Myocardial fibrosis and apoptosis, but not inflammation, are present in long-term experimental diabetes

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 6, 2009, Pages

  Ares Carrasco, S ^a   Picatoste, B ^a   Benito Martin A ^a   Zubiri, I ^a   Sanz, A B ^a   Sanchez Nino M D ^a   Ortiz, A ^a,b   Egido, J ^a,b   Tunon J ^a,b   Lorenzo, O ^a,b  

^a HOSPITAL UNIVERSITARIO FUNDACIÓN JIMÉNEZ DÍAZ   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Heart; Hypertension; Inflammation

Indexed keywords

ANGIOTENSINOGEN; ANTIOXIDANT; CASPASE 3; CATALASE; CONNECTIVE TISSUE GROWTH FACTOR; FAS ANTIGEN; FAS LIGAND; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; MATRIX PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; OXIDIZING AGENT; PROTEIN BAX; SMAD3 PROTEIN; SMAD4 PROTEIN; STREPTOZOCIN; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASSAY; CELL INFILTRATION; CLINICAL FEATURE; CONTROLLED STUDY; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION; HEART CELL CULTURE; HEART LEFT VENTRICLE; HEART MUSCLE; HEART MUSCLE FIBROSIS; HEART MUSCLE INJURY; HISTOLOGY; HYPERTENSION; INFLAMMATORY CELL; INJECTION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MYOCARDITIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; STREPTOZOCIN DIABETES; WESTERN BLOTTING;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BIOLOGICAL MARKERS; CARDIOMYOPATHIES; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; EXTRACELLULAR MATRIX PROTEINS; FIBROSIS; HYPERTENSION; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MYOCARDIUM; RATS; RATS, INBRED SHR; RATS, INBRED WKY; TIME FACTORS;

EID: 72249102361     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00157.2009     Document Type: Article

References (41)

1. Bell DS. Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 26: 2433-2441, 2003.
2. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 115: 3213-3223, 2007.
3. Casadei B. The emerging role of neural nitric oxide synthase in the regulation of myocardial function. Exp Physiol 91: 943-955, 2006.
4. Cheng M, Gao HQ, Xu L, Li BY, Zhang H, Li XH. Cardioprotective effects of grape seed proanthocyanidins extracts in streptozocin induced diabetic rats. J Cardiovasc Pharmacol 50: 503-509, 2007. (Pubitemid 350146452)
5. Damå s JK, Aukrust P, Ueland T, Odegaard A, Eiken HG, Gullestad L, Sejersted OM, Christensen G. Monocyte chemoattractant protein-1 enhances and interleukin-10 suppresses the production of inflammatory cytokines in adult rat cardiomyocytes. Basic Res Cardiol 96: 345-352, 2001.
6. Ekhterae D, Lin Z, Lundberg MS, Crow MT, Brosius FC, Nunez G. ARC inhibits cytochrome c release from mitochondria and protects against hypoxia-induced apoptosis in heart-derived H9c2 cells. Circ Res 85: e70-e77, 1999.
7. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomiopathy: evidence, mechanisms and terapeutical implications. Endocr Rev 25: 543-567, 2004.
8. Feuerstein GZ, Young PR. Apoptosis in cardiac diseases: stress- and mitogen-activated signaling pathways. Cardiovasc Res 45: 560-569, 2000.
9. Fiordaliso F, Li B, Latini R, Sonnenblick EH, Anversa P, Leri A, Kajstura J. Myocyte death in streptozotocin-induced diabetes in rats is angiotensin II-dependent. Lab Invest 80: 513-527, 2000. (Pubitemid 30226633)
10. Fiordaliso F, De Angelis N, Bai A, Cuccovillo I, Salio M, Serra DM, Bianchi R, Razzetti R, Latini R, Masson S. Effect of beta-adrenergic and renin-angiotensin system blockade on myocyte apoptosis and oxidative stress in diabetic hypertensive rats. Life Sci 81: 951-959, 2007.
11. Fisman EZ, Motro M, Tenenbaum A. Cardiovascular diabetology in the core of a novel interleukins classification: the bad, the good and the aloof. Cardiovasc Diabetol 2: 11, 2003. (Pubitemid 38751102)
12. Forcheron F, Basset A, Abdallah P, Del Carmine P, Gadot N, Beylot M. Diabetic cardiomyopathy: effects of fenofibrate and metformin in an experimental model-the Zucker diabetic rat. Cardiovasc Diabetol 8: 16, 2009.
13. Foss NT, Foss-Freitas MC, Ferreira MA, Cardili RN, Barbosa CM, Foss MC. Impaired cytokine production by peripheral blood mononuclear cells in type 1 diabetic patients. Diabetes Metab 33: 439-443, 2007. (Pubitemid 350213453)
14. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, Nadal-Ginard B, Anversa P. Myocyte cell death in human diabetes. Circ Res 87: 1123-1132, 2000.
15. Gooch JL, Y Gorin, BX Zhang, Abboud HE. Involvement of calcineurin in transforming growth factor-β-mediated regulation of extracellular matrix accumulation. J Biol Chem 279: 15561-15570, 2004.
16. Gurusamy N, Watanabe K, Ma M, Prakash P, Hirabayashi K, Zhang S, Muslin AJ, Kodama M, Aizawa Y. Glycogen synthase kinase 3beta together with 14-3-3 protein regulates diabetic cardiomyopathy: effect of losartan and tempol. FEBS Lett 580: 1932-1940, 2006.
17. Hamblin M, Friedman DB, Hill S, Caprioli RM, Smith HM, Hill MF. Alterations in the diabetic myocardial proteome coupled with increased myocardial oxidative stress underlies diabetic cardiomyopathy. J Mol Cell Cardiol 42: 884-895, 2007. (Pubitemid 46527591)
18. Heeschen C, Dimmeler S, Hamm CW, Fichtlscherer S, Boersma E, Simoons ML, Zeiher AM; Study Investigators CAPTURE. Serum level of the antiinflammatory cytokine interleukin-10 is an important prognostic determinant in patients with acute coronary syndromes. Circulation 107: 2109-2114, 2003. (Pubitemid 36532192)
19. Hishikawa K, Oemar BS, Tanner FC, Nakaki T, Lüscher TF, Fujii T. Connective tissue growth factor induces apoptosis in human breast cancer cell line MCF-7. J Biol Chem 274: 37461-37466, 1999. (Pubitemid 30016834)
20. Kai H, Kuwahara F, Tokuda K, Imaizumi T. Diastolic dysfunction in hypertensive hearts: roles of perivascular inflammation and reactive myocardial fibrosis. Hypertens Res 28: 483-490, 2005. (Pubitemid 41195386)
21. Kaur K, Sharma AK, Dhingra S, Singal PK. Interplay of TNF-alpha and IL-10 in regulating oxidative stress in isolated adult cardiac myocytes. J Mol Cell Cardiol 41: 1023-1030, 2006. (Pubitemid 44791332)
22. Kawaguchi M, Techigawara M, Ishihata T, Asakura T, Saito F, Maehara K, Maruyama Y. A comparison of ultrastructural changes on endomyocardial biopsy specimens obtained from patients with diabetes mellitus with and without hypertension. Heart Vessels 12: 267, 1997. (Pubitemid 28477120)
23. Kim EY, Moudgil KD. Regulation of autoimmune inflammation by pro-inflammatory cytokines. Immunol Lett 120: 1-5, 2008.
24. Kim SG, Jong HS, Kim TY, Lee JW, Kim NK, Hong SH, Bang YJ. Transforming growth factor-beta 1 induces apoptosis through Fas ligand-independent activation of the Fas death pathway in human gastric SNU-620 carcinoma cells. Mol Biol Cell 15: 420-434, 2004.
25. Klöting N, Follak N, Klöting I. Diabetes per se and metabolic state influence gene expression in tissue-dependent manner of BB/OK rats. Diabetes Metab Res Rev 21: 281-287, 2005. (Pubitemid 40716161)
26. Lanza GA, Pitocco D, Navarese EP, Sestito A, Sgueglia GA, Manto A, Infusino F, Musella T, Ghirlanda G, Crea F. Association between cardiac autonomic dysfunction and inflammation in type 1 diabetic patients: effect of beta-blockade. Eur Heart J 28: 814-820, 2007. (Pubitemid 47343595)
27. Massagué J, Cheifetz S, Laiho M, Ralph DA, Weis FM, Zentella A. Transforming growth factor-beta. Cancer Surv 12: 81-103, 1992.
28. Nonaka-Sarukawa M, Okada T, Ito T, Yamamoto K, Yoshioka T, Nomoto T, Hojo Y, Shimpo M, Urabe M, Mizukami H, Kume A, Ikeda U, Shimada K, Ozawa K. Adeno-associated virus vector-mediated systemic interleukin-10 expression ameliorates hypertensive organ damage in Dahl salt-sensitive rats. J Gene Med 10: 368-374, 2008.
29. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 98: 596-605, 2006. (Pubitemid 43755278)
30. Rajan SK, Gokhale SM. Cardiovascular function in patients with insulindependent diabetes mellitus: a study using noninvasive methods. Ann NY Acad Sci 958: 425-430, 2002.
31. Ray KK, Cannon CP, Morrow DA, Kirtane AJ, Buros J, Rifai N, McCabe CH, Gibson CM, Braunwald E. Synergistic relationship between hyperglycaemia and inflammation with respect to clinical outcomes in non-ST-elevation acute coronary syndromes: analyses from OPUS-TIMI 16 and TACTICS-TIMI 18. Eur Heart J 28: 806-813, 2007. (Pubitemid 47343593)
32. Rees DA, Alcolado JC. Animal models of diabetes mellitus. Diabet Med 22: 359-370, 2005.
33. Rupérez M, Lorenzo O, Blanco-Colio LM, Esteban V, Egido J, Ruiz-Ortega M. Connective tissue growth factor is a mediator of angiotensin II-induced fibrosis. Circulation 108: 1499-1505, 2003. (Pubitemid 37176458)
34. Schram MT, Chaturvedi N, Schalkwijk CG, Fuller JH, Stehouwer CDA. Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes: the EURODIAB Prospective Complications Study. Diabetologia 48: 370-378, 2005. (Pubitemid 40543311)
35. Schröder D, Heger J, Piper HM, Euler G. Angiotensin II stimulates apoptosis via TGF-beta1 signaling in ventricular cardiomyocytes of rat. J Mol Med 84: 975-983, 2006. \
36. van Heerebeek L, Hamdani N, Handoko ML, Falcao-Pires I, Musters RJ, Kupreishvili K, Ijsselmuiden AJ, Schalkwijk CG, Bronzwaer JG, Diamant M, Borbély A, van der Velden J, Stienen GJ, Laarman GJ, Niessen HW, Paulus WJ. Diastolic stiffness of the failing diabetic heart: importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation 117: 43-51, 2008.
37. Sardão VA, Oliveira PJ, Holy J, Oliveira CR, Wallace BK. Vital imaging of H9c2 myoblasts exposed to tert-butylhydroperoxide- characterization of morphological features of cell death. BMC Cell Biol 8: 11, 2007. (Pubitemid 46477764)
38. Westermann D, Rutschow S, Jäger S, Linderer A, Anker S, Riad A, Unger T, Schultheiss HP, Pauschinger M, Tschöpe C. Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy: the role of angiotensin type 1 receptor antagonism. Diabetes 56: 641-646, 2007. (Pubitemid 46348458)
39. Westermann D, Van Linthout S, Dhayat S, Dhayat N, Escher F, Bücker-Gärtner C, Spillmann F, Noutsias M, Riad A, Schultheiss HP, Tschöpe C. Cardioprotective and anti-inflammatory effects of interleukin converting enzyme inhibition in experimental diabetic cardiomyopathy. Diabetes 56: 1834-1841, 2007.
40. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 1047-1053, 2004.
41. Yoshida T, Hanawa H, Toba K, Watanabe H, Watanabe R, Yoshida K, Abe S, Kato K, Kodama M, Aizawa Y. Expression of immunological molecules by cardiomyocytes and inflammatory and interstitial cells in rat autoimmune myocarditis. Cardiovasc Res 68: 278-288, 2005. (Pubitemid 41428424)