Diabetes-associated cardiac fibrosis: Cellular effectors, molecular mechanisms and therapeutic opportunities

Journal of Molecular and Cellular Cardiology

Volumn 90, Issue , 2016, Pages 84-93

  Russo, Ilaria ^a   Frangogiannis, Nikolaos G ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Diabetes; Fibroblast; Fibrosis; Heart failure; Obesity

Indexed keywords

ADIPONECTIN; ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; ENDOTHELIN 1; INTERLEUKIN 1BETA; LEPTIN; MICRORNA; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; SCLEROPROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; AGER PROTEIN, HUMAN; ANTIDIABETIC AGENT; SMAD PROTEIN;

ALLOXAN-INDUCED DIABETES MELLITUS; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIASTOLIC DYSFUNCTION; ENDOTHELIUM CELL; HEART ARRHYTHMIA; HEART FAILURE; HEART FIBROBLAST; HEART INFARCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MAST CELL; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PERICYTE; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; CARDIAC MUSCLE CELL; DIABETIC CARDIOMYOPATHIES; DRUG EFFECTS; ENDOMYOCARDIAL FIBROSIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANIMALS; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHIES; ENDOMYOCARDIAL FIBROSIS; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; HYPOGLYCEMIC AGENTS; MACROPHAGES; MYOCYTES, CARDIAC; RENIN-ANGIOTENSIN SYSTEM; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84949921072     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.12.011     Document Type: Review

References (156)

1. Gilbert R.E., Krum H. Heart failure in diabetes: effects of anti-hyperglycaemic drug therapy. Lancet 2015, 385:2107-2117.
2. Kannel W.B., Hjortland M., Castelli W.P. Role of diabetes in congestive heart failure: the Framingham study. Am. J. Cardiol. 1974, 34:29-34.
3. Cavender M.A., Steg P.G., Smith S.C., Eagle K., Ohman E.M., Goto S., et al. Impact of diabetes mellitus on hospitalization for heart failure, cardiovascular events, and death: outcomes at 4years from the reduction of atherothrombosis for continued health (REACH) registry. Circulation 2015, 132:923-931.
4. MacDonald M.R., Petrie M.C., Varyani F., Ostergren J., Michelson E.L., Young J.B., et al. Impact of diabetes on outcomes in patients with low and preserved ejection fraction heart failure: an analysis of the candesartan in heart failure: assessment of reduction in mortality and morbidity (CHARM) programme. Eur. Heart J. 2008, 29:1377-1385.
5. Bell D.S. Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 2003, 26:2433-2441.
6. Ferrannini E., Cushman W.C. Diabetes and hypertension: the bad companions. Lancet 2012, 380:601-610.
7. Rubler S., Dlugash J., Yuceoglu Y.Z., Kumral T., Branwood A.W., Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am. J. Cardiol. 1972, 30:595-602.
8. Kwong R.Y., Sattar H., Wu H., Vorobiof G., Gandla V., Steel K., et al. Incidence and prognostic implication of unrecognized myocardial scar characterized by cardiac magnetic resonance in diabetic patients without clinical evidence of myocardial infarction. Circulation 2008, 118:1011-1020.
9. Turkbey E.B., Backlund J.Y., Genuth S., Jain A., Miao C., Cleary P.A., et al. Myocardial structure, function, and scar in patients with type 1 diabetes mellitus. Circulation 2011, 124:1737-1746.
10. Regan T.J., Lyons M.M., Ahmed S.S., Levinson G.E., Oldewurtel H.A., Ahmad M.R., et al. Evidence for cardiomyopathy in familial diabetes mellitus. J. Clin. Invest. 1977, 60:884-899.
11. Kawaguchi M., Techigawara M., Ishihata T., Asakura T., Saito F., Maehara K., et al. A comparison of ultrastructural changes on endomyocardial biopsy specimens obtained from patients with diabetes mellitus with and without hypertension. Heart Vessel. 1997, 12:267-274.
12. Fischer V.W., Barner H.B., Larose L.S. Pathomorphologic aspects of muscular tissue in diabetes mellitus. Hum. Pathol. 1984, 15:1127-1136.
13. van Hoeven K.H., Factor S.M. A comparison of the pathological spectrum of hypertensive, diabetic, and hypertensive-diabetic heart disease. Circulation 1990, 82:848-855.
14. Nunoda S., Genda A., Sugihara N., Nakayama A., Mizuno S., Takeda R. Quantitative approach to the histopathology of the biopsied right ventricular myocardium in patients with diabetes mellitus. Heart Vessel. 1985, 1:43-47.
15. Sutherland C.G., Fisher B.M., Frier B.M., Dargie H.J., More I.A., Lindop G.B. Endomyocardial biopsy pathology in insulin-dependent diabetic patients with abnormal ventricular function. Histopathology 1989, 14:593-602.
16. Shimizu M., Umeda K., Sugihara N., Yoshio H., Ino H., Takeda R., et al. Collagen remodelling in myocardia of patients with diabetes. J. Clin. Pathol. 1993, 46:32-36.
17. van Heerebeek L., Hamdani N., Handoko M.L., Falcao-Pires I., Musters R.J., Kupreishvili K., et al. Diastolic stiffness of the failing diabetic heart: importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation 2008, 117:43-51.
18. Falcao-Pires I., Hamdani N., Borbely A., Gavina C., Schalkwijk C.G., van der Velden J., et al. Diabetes mellitus worsens diastolic left ventricular dysfunction in aortic stenosis through altered myocardial structure and cardiomyocyte stiffness. Circulation 2011, 124:1151-1159.
19. Cavalera M., Wang J., Frangogiannis N.G. Obesity, metabolic dysfunction, and cardiac fibrosis: pathophysiological pathways, molecular mechanisms, and therapeutic opportunities. Transl. Res. 2014, 164:323-335.
20. Shen X., Bornfeldt K.E. Mouse models for studies of cardiovascular complications of type 1 diabetes. Ann. N. Y. Acad. Sci. 2007, 1103:202-217.
21. Huynh K., McMullen J.R., Julius T.L., Tan J.W., Love J.E., Cemerlang N., et al. Cardiac-specific IGF-1 receptor transgenic expression protects against cardiac fibrosis and diastolic dysfunction in a mouse model of diabetic cardiomyopathy. Diabetes 2010, 59:1512-1520.
22. Ares-Carrasco S., Picatoste B., Benito-Martin A., Zubiri I., Sanz A.B., Sanchez-Nino M.D., et al. Myocardial fibrosis and apoptosis, but not inflammation, are present in long-term experimental diabetes. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H2109-H2119.
23. Hao P.P., Yang J.M., Zhang M.X., Zhang K., Chen Y.G., Zhang C., et al. Angiotensin-(1-7) treatment mitigates right ventricular fibrosis as a distinctive feature of diabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 2015, 308:H1007-H1019.
24. Meloni M., Descamps B., Caporali A., Zentilin L., Floris I., Giacca M., et al. Nerve growth factor gene therapy using adeno-associated viral vectors prevents cardiomyopathy in type 1 diabetic mice. Diabetes 2012, 61:229-240.
25. Li J., Zhu H., Shen E., Wan L., Arnold J.M., Peng T. Deficiency of rac1 blocks NADPH oxidase activation, inhibits endoplasmic reticulum stress, and reduces myocardial remodeling in a mouse model of type 1 diabetes. Diabetes 2010, 59:2033-2042.
26. Basu R., Oudit G.Y., Wang X., Zhang L., Ussher J.R., Lopaschuk G.D., et al. Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H2096-H2108.
27. Regan T.J., Wu C.F., Yeh C.K., Oldewurtel H.A., Haider B. Myocardial composition and function in diabetes. The effects of chronic insulin use. Circ. Res. 1981, 49:1268-1277.
28. Haider B., Yeh C.K., Thomas G., Oldewurtel H.A., Lyons M.M., Regan T.J. Influence of diabetes on the myocardium and coronary arteries of rhesus monkey fed an atherogenic diet. Circ. Res. 1981, 49:1278-1288.
29. Khaidar A., Marx M., Lubec B., Lubec G. l-arginine reduces heart collagen accumulation in the diabetic db/db mouse. Circulation 1994, 90:479-483.
30. Gonzalez-Quesada C., Cavalera M., Biernacka A., Kong P., Lee D.W., Saxena A., et al. Thrombospondin-1 induction in the diabetic myocardium stabilizes the cardiac matrix in addition to promoting vascular rarefaction through angiopoietin-2 upregulation. Circ. Res. 2013, 113:1331-1344.
31. Biernacka A., Cavalera M., Wang J., Russo I., Shinde A., Kong P., et al. Smad3 signaling promotes fibrosis while preserving cardiac and aortic geometry in obese diabetic mice. Circ. Heart Fail. 2015, 8:788-798.
32. Huynh K., Kiriazis H., Du X.J., Love J.E., Jandeleit-Dahm K.A., Forbes J.M., et al. Coenzyme Q10 attenuates diastolic dysfunction, cardiomyocyte hypertrophy and cardiac fibrosis in the db/db mouse model of type 2 diabetes. Diabetologia 2012, 55:1544-1553.
33. Sloan C., Tuinei J., Nemetz K., Frandsen J., Soto J., Wride N., et al. Central leptin signaling is required to normalize myocardial fatty acid oxidation rates in caloric-restricted ob/ob mice. Diabetes 2011, 60:1424-1434.
34. Zaman A.K., Fujii S., Goto D., Furumoto T., Mishima T., Nakai Y., et al. Salutary effects of attenuation of angiotensin II on coronary perivascular fibrosis associated with insulin resistance and obesity. J. Mol. Cell. Cardiol. 2004, 37:525-535.
35. Van den Bergh A., Vanderper A., Vangheluwe P., Desjardins F., Nevelsteen I., Verreth W., et al. Dyslipidaemia in type II diabetic mice does not aggravate contractile impairment but increases ventricular stiffness. Cardiovasc. Res. 2008, 77:371-379.
36. Fredersdorf S., Thumann C., Ulucan C., Griese D.P., Luchner A., Riegger G.A., et al. Myocardial hypertrophy and enhanced left ventricular contractility in Zucker diabetic fatty rats. Cardiovasc. Pathol. 2004, 13:11-19.
37. Aroor A.R., Sowers J.R., Bender S.B., Nistala R., Garro M., Mugerfeld I., et al. Dipeptidylpeptidase inhibition is associated with improvement in blood pressure and diastolic function in insulin-resistant male zucker obese rats. Endocrinology 2013, 154:2501-2513.
38. Zibadi S., Vazquez R., Moore D., Larson D.F., Watson R.R. Myocardial lysyl oxidase regulation of cardiac remodeling in a murine model of diet-induced metabolic syndrome. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H976-H982.
39. Qin F., Siwik D.A., Luptak I., Hou X., Wang L., Higuchi A., et al. The polyphenols resveratrol and S17834 prevent the structural and functional sequelae of diet-induced metabolic heart disease in mice. Circulation 2012, 125:1757-1764. S1-6.
40. Calligaris S.D., Lecanda M., Solis F., Ezquer M., Gutierrez J., Brandan E., et al. Mice long-term high-fat diet feeding recapitulates human cardiovascular alterations: an animal model to study the early phases of diabetic cardiomyopathy. PLoS One 2013, 8:e60931.
41. Factor S.M., Bhan R., Minase T., Wolinsky H., Sonnenblick E.H. Hypertensive-diabetic cardiomyopathy in the rat: an experimental model of human disease. Am. J. Pathol. 1981, 102:219-228.
42. van Bilsen M., Daniels A., Brouwers O., Janssen B.J., Derks W.J., Brouns A.E., et al. Hypertension is a conditional factor for the development of cardiac hypertrophy in type 2 diabetic mice. PLoS One 2014, 9:e85078.
43. Kong P., Christia P., Frangogiannis N.G. The pathogenesis of cardiac fibrosis. Cell. Mol. Life Sci. 2014, 71:549-574.
44. Souders C.A., Bowers S.L., Baudino T.A. Cardiac fibroblast: the renaissance cell. Circ. Res. 2009, 105:1164-1176.
45. Shinde A.V., Frangogiannis N.G. Fibroblasts in myocardial infarction: a role in inflammation and repair. J. Mol. Cell. Cardiol. 2014, 70C:74-82.
46. Willems I.E., Havenith M.G., De Mey J.G., Daemen M.J. The alpha-smooth muscle actin-positive cells in healing human myocardial scars. Am. J. Pathol. 1994, 145:868-875.
47. Cleutjens J.P., Verluyten M.J., Smiths J.F., Daemen M.J. Collagen remodeling after myocardial infarction in the rat heart. Am. J. Pathol. 1995, 147:325-338.
48. Frangogiannis N.G., Michael L.H., Entman M.L. Myofibroblasts in reperfused myocardial infarcts express the embryonic form of smooth muscle myosin heavy chain (SMemb). Cardiovasc. Res. 2000, 48:89-100.
49. van Putten S., Shafieyan Y., Hinz B. Mechanical control of cardiac myofibroblasts. J. Mol. Cell. Cardiol. 2015.
50. Fowlkes V., Clark J., Fix C., Law B.A., Morales M.O., Qiao X., et al. Type II diabetes promotes a myofibroblast phenotype in cardiac fibroblasts. Life Sci. 2013, 92:669-676.
51. Hutchinson K.R., Lord C.K., West T.A., Stewart J.A. Cardiac fibroblast-dependent extracellular matrix accumulation is associated with diastolic stiffness in type 2 diabetes. PLoS One 2013, 8:e72080.
52. Sedgwick B., Riches K., Bageghni S.A., O'Regan D.J., Porter K.E., Turner N.A. Investigating inherent functional differences between human cardiac fibroblasts cultured from nondiabetic and type 2 diabetic donors. Cardiovasc. Pathol. 2014, 23:204-210.
53. Pinto A.R., Paolicelli R., Salimova E., Gospocic J., Slonimsky E., Bilbao-Cortes D., et al. An abundant tissue macrophage population in the adult murine heart with a distinct alternatively-activated macrophage profile. PLoS One 2012, 7:e36814.
54. Epelman S., Lavine K.J., Beaudin A.E., Sojka D.K., Carrero J.A., Calderon B., et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014, 40:91-104.
55. Dewald O., Zymek P., Winkelmann K., Koerting A., Ren G., Abou-Khamis T., et al. CCL2/monocyte chemoattractant protein-1 regulates inflammatory responses critical to healing myocardial infarcts. Circ. Res. 2005, 96:881-889.
56. Nahrendorf M., Swirski F.K., Aikawa E., Stangenberg L., Wurdinger T., Figueiredo J.L., et al. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J. Exp. Med. 2007, 204:3037-3047.
57. Usher M.G., Duan S.Z., Ivaschenko C.Y., Frieler R.A., Berger S., Schutz G., et al. Myeloid mineralocorticoid receptor controls macrophage polarization and cardiovascular hypertrophy and remodeling in mice. J. Clin. Invest. 2010, 120:3350-3364.
58. Hartupee J., Mann D.L. Role of inflammatory cells in fibroblast activation. J. Mol. Cell. Cardiol. 2015, (epub ahead of print).
59. Hulsmans M., Sam F., Nahrendorf M. Monocyte and macrophage contributions to cardiac remodeling. J. Mol. Cell. Cardiol. 2015, (epub ahead of print).
60. Urbina P., Singla D.K. BMP-7 attenuates adverse cardiac remodeling mediated through M2 macrophages in prediabetic cardiomyopathy. Am. J. Physiol. Heart Circ. Physiol. 2014, 307:H762-H772.
61. Fukuda M., Nakamura T., Kataoka K., Nako H., Tokutomi Y., Dong Y.F., et al. Potentiation by candesartan of protective effects of pioglitazone against type 2 diabetic cardiovascular and renal complications in obese mice. J. Hypertens. 2010, 28:340-352.
62. Fukuda M., Nakamura T., Kataoka K., Nako H., Tokutomi Y., Dong Y.F., et al. Ezetimibe ameliorates cardiovascular complications and hepatic steatosis in obese and type 2 diabetic db/db mice. J. Pharmacol. Exp. Ther. 2010, 335:70-75.
63. Saxena A., Dobaczewski M., Rai V., Haque Z., Chen W., Li N., et al. Regulatory T cells are recruited in the infarcted mouse myocardium and may modulate fibroblast phenotype and function. Am. J. Physiol. Heart Circ. Physiol. 2014, 307:H1233-H1242.
64. Nevers T., Salvador A.M., Grodecki-Pena A., Knapp A., Velazquez F., Aronovitz M., et al. Left ventricular T-cell recruitment contributes to the pathogenesis of heart failure. Circ. Heart Fail. 2015, 8:776-787.
65. Frieler R.A., Mortensen R.M. Immune cell and other noncardiomyocyte regulation of cardiac hypertrophy and remodeling. Circulation 2015, 131:1019-1030.
66. Zeisberg E.M., Tarnavski O., Zeisberg M., Dorfman A.L., McMullen J.R., Gustafsson E., et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 2007, 13:952-961.
67. Aisagbonhi O., Rai M., Ryzhov S., Atria N., Feoktistov I., Hatzopoulos A.K. Experimental myocardial infarction triggers canonical Wnt signaling and endothelial-to-mesenchymal transition. Dis. Model. Mech. 2011, 4:469-483.
68. Widyantoro B., Emoto N., Nakayama K., Anggrahini D.W., Adiarto S., Iwasa N., et al. Endothelial cell-derived endothelin-1 promotes cardiac fibrosis in diabetic hearts through stimulation of endothelial-to-mesenchymal transition. Circulation 2010, 121:2407-2418.
69. Humphreys B.D. Targeting pericyte differentiation as a strategy to modulate kidney fibrosis in diabetic nephropathy. Semin. Nephrol. 2012, 32:463-470.
70. Frangogiannis N.G., Perrard J.L., Mendoza L.H., Burns A.R., Lindsey M.L., Ballantyne C.M., et al. Stem cell factor induction is associated with mast cell accumulation after canine myocardial ischemia and reperfusion. Circulation 1998, 98:687-698.
71. Levick S.P., McLarty J.L., Murray D.B., Freeman R.M., Carver W.E., Brower G.L. Cardiac mast cells mediate left ventricular fibrosis in the hypertensive rat heart. Hypertension 2009, 53:1041-1047.
72. Zhang W., Chancey A.L., Tzeng H.P., Zhou Z., Lavine K.J., Gao F., et al. The development of myocardial fibrosis in transgenic mice with targeted overexpression of tumor necrosis factor requires mast cell-fibroblast interactions. Circulation 2012, 124:2106-2116.
73. Nishikori Y., Shiota N., Okunishi H. The role of mast cells in cutaneous wound healing in streptozotocin-induced diabetic mice. Arch. Dermatol. Res. 2014, 306:823-835.
74. Alpert M.A., Omran J., Mehra A., Ardhanari S. Impact of obesity and weight loss on cardiac performance and morphology in adults. Prog. Cardiovasc. Dis. 2014, 56:391-400.
75. Barouch L.A., Gao D., Chen L., Miller K.L., Xu W., Phan A.C., et al. Cardiac myocyte apoptosis is associated with increased DNA damage and decreased survival in murine models of obesity. Circ. Res. 2006, 98:119-124.
76. Han D.C., Isono M., Hoffman B.B., Ziyadeh F.N. High glucose stimulates proliferation and collagen type I synthesis in renal cortical fibroblasts: mediation by autocrine activation of TGF-beta. J. Am. Soc. Nephrol. 1999, 10:1891-1899.
77. Shamhart P.E., Luther D.J., Adapala R.K., Bryant J.E., Petersen K.A., Meszaros J.G., et al. Hyperglycemia enhances function and differentiation of adult rat cardiac fibroblasts. Can. J. Physiol. Pharmacol. 2014, 92:598-604.
78. Aguilar H., Fricovsky E., Ihm S., Schimke M., Maya-Ramos L., Aroonsakool N., et al. Role for high-glucose-induced protein O-GlcNAcylation in stimulating cardiac fibroblast collagen synthesis. Am. J. Physiol. Cell. Physiol. 2014, 306:C794-C804.
79. Singh V.P., Baker K.M., Kumar R. Activation of the intracellular renin-angiotensin system in cardiac fibroblasts by high glucose: role in extracellular matrix production. Am. J. Physiol. Heart Circ. Physiol. 2008, 294:H1675-H1684.
80. Fiaschi T., Magherini F., Gamberi T., Lucchese G., Faggian G., Modesti A., et al. Hyperglycemia and angiotensin II cooperate to enhance collagen I deposition by cardiac fibroblasts through a ROS-STAT3-dependent mechanism. Biochim. Biophys. Acta 1843, 2014:2603-2610.
81. Tang M., Zhang W., Lin H., Jiang H., Dai H., Zhang Y. High glucose promotes the production of collagen types I and III by cardiac fibroblasts through a pathway dependent on extracellular-signal-regulated kinase 1/2. Mol. Cell. Biochem. 2007, 301:109-114.
82. Conway B.R., Betz B., Sheldrake T.A., Manning J.R., Dunbar D.R., Dobyns A., et al. Tight blood glycaemic and blood pressure control in experimental diabetic nephropathy reduces extracellular matrix production without regression of fibrosis. Nephrology (Carlton) 2014, 19:802-813.
83. Privratsky J.R., Wold L.E., Sowers J.R., Quinn M.T., Ren J. AT1 blockade prevents glucose-induced cardiac dysfunction in ventricular myocytes: role of the AT1 receptor and NADPH oxidase. Hypertension 2003, 42:206-212.
84. Brown L., Wall D., Marchant C., Sernia C. Tissue-specific changes in angiotensin II receptors in streptozotocin-diabetic rats. J. Endocrinol. 1997, 154:355-362.
85. Senador D., Kanakamedala K., Irigoyen M.C., Morris M., Elased K.M. Cardiovascular and autonomic phenotype of db/db diabetic mice. Exp. Physiol. 2009, 94:648-658.
86. Toblli J.E., Cao G., DeRosa G., Forcada P. Reduced cardiac expression of plasminogen activator inhibitor 1 and transforming growth factor beta1 in obese Zucker rats by perindopril. Heart 2005, 91:80-86.
87. Zaman A.K., Fujii S., Sawa H., Goto D., Ishimori N., Watano K., et al. Angiotensin-converting enzyme inhibition attenuates hypofibrinolysis and reduces cardiac perivascular fibrosis in genetically obese diabetic mice. Circulation 2001, 103:3123-3128.
88. Singh V.P., Le B., Khode R., Baker K.M., Kumar R. Intracellular angiotensin II production in diabetic rats is correlated with cardiomyocyte apoptosis, oxidative stress, and cardiac fibrosis. Diabetes 2008, 57:3297-3306.
89. Zhou Y., Poczatek M.H., Berecek K.H., Murphy-Ullrich J.E. Thrombospondin 1 mediates angiotensin II induction of TGF-beta activation by cardiac and renal cells under both high and low glucose conditions. Biochem. Biophys. Res. Commun. 2006, 339:633-641.
90. Chen K., Mehta J.L., Li D., Joseph L., Joseph J. Transforming growth factor beta receptor endoglin is expressed in cardiac fibroblasts and modulates profibrogenic actions of angiotensin II. Circ. Res. 2004, 95:1167-1173.
91. Vazquez-Medina J.P., Popovich I., Thorwald M.A., Viscarra J.A., Rodriguez R., Sonanez-Organis J.G., et al. Angiotensin receptor-mediated oxidative stress is associated with impaired cardiac redox signaling and mitochondrial function in insulin-resistant rats. Am. J. Physiol. Heart Circ. Physiol. 2013, 305:H599-H607.
92. Essick E.E., Sam F. Cardiac hypertrophy and fibrosis in the metabolic syndrome: a role for aldosterone and the mineralocorticoid receptor. Int. J. Hypertens. 2011, 2011:346985.
93. Miric G., Dallemagne C., Endre Z., Margolin S., Taylor S.M., Brown L. Reversal of cardiac and renal fibrosis by pirfenidone and spironolactone in streptozotocin-diabetic rats. Br. J. Pharmacol. 2001, 133:687-694.
94. Bostick B., Habibi J., DeMarco V.G., Jia G., Domeier T.L., Lambert M.D., et al. Mineralocorticoid receptor blockade prevents Western diet-induced diastolic dysfunction in female mice. Am. J. Physiol. Heart Circ. Physiol. 2015, 308:H1126-H1135.
95. Kosmala W., Przewlocka-Kosmala M., Szczepanik-Osadnik H., Mysiak A., Marwick T.H. Fibrosis and cardiac function in obesity: a randomised controlled trial of aldosterone blockade. Heart 2013, 99:320-326.
96. Saxena A., Shinde A.V., Haque Z., Wu Y.J., Chen W., Su Y., et al. The role of interleukin receptor associated kinase (IRAK)-M in regulation of myofibroblast phenotype in vitro, and in an experimental model of non-reperfused myocardial infarction. J. Mol. Cell. Cardiol. 2015, (epub ahead of print).
97. Venkatachalam K., Venkatesan B., Valente A.J., Melby P.C., Nandish S., Reusch J.E., et al. WISP1, a pro-mitogenic, pro-survival factor, mediates tumor necrosis factor-alpha (TNF-alpha)-stimulated cardiac fibroblast proliferation but inhibits TNF-alpha-induced cardiomyocyte death. J. Biol. Chem. 2009, 284:14414-14427.
98. Saxena A., Chen W., Su Y., Rai V., Uche O.U., Li N., et al. IL-1 induces proinflammatory leukocyte infiltration and regulates fibroblast phenotype in the infarcted myocardium. J. Immunol. 2013, 191:4838-4848.
99. Suzuki H., Kayama Y., Sakamoto M., Iuchi H., Shimizu I., Yoshino T., et al. Arachidonate 12/15-lipoxygenase-induced inflammation and oxidative stress are involved in the development of diabetic cardiomyopathy. Diabetes 2015, 64:618-630.
100. Westermann D., Rutschow S., Jager S., Linderer A., Anker S., Riad A., et al. Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy: the role of angiotensin type 1 receptor antagonism. Diabetes 2007, 56:641-646.
101. Isic A., Scharin Tang M., Haugen E., Fu M. TNFalpha-antagonist neither improve cardiac remodelling or cardiac function at early stage of heart failure in diabetic rats. Autoimmunity 2008, 41:473-477.
102. Westermann D., Van Linthout S., Dhayat S., Dhayat N., Schmidt A., Noutsias M., et al. Tumor necrosis factor-alpha antagonism protects from myocardial inflammation and fibrosis in experimental diabetic cardiomyopathy. Basic Res. Cardiol. 2007, 102:500-507.
103. Dobaczewski M., Frangogiannis N.G. Chemokines and cardiac fibrosis. Front. Biosci. (Schol. Ed.) 2009, 1:391-405.
104. Frangogiannis N.G., Dewald O., Xia Y., Ren G., Haudek S., Leucker T., et al. Critical role of monocyte chemoattractant protein-1/CC chemokine ligand 2 in the pathogenesis of ischemic cardiomyopathy. Circulation 2007, 115:584-592.
105. Chu P.Y., Mariani J., Finch S., McMullen J.R., Sadoshima J., Marshall T., et al. Bone marrow-derived cells contribute to fibrosis in the chronically failing heart. Am. J. Pathol. 2010, 176:1735-1742.
106. Yu Y., Ohmori K., Chen Y., Sato C., Kiyomoto H., Shinomiya K., et al. Effects of pravastatin on progression of glucose intolerance and cardiovascular remodeling in a type II diabetes model. J. Am. Coll. Cardiol. 2004, 44:904-913.
107. Chu P.Y., Walder K., Horlock D., Williams D., Nelson E., Byrne M., et al. CXCR4 antagonism attenuates the development of diabetic cardiac fibrosis. PLoS One 2015, 10:e0133616.
108. Biernacka A., Dobaczewski M., Frangogiannis N.G. TGF-beta signaling in fibrosis. Growth Factors 2011, 29:196-202.
109. Dobaczewski M., Chen W., Frangogiannis N.G. Transforming growth factor (TGF)-beta signaling in cardiac remodeling. J. Mol. Cell. Cardiol. 2011, 51:600-606.
110. Carroll J.F., Tyagi S.C. Extracellular matrix remodeling in the heart of the homocysteinemic obese rabbit. Am. J. Hypertens. 2005, 18:692-698.
111. Abed H.S., Samuel C.S., Lau D.H., Kelly D.J., Royce S.G., Alasady M., et al. Obesity results in progressive atrial structural and electrical remodeling: implications for atrial fibrillation. Heart Rhythm. 2013, 10:90-100.
112. Ziyadeh F.N., Sharma K., Ericksen M., Wolf G. Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-beta. J. Clin. Invest. 1994, 93:536-542.
113. Kumpers P., Gueler F., Rong S., Mengel M., Tossidou I., Peters I., et al. Leptin is a coactivator of TGF-beta in unilateral ureteral obstructive kidney disease. Am. J. Physiol. Ren. Physiol. 2007, 293:F1355-F1362.
114. Dobaczewski M., Bujak M., Li N., Gonzalez-Quesada C., Mendoza L.H., Wang X.F., et al. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ. Res. 2010, 107:418-428.
115. Rahaman S.O., Grove L.M., Paruchuri S., Southern B.D., Abraham S., Niese K.A., et al. TRPV4 mediates myofibroblast differentiation and pulmonary fibrosis in mice. J. Clin. Invest. 2014, 124:5225-5238.
116. Sen S., Chen S., Feng B., Iglarz M., Chakrabarti S. Renal, retinal and cardiac changes in type 2 diabetes are attenuated by macitentan, a dual endothelin receptor antagonist. Life Sci. 2012, 91:658-668.
117. Abel E.D., Litwin S.E., Sweeney G. Cardiac remodeling in obesity. Physiol. Rev. 2008, 88:389-419.
118. Desco M.C., Asensi M., Marquez R., Martinez-Valls J., Vento M., Pallardo F.V., et al. Xanthine oxidase is involved in free radical production in type 1 diabetes: protection by allopurinol. Diabetes 2002, 51:1118-1124.
119. Boudina S., Sena S., Theobald H., Sheng X., Wright J.J., Hu X.X., et al. Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 2007, 56:2457-2466.
120. Ballal K., Wilson C.R., Harmancey R., Taegtmeyer H. Obesogenic high fat western diet induces oxidative stress and apoptosis in rat heart. Mol. Cell. Biochem. 2010, 344:221-230.
121. Serpillon S., Floyd B.C., Gupte R.S., George S., Kozicky M., Neito V., et al. Superoxide production by NAD(P)H oxidase and mitochondria is increased in genetically obese and hyperglycemic rat heart and aorta before the development of cardiac dysfunction. The role of glucose-6-phosphate dehydrogenase-derived NADPH. Am. J. Physiol. Heart Circ. Physiol. 2009, 297:H153-H162.
122. Aragno M., Mastrocola R., Alloatti G., Vercellinatto I., Bardini P., Geuna S., et al. Oxidative stress triggers cardiac fibrosis in the heart of diabetic rats. Endocrinology 2008, 149:380-388.
123. Goldin A., Beckman J.A., Schmidt A.M., Creager M.A. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 2006, 114:597-605.
124. Zhao L.M., Zhang W., Wang L.P., Li G.R., Deng X.L. Advanced glycation end products promote proliferation of cardiac fibroblasts by upregulation of KCa3.1 channels. Pflugers Arch. 2012, 464:613-621.
125. Oldfield M.D., Bach L.A., Forbes J.M., Nikolic-Paterson D., McRobert A., Thallas V., et al. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J. Clin. Invest. 2001, 108:1853-1863.
126. Yamazaki K.G., Gonzalez E., Zambon A.C. Crosstalk between the renin-angiotensin system and the advance glycation end product axis in the heart: role of the cardiac fibroblast. J. Cardiovasc. Transl. Res. 2012, 5:805-813.
127. Nielsen J.M., Kristiansen S.B., Norregaard R., Andersen C.L., Denner L., Nielsen T.T., et al. Blockage of receptor for advanced glycation end products prevents development of cardiac dysfunction in db/db type 2 diabetic mice. Eur. J. Heart Fail. 2009, 11:638-647.
128. Perego L., Pizzocri P., Corradi D., Maisano F., Paganelli M., Fiorina P., et al. Circulating leptin correlates with left ventricular mass in morbid (grade III) obesity before and after weight loss induced by bariatric surgery: a potential role for leptin in mediating human left ventricular hypertrophy. J. Clin. Endocrinol. Metab. 2005, 90:4087-4093.
129. Barouch L.A., Berkowitz D.E., Harrison R.W., O'Donnell C.P., Hare J.M. Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation 2003, 108:754-759.
130. Rajapurohitam V., Gan X.T., Kirshenbaum L.A., Karmazyn M. The obesity-associated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ. Res. 2003, 93:277-279.
131. Schram K., Ganguly R., No E.K., Fang X.P., Thong F.S.L., Sweeney G. Regulation of MT1-MMP and MMP-2 by leptin in cardiac fibroblasts involves rho/ROCK-dependent actin cytoskeletal reorganization and leads to enhanced cell migration. Endocrinology 2011, 152:2037-2047.
132. Fukui A., Takahashi N., Nakada C., Masaki T., Kume O., Shinohara T., et al. Role of leptin signaling in the pathogenesis of angiotensin II-mediated atrial fibrosis and fibrillation. Circ. Arrhythm. Electrophysiol. 2013, 6:402-409.
133. Zibadi S., Cordova F., Slack E.H., Watson R.R., Larson D.F. Leptin's regulation of obesity-induced cardiac extracellular matrix remodeling. Cardiovasc. Toxicol. 2011, 11:325-333.
134. Matsuzawa Y., Funahashi T., Kihara S., Shimomura I. Adiponectin and metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 2004, 24:29-33.
135. Hopkins T.A., Ouchi N., Shibata R., Walsh K. Adiponectin actions in the cardiovascular system. Cardiovasc. Res. 2007, 74:11-18.
136. Dadson K., Chasiotis H., Wannaiampikul S., Tungtrongchitr R., Xu A., Sweeney G. Adiponectin mediated APPL1-AMPK signaling induces cell migration, MMP activation, and collagen remodeling in cardiac fibroblasts. J. Cell. Biochem. 2014, 115:785-793.
137. Cai X.J., Chen L., Li L., Feng M., Li X., Zhang K., et al. Adiponectin inhibits lipopolysaccharide-induced adventitial fibroblast migration and transition to myofibroblasts via AdipoR1-AMPK-iNOS pathway. Mol. Endocrinol. 2010, 24:218-228.
138. Fujita K., Maeda N., Sonoda M., Ohashi K., Hibuse T., Nishizawa H., et al. Adiponectin protects against angiotensin II-induced cardiac fibrosis through activation of PPAR-alpha. Arterioscler. Thromb. Vasc. Biol. 2008, 28:863-870.
139. Shibata R., Ouchi N., Ito M., Kihara S., Shiojima I., Pimentel D.R., et al. Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 2004, 10:1384-1389.
140. Frangogiannis N.G. Matricellular proteins in cardiac adaptation and disease. Physiol. Rev. 2012, 92:635-688.
141. Raman P., Krukovets I., Marinic T.E., Bornstein P., Stenina O.I. Glycosylation mediates up-regulation of a potent antiangiogenic and proatherogenic protein, thrombospondin-1, by glucose in vascular smooth muscle cells. J. Biol. Chem. 2007, 282:5704-5714.
142. Varma V., Yao-Borengasser A., Bodles A.M., Rasouli N., Phanavanh B., Nolen G.T., et al. Thrombospondin-1 is an adipokine associated with obesity, adipose inflammation, and insulin resistance. Diabetes 2008, 57:432-439.
143. Kong P., Gonzalez-Quesada C., Li N., Cavalera M., Lee D.W., Frangogiannis N.G. Thrombospondin-1 regulates adiposity and metabolic dysfunction in diet-induced obesity enhancing adipose inflammation and stimulating adipocyte proliferation. Am. J. Physiol. Endocrinol. Metab. 2013, 305:E439-E450.
144. Thum T. Noncoding RNAs and myocardial fibrosis. Nat. Rev. Cardiol. 2014, 11:655-663.
145. Diao X., Shen E., Wang X., Hu B. Differentially expressed microRNAs and their target genes in the hearts of streptozotocin-induced diabetic mice. Mol. Med. Rep. 2011, 4:633-640.
146. Costantino S., Paneni F., Luscher T.F., Cosentino F. MicroRNA profiling unveils hyperglycaemic memory in the diabetic heart. Eur. Heart J. 2015, (epub ahead of print).
147. Chen S., Puthanveetil P., Feng B., Matkovich S.J., Dorn G.W., Chakrabarti S. Cardiac miR-133a overexpression prevents early cardiac fibrosis in diabetes. J. Cell. Mol. Med. 2014, 18:415-421.
148. Wong T.C., Piehler K.M., Kang I.A., Kadakkal A., Kellman P., Schwartzman D.S., et al. Myocardial extracellular volume fraction quantified by cardiovascular magnetic resonance is increased in diabetes and associated with mortality and incident heart failure admission. Eur. Heart J. 2014, 35:657-664.
149. Bertoia M.L., Allison M.A., Manson J.E., Freiberg M.S., Kuller L.H., Solomon A.J., et al. Risk factors for sudden cardiac death in post-menopausal women. J. Am. Coll. Cardiol. 2012, 60:2674-2682.
150. Iribarren C., Karter A.J., Go A.S., Ferrara A., Liu J.Y., Sidney S., et al. Glycemic control and heart failure among adult patients with diabetes. Circulation 2001, 103:2668-2673.
151. Hayward R.A., Reaven P.D., Wiitala W.L., Bahn G.D., Reda D.J., Ge L., et al. Follow-up of glycemic control and cardiovascular outcomes in type 2 diabetes. N. Engl. J. Med. 2015, 372:2197-2206.
152. Castagno D., Baird-Gunning J., Jhund P.S., Biondi-Zoccai G., MacDonald M.R., Petrie M.C., et al. Intensive glycemic control has no impact on the risk of heart failure in type 2 diabetic patients: evidence from a 37,229 patient meta-analysis. Am. Heart J. 2011, 162:938-948. (e2).
153. Fatemi O., Yuriditsky E., Tsioufis C., Tsachris D., Morgan T., Basile J., et al. Impact of intensive glycemic control on the incidence of atrial fibrillation and associated cardiovascular outcomes in patients with type 2 diabetes mellitus (from the action to control cardiovascular risk in diabetes study). Am. J. Cardiol. 2014, 114:1217-1222.
154. Frangogiannis N.G. Targeting the transforming growth factor (TGF)-beta cascade in the remodeling heart: benefits and perils. J. Mol. Cell. Cardiol. 2014, 76:169-171.
155. Aronson D., Musallam A., Lessick J., Dabbah S., Carasso S., Hammerman H., et al. Impact of diastolic dysfunction on the development of heart failure in diabetic patients after acute myocardial infarction. Circ. Heart Fail. 2010, 3:125-131.
156. Frangogiannis N.G. The inflammatory response in myocardial injury, repair, and remodelling. Nat. Rev. Cardiol. 2014, 11:255-265.