Foxp3+ CD4+ T cells improve healing after myocardial infarction by modulating monocyte/macrophage differentiation

Circulation Research

Volumn 115, Issue 1, 2014, Pages 55-67

  Weirather, Johannes ^a   Hofmann, Ulrich D W ^a   Beyersdorf, Niklas ^b   Ramos, Gustavo C ^a   Vogel, Benjamin ^a   Frey, Anna ^a   Ertl, Georg ^a   Kerkau, Thomas ^b   Frantz, Stefan ^a  

^a UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

myocardial infarction; wound healing

Indexed keywords

BASILIXIMAB; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; OSTEOPONTIN; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CARDITIS; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CELL POLARITY; CONTROLLED STUDY; CORONARY ARTERY LIGATION; CYTOKINE PRODUCTION; DETERIORATION; FLUORESCENCE ACTIVATED CELL SORTING; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE; HEART RUPTURE; IN VITRO STUDY; INNATE IMMUNITY; LEFT CORONARY ARTERY; LYMPH NODE; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MONOCYTE; MOUSE; MOUSE MODEL; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SCAR; SURVIVAL; T LYMPHOCYTE ACTIVATION; WOUND HEALING; ANIMAL; C57BL MOUSE; CYTOLOGY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

MYOCARDIAL INFARCTION; WOUND HEALING;

ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; FORKHEAD TRANSCRIPTION FACTORS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MONOCYTES; MYELOID CELLS; MYOCARDIAL INFARCTION; T-LYMPHOCYTES, REGULATORY; WOUND HEALING;

EID: 84903216099     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.303895     Document Type: Article

References (59)

1. Blankesteijn WM, Creemers E, Lutgens E, Cleutjens JP, Daemen MJ, Smits JF. Dynamics of cardiac wound healing following myocardial infarction: observations in genetically altered mice. Acta Physiol Scand. 2001;173:75-82.
2. Ertl G, Frantz S. Healing after myocardial infarction. Cardiovasc Res. 2005;66:22-32.
3. Ertl G, Frantz S. Wound model of myocardial infarction. Am J Physiol Heart Circ Physiol. 2005;288:H981-H983.
4. Nahrendorf M, Pittet MJ, Swirski FK. Monocytes: protagonists of infarct inflammation and repair after myocardial infarction. Circulation. 2010;121:2437-2445.
5. 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. 2012;125:1652-1663.
6. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell. 2008;133:775-787.
7. Curiel TJ. Tregs and rethinking cancer immunotherapy. J Clin Invest. 2007;117:1167-1174.
8. Joosten SA, Ottenhoff TH. Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination. Hum Immunol. 2008;69:760-770.
9. Walsh PT, Taylor DK, Turka LA. Tregs and transplantation tolerance. J Clin Invest. 2004;114:1398-1403.
10. Murphy TJ, Ni Choileain N, Zang Y, Mannick JA, Lederer JA. CD4+CD25+ regulatory T cells control innate immune reactivity after injury. J Immunol. 2005;174:2957-2963.
11. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol. 2007;8:191-197.
12. Felonato M, Pina A, de Araujo EF, Loures FV, Bazan SB, Feriotti C, Calich VL. Anti-CD25 treatment depletes Treg cells and decreases disease severity in susceptible and resistant mice infected with Paracoccidioides brasiliensis. PLoS One. 2012;7:e51071.
13. Setiady YY, Coccia JA, Park PU. In vivo depletion of CD4+FOXP3+ Treg cells by the PC61 anti-CD25 monoclonal antibody is mediated by FcgammaRIII+ phagocytes. Eur J Immunol. 2010;40:780-786.
14. Beyersdorf N, Hanke T, Kerkau T, Hunig T. Superagonistic anti-cd28 antibodies: potent activators of regulatory t cells for the therapy of autoimmune diseases. Ann Rheum Dis. 2005;64(suppl 4):iv91-iv95.
15. Lin CH, Hünig T. Efficient expansion of regulatory T cells in vitro and in vivo with a CD28 superagonist. Eur J Immunol. 2003;33:626-638.
16. Lahl K, Loddenkemper C, Drouin C, Freyer J, Arnason J, Eberl G, Hamann A, Wagner H, Huehn J, Sparwasser T. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J Exp Med. 2007;204:57-63.
17. Frantz S, Hu K, Widder J, Bayer B, Witzel CC, Schmidt I, Galuppo P, Strotmann J, Ertl G, Bauersachs J. Peroxisome proliferator activatedreceptor agonism and left ventricular remodeling in mice with chronic myocardial infarction. Br J Pharmacol. 2004;141:9-14.
18. Afanasyeva M, Georgakopoulos D, Belardi DF, Ramsundar AC, Barin JG, Kass DA, Rose NR. Quantitative analysis of myocardial inflammation by flow cytometry in murine autoimmune myocarditis: correlation with cardiac function. Am J Pathol. 2004;164:807-815.
19. Gao XM, Xu Q, Kiriazis H, Dart AM, Du XJ. Mouse model of post-infarct ventricular rupture: time course, strain- and gender-dependency, tensile strength, and histopathology. Cardiovasc Res. 2005;65:469-477.
20. 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. 2013;112:675-688.
21. Solinas G, Schiarea S, Liguori M, Fabbri M, Pesce S, Zammataro L, Pasqualini F, Nebuloni M, Chiabrando C, Mantovani A, Allavena P. Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J Immunol. 2010;185:642-652.
22. Töröcsik D, Bárdos H, Nagy L, Adány R. Identification of factor XIII-A as a marker of alternative macrophage activation. Cell Mol Life Sci. 2005;62:2132-2139.
23. 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. 2010;176:2177-2187.
24. van Blijswijk J, Schraml BU, Reis e Sousa C. Advantages and limitations of mouse models to deplete dendritic cells. Eur J Immunol. 2013;43:22-26.
25. Wiendl H, Gross CC. Modulation of il-2ralpha with daclizumab for treatment of multiple sclerosis. Nat Rev Neurol. 2013;9:394-404.
26. Lee DC, Harker JA, Tregoning JS, Atabani SF, Johansson C, Schwarze J, Openshaw PJ. CD25+ natural regulatory T cells are critical in limiting innate and adaptive immunity and resolving disease following respiratory syncytial virus infection. J Virol. 2010;84:8790-8798.
27. Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol. 2010;11:889-896.
28. Horton JW, Maass D, White J, Sanders B. Nitric oxide modulation of TNF-alpha-induced cardiac contractile dysfunction is concentration dependent. Am J Physiol Heart Circ Physiol. 2000;278:H1955-H1965.
29. Haudek SB, Taffet GE, Schneider MD, Mann DL. TNF provokes cardiomyocyte apoptosis and cardiac remodeling through activation of multiple cell death pathways. J Clin Invest. 2007;117:2692-2701.
30. Sato T, Suzuki H, Shibata M, Kusuyama T, Omori Y, Soda T, Shoji M, Iso Y, Koba S, Geshi E, Katagiri T, Shioda S, Sekikawa K. Tumor-necrosisfactor- alpha-gene-deficient mice have improved cardiac function through reduction of intercellular adhesion molecule-1 in myocardial infarction. Circ J. 2006;70:1635-1642.
31. Wang D, Yang XP, Liu YH, Carretero OA, LaPointe MC. Reduction of myocardial infarct size by inhibition of inducible nitric oxide synthase. Am J Hypertens. 1999;12:174-182.
32. Wildhirt SM, Weismueller S, Schulze C, Conrad N, Kornberg A, Reichart B. Inducible nitric oxide synthase activation after ischemia/reperfusion contributes to myocardial dysfunction and extent of infarct size in rabbits: evidence for a late phase of nitric oxide-mediated reperfusion injury. Cardiovasc Res. 1999;43:698-711.
33. Feng Q, Lu X, Jones DL, Shen J, Arnold JM. Increased inducible nitric oxide synthase expression contributes to myocardial dysfunction and higher mortality after myocardial infarction in mice. Circulation. 2001;104:700-704.
34. Gilson WD, Epstein FH, Yang Z, Xu Y, Prasad KM, Toufektsian MC, Laubach VE, French BA. Borderzone contractile dysfunction is transiently attenuated and left ventricular structural remodeling is markedly reduced following reperfused myocardial infarction in inducible nitric oxide synthase knockout mice. J Am Coll Cardiol. 2007;50:1799-1807.
35. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87:1620-1624.
36. Geng Y, Hansson GK, Holme E. Interferon-gamma and tumor necrosis factor synergize to induce nitric oxide production and inhibit mitochondrial respiration in vascular smooth muscle cells. Circ Res. 1992;71:1268-1276.
37. Arstall MA, Sawyer DB, Fukazawa R, Kelly RA. Cytokine-mediated apoptosis in cardiac myocytes: the role of inducible nitric oxide synthase induction and peroxynitrite generation. Circ Res. 1999;85:829-840.
38. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007;87:1285-1342.
39. Zamilpa R, Kanakia R, Cigarroa J IV, Dai Q, Escobar GP, Martinez H, Jimenez F, Ahuja SS, Lindsey ML. CC chemokine receptor 5 deletion impairs macrophage activation and induces adverse remodeling following myocardial infarction. Am J Physiol Heart Circ Physiol. 2011;300:H1418-H1426.
40. Frangogiannis NG. Matricellular proteins in cardiac adaptation and disease. Physiol Rev. 2012;92:635-688.
41. Nahrendorf M, Hu K, Frantz S, et al. Factor XIII deficiency causes cardiac rupture, impairs wound healing, and aggravates cardiac remodeling in mice with myocardial infarction. Circulation. 2006;113:1196-1202.
42. Ikeuchi M, Tsutsui H, Shiomi T, Matsusaka H, Matsushima S, Wen J, Kubota T, Takeshita A. Inhibition of TGF-beta signaling exacerbates early cardiac dysfunction but prevents late remodeling after infarction. Cardiovasc Res. 2004;64:526-535.
43. Tang TT, Yuan J, Zhu ZF, et al. Regulatory T cells ameliorate cardiac remodeling after myocardial infarction. Basic Res Cardiol. 2012;107:232.
44. Müller N, van den Brandt J, Odoardi F, Tischner D, Herath J, Flügel A, Reichardt HM. A CD28 superagonistic antibody elicits 2 functionally distinct waves of T cell activation in rats. J Clin Invest. 2008;118:1405-1416.
45. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11:723-737.
46. Harel-Adar T, Ben Mordechai T, Amsalem Y, Feinberg MS, Leor J, Cohen S. Modulation of cardiac macrophages by phosphatidylserinepresenting liposomes improves infarct repair. Proc Natl Acad Sci U S A. 2011;108:1827-1832.
47. Wynn TA. Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol. 2004;4:583-594.
48. Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest. 1999;104:777-785.
49. Oriente A, Fedarko NS, Pacocha SE, Huang SK, Lichtenstein LM, Essayan DM. Interleukin-13 modulates collagen homeostasis in human skin and keloid fibroblasts. J Pharmacol Exp Ther. 2000;292:988-994.
50. Singh M, Foster CR, Dalal S, Singh K. Osteopontin: role in extracellular matrix deposition and myocardial remodeling post-MI. J Mol Cell Cardiol. 2010;48:538-543.
51. Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y, Sefik E, Tan TG, Wagers AJ, Benoist C, Mathis D. A special population of regulatory T cells potentiates muscle repair. Cell. 2013;155:1282-1295.
52. Gong D, Shi W, Yi SJ, Chen H, Groffen J, Heisterkamp N. Tgfbeta signaling plays a critical role in promoting alternative macrophage activation. BMC Immunol. 2012;13:31
53. 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. 2007;204:3037-3047.
54. Ashizawa N, Graf K, Do YS, Nunohiro T, Giachelli CM, Meehan WP, Tuan TL, Hsueh WA. Osteopontin is produced by rat cardiac fibroblasts and mediates A(II)-induced DNA synthesis and collagen gel contraction. J Clin Invest. 1996;98:2218-2227.
55. Tsujimoto I, Moriya K, Sakai K, Dickneite G, Sakai T. Critical role of factor XIII in the initial stages of carbon tetrachloride-induced adult liver remodeling. Am J Pathol. 2011;179:3011-3019.
56. Nahrendorf M, Aikawa E, Figueiredo JL, Stangenberg L, van den Borne SW, Blankesteijn WM, Sosnovik DE, Jaffer FA, Tung CH, Weissleder R. Transglutaminase activity in acute infarcts predicts healing outcome and left ventricular remodelling: implications for FXIII therapy and antithrombin use in myocardial infarction. Eur Heart J. 2008;29:445-454.
57. Tabares P, Berr S, Romer PS, Chuvpilo S, Matskevich AA, Tyrsin D, Fedotov Y, Einsele H, Tony HP, Hunig T. Human regulatory t cells are selectively activated by low-dose application of the cd28 superagonist tgn1412/tab08. Eur J Immunol. 2014;44:1225-1236.
58. Koreth J, Matsuoka K, Kim HT, et al. Interleukin-2 and regulatory T cells in graft-versus-host disease. N Engl J Med. 2011;365:2055-2066.
59. Webster KE, Walters S, Kohler RE, Mrkvan T, Boyman O, Surh CD, Grey ST, Sprent J. In vivo expansion of T reg cells with IL-2-mAb complexes: induction of resistance to EAE and long-term acceptance of islet allografts without immunosuppression. J Exp Med. 2009;206:751-760.