, Nie SF, Liu J, Zhou SF, Li JJ, Yao R, Liao MY, Tu X, Liao YH, Cheng X. Regulatory T cells ameliorate cardiac remodeling after myocardial infarction. Basic Res Cardiol 107: 232, 2012.
34. Varda-Bloom N, Leor J, Ohad DG, Hasin Y, Amar M, Fixler R, Battler A, Eldar M, Hasin D. Cytotoxic T lymphocytes are activated following myocardial infarction and can recognize and kill healthy myocytes in vitro. J Mol Cell Cardiol 32: 2141-2149, 2000.
35. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 8: 523-532, 2008.
36. Weirather J, Hofmann UD, Beyersdorf N, Ramos GC, Vogel B, Frey A, Ertl G, Kerkau T, Frantz S. Foxp3+ CD4+ T cells improve healing after myocardial infarction by modulating monocyte/macrophage differentiation. Circ Res 115: 55-67, 2014.
37. Yan X, Anzai A, Katsumata Y, Matsuhashi T, Ito K, Endo J, Yamamoto T, Takeshima A, Shinmura K, Shen W, Fukuda K, Sano M. Temporal dynamics of cardiac immune cell accumulation following acute myocardial infarction. J Mol Cell Cardiol 62: 24-35, 2013.
38. Zhang J, Herman EH, Ferrans VJ. Dendritic cells in the hearts of spontaneously hypertensive rats treated with doxorubicin with or without ICRF-187. Am J Pathol 142: 1916-1926, 1993.
39. Zouggari Y, Ait-Oufella H, Bonnin P, Simon T, Sage AP, Guerin C, Vilar J, Caligiuri G, Tsiantoulas D, Laurans L, Dumeau E, Kotti S, Bruneval P, Charo IF, Binder CJ, Danchin N, Tedgui A, Tedder TF, Silvestre JS, Mallat Z. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat Med 19: 1273-1280, 2013.