Journal of Molecular and Cellular Cardiology
Volume 49, Issue 3 , Pages 469-481 , September 2010

Therapy with granulocyte colony-stimulating factor in the chronic stage, but not in the acute stage, improves experimental autoimmune myocarditis in rats via nitric oxide

  • Kana Shimada

      Affiliations

    • Department of Cardiovascular Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • ,
  • Taka-aki Okabe

      Affiliations

    • Department of Cardiovascular Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • ,
  • Yu Mikami

      Affiliations

    • Department of Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • ,
  • Miki Hattori

      Affiliations

    • Department of Cardiovascular Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • ,
  • Masatoshi Fujita

      Affiliations

    • Department of Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • ,
  • Chiharu Kishimoto

      Affiliations

    • Department of Cardiovascular Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    • Corresponding Author InformationCorresponding author. Department of Cardiovascular Medicine, Graduate School of Medicine, Kyoto University, 54 Kawaracho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Tel.: +81 075 751 3197; fax: +81 075 751 4281.

Received 30 January 2010 ,Accepted 4 February 2010.

References 

  1. Feldman AM, McNamara D. Myocarditis. N Engl J Med. 2000;343:1388–1398
  2. Levi D, Alejos J. Diagnosis and treatment of pediatric viral myocarditis. Curr Opin Cardiol. 2001;16:77–83
  3. Cohn JN. The management of chronic heart failure. N Engl J Med. 1996;335:490–498
  4. Dec GW, Fuster V. Idiopathic dilated cardiomyopathy. N Engl J Med. 1994;331:1564–1575
  5. Kodama M, Matsumoto Y, Fujiwara M, Masani F, Izumi T, Shibata A. A novel experimental model of giant cell myocarditis induced in rats by immunization with cardiac myosin fraction. Clin Immunol Immunopathol. 1990;57:250–262
  6. Shioji K, Kishimoto C, Nakamura H, Toyokuni S, Nakayama Y, Yodoi J, et al. Upregulation of thioredoxin (TRX) expression in giant cell myocarditis in rats. FEBS Lett. 2000;472:109–113
  7. Shioji K, Kishimoto C, Sasayama S. Fc receptor-mediated inhibitory effect of immunoglobulin therapy on autoimmune giant cell myocarditis: concomitant suppression of the expression of dendritic cells. Circ Res. 2001;89:540–546
  8. Kishimoto C, Kuribayashi K, Fukuma K, Masuda T, Tomioka N, Abelmann WH, et al. Immunologic identification of lymphocyte subsets in experimental murine myocarditis with encephalomyocarditis virus. Different kinetics of lymphocyte subsets between the heart and the peripheral blood, and significance of Thy 1.2+ (pan T) and Lyt 1+, 23+ (immature T) subsets in the development of myocarditis. Circ Res. 1987;61:715–725
  9. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410:701–705
  10. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999;85:221–228
  11. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43:109–142
  12. Moncada S. The l-arginine: nitric oxide pathway. Acad Physiol Scand. 1992;145:201–227
  13. Moncada S, Higgs A. The l-arginine–nitric oxide pathway. N Engl J Med. 1993;329:2002–2012
  14. Hiraoka Y, Kishimoto C, Takada H, Nakamura M, Kurokawa M, Ochiai H, et al. Nitric oxide and murine coxsackievirus B3 myocarditis: aggravation of myocarditis by inhibition of nitric oxide synthase. J Am Coll Cardiol. 1996;28:1610–1615
  15. Diet A, Abbas K, Bouton C, Guillon B, Tomasello F, Fourquet S, et al. Regulation of peroxiredoxins by nitric oxide in immunostimulated macrophages. J Biol Chem. 2007;282:36199–36205
  16. Ronco MT, Francés D, deLuján Alvarez M, Quiroga A, Monti J, Parody JP, et al. Vascular endothelial growth factor and nitric oxide in rat liver regeneration. Life Sci. 2007;81:750–755
  17. Betters JL, Long JH, Howe KS, Braith RW, Soltow QA, Lira VA, et al. Nitric oxide reverses prednisolone-induced inactivation of muscle satellite cells. Muscle Nerve. 2008;37:203–209
  18. Yuan Z, Kishimoto C, Shioji K, Nakamura H, Yodoi J, Sasayama S. Temocapril treatment ameliorates autoimmune myocarditis associated with enhanced cardiomyocyte thioredoxin expression. Cardiovasc Res. 2002;55:320–328
  19. Shioji K, Kishimoto C, Nakamura H, Masutani H, Yuan Z, Oka S, et al. Overexpression of thioredoxin-1 in transgenic mice attenuates adriamycin-induced cardiotoxicity. Circulation. 2002;106:1403–1409
  20. Miller FJ, Gutterman DD, Rios CD, Heistad DD, Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res. 1998;82:1298–1305
  21. Takaya T, Kawashima S, Shinohara M, Yamashita T, Toh R, Sasaki N, et al. Angiotensin II type 1 receptor blocker telmisartan suppresses superoxide production and reduces atherosclerotic lesion formation in apolipoprotein E-deficient mice. Atherosclerosis. 2006;186:402–410
  22. Neilan T, Blake SL, Ichinose F, Raher MJ, Buys ES, Jassal DS, et al. Disruption of nitric oxide synthase 3 protects against the cardiac injury, dysfunction, and mortality induced by doxorubicin. Circulation. 2007;116:506–514
  23. Werner N, Nickenig G. Clinical and therapeutical implications of EPC biology in atherosclerosis. J Cell Mol Med. 2006;10:318–332
  24. Sata M. Role of circulating vascular progenitors in angiogenesis, vascular healing, and pulmonary hypertension: lessons from animal models. Arterioscler Thromb Vasc Biol. 2006;26:1008–1014
  25. Roberts N, Jahangiri M, Xu Q. Progenitor cells in vascular disease. J Cell Mol Med. 2005;9:583–591
  26. Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG. Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension. 2005;46:7–18
  27. Khakoo AY, Finkel T. Endothelial progenitor cells. Annu Rev Med. 2005;56:79–101
  28. Rabelink TJ, de Boer HC, de Koning EJ, van Zonneveld AJ. Endothelial progenitor cells: more than an inflammatory response?. Arterioscler Thromb Vasc Biol. 2004;24:834–838
  29. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, et al. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999;5:434–438
  30. Orlic D, Kajstura J, Chimenti S, Bodine DM, Leri A, Anversa P. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci. 2001;938:221–229
  31. Hill JM, Syed MA, Arai AE, Powell TM, Paul JD, Zalos G, et al. Outcomes and risks of granulocyte colony-stimulating factor in patients with coronary artery disease. J Am Coll Cardiol. 2005;46:1643–1648
  32. Ohnishi S, Yanagawa B, Tanaka K, Miyahara Y, Obata H, Kataoka M, et al. Transplantation of mesenchymal stem cells attenuates myocardial injury and dysfunction in a rat model of acute myocarditis. J Moll Cell Cardiol. 2007;42:88–97
  33. Nagaya N, Kangawa K, Itoh T, Iwase T, Murakami S, Miyahara Y, et al. Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation. 2005;112:1128–1135
  34. Eriksson U, Kurrer MO, Bingisser R, Eugster HP, Saremaslani P, Follath F, et al. Lethal autoimmune myocarditis in interferon-γ receptor-deficient mice: enhanced disease severity by impaired inducible nitric oxide synthase induction. Circulation. 2001;103:18–21
  35. Valaperti A, Marty RR, Kania G, Germano D, Mauermann N, Dirnhofer S, et al. CD11b+ monocytes abrogate Th17 CD4+ T cell-mediated experimental autoimmune myocarditis. J Immunol. 2008;180:2686–2695
  36. Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M. GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J Exp Med. 2008;205:2281–2294
  37. Kodama M, Hanawa H, Saeki M, Hosono H, Inomata T, Suzuki K, et al. Rat dilated cardiomyopathy after autoimmune giant cell myocarditis. Circ Res. 1994;75:278–284
  38. Mathur AN, Chang HC, Zisoulis DG, Stritesky GL, Yu Q, O'Malley JT, et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol. 2007;178:4901–4907
  39. Fairweather D, Kaya Z, Shellam GR, Lawson CM, Rose NR. From infection to autoimmunity. J Autoimmun. 2001;16:175–186
  40. Cunningham MW. T cell mimicry in inflammatory heart disease. Mol Immunol. 2004;40:1121–1127
  41. Hiraoka Y, Kishimoto C, Takada H, Suzaki N, Shiraki K. Colony-stimulating factors and coxsackievirus B3 myocarditis in mice. Macrophage colony-stimulating factor suppresses acute myocarditis with increasing interferon α. Am Heart J. 1995;130:1259–1264
  42. Kishimoto C, Kuroki Y, Hiraoka Y, Ochiai H, Kurokawa M, Sasayama S. Cytokine and murine coxsackievirus B3 myocarditis. Interleukin-2 suppressed myocarditis in the acute stage but enhanced the condition in the subsequent stage. Circulation. 1994;89:2836–2842
  43. Haghighat A, Weiss D, Whalin MK, Cowan DP, Taylor WR. Granulocyte colony-stimulating factor and granulocyte macrophage colony-stimulating factor exacerbate atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2007;115:2049–2054
  44. Park KW, Kwon YW, Cho HJ, Shin JI, Kim YJ, Lee SE, et al. G-CSF exerts dual effects on endothelial cells. Opposing actions of direct eNOS induction versus indirect CRP elevation. J Moll Cell Cardiol. 2008;45:670–678
  45. Minatoguchi S, Takemura G, Chen XH, Wang N, Uno Y, Koda M, et al. Acceleration of the healing process and myocardial regeneration may be important as a mechanism of improvement of cardiac function and remodeling by postinfarction granulocyte colony-stimulating factor treatment. Circulation. 2004;109:2572–2580
  46. Dawn B, Guo Y, Rezazadeh A, Huang Y, Stein AB, Hunt G, et al. Postinfarct cytokine therapy regenerates cardiac tissue and improves left ventricular function. Circ Res. 2006;98:1098–1105
  47. Gulick T, Chung MK, Pieper SJ, Lange LG, Schreiner GF. Interleukin 1 and tumor necrosis factor inhibit cardiac myocyte beta-adrenergic responsiveness. Proc Natl Acad Sci USA. 1989;86:6753–6757
  48. Harada M, Qin Y, Takano H, Minamino T, Zou Y, Toko H, et al. G-CSF prevents cardiac remodeling after myocardial infarction by activating the Jak–Stat pathway in cardiomyocytes. Nat Med. 2005;11:305–311
  49. Hamamoto M, Tomita S, Nakatani T, Yutani C, Yamashiro S, Sueda T, et al. Granulocyte-colony stimulating factor directly enhances proliferation of human troponin I-positive cells derived from idiopathic dilated cardiomyopathy through specific receptors. J Heart Lung Transplant. 2004;23:1430–1437

PII: S0022-2828(10)00038-6

doi: 10.1016/j.yjmcc.2010.02.003

Journal of Molecular and Cellular Cardiology
Volume 49, Issue 3 , Pages 469-481 , September 2010

Article Tools

* Image Usage & Resolution