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Circulation Research. 2000;87:1123-1132

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(Circulation Research. 2000;87:1123.)
© 2000 American Heart Association, Inc.


Clinical Research

Myocardial Cell Death in Human Diabetes

Andrea Frustaci, Jan Kajstura, Cristina Chimenti, Igor Jakoniuk, Annarosa Leri, Attilio Maseri, Bernardo Nadal-Ginard, Piero Anversa

From the Department of Medicine (J.K., I.J., A.L., B.N.-G., P.A.), New York Medical College, Valhalla, NY, and Department of Cardiology (A.F., C.C., A.M.), Sacred Heart University, Rome, Italy.

Correspondence to Piero Anversa, MD, Department of Medicine, New York Medical College, Vosburgh Pavilion, Room 302, Valhalla, NY 10595. E-mail piero_anversa{at}nymc.edu

Abstract—The renin-angiotensin system is upregulated with diabetes, and this may contribute to the development of a dilated myopathy. Angiotensin II (Ang II) locally may lead to oxidative damage, activating cardiac cell death. Moreover, diabetes and hypertension could synergistically impair myocardial structure and function. Therefore, apoptosis and necrosis were measured in ventricular myocardial biopsies obtained from diabetic and diabetic-hypertensive patients. Accumulation of a marker of oxidative stress, nitrotyrosine, and Ang II labeling were evaluated quantitatively. The diabetic heart showed cardiac hypertrophy, cavitary dilation, and depressed ventricular performance. These alterations were more severe with diabetes and hypertension. Diabetes was characterized by an 85-fold, 61-fold, and 26-fold increase in apoptosis of myocytes, endothelial cells, and fibroblasts, respectively. Apoptosis in cardiac cells did not increase additionally with diabetes and hypertension. Diabetes increased necrosis by 4-fold in myocytes, 9-fold in endothelial cells, and 6-fold in fibroblasts. However, diabetes and hypertension increased necrosis by 7-fold in myocytes and 18-fold in endothelial cells. Similarly, Ang II labeling in myocytes and endothelial cells increased more with diabetes and hypertension than with diabetes alone. Nitrotyrosine localization in cardiac cells followed a comparable pattern. In spite of the difference in the number of nitrotyrosine-positive cells with diabetes and with diabetes and hypertension, apoptosis and necrosis of myocytes, endothelial cells, and fibroblasts were detected only in cells containing this modified amino acid. In conclusion, local increases in Ang II with diabetes and with diabetes and hypertension may enhance oxidative damage, activating cardiac cell apoptosis and necrosis.


Key Words: oxidative damage • renin-angiotensin system • nitrotyrosine • heart failure




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Am. J. Physiol. Heart Circ. Physiol.Home page
V. Pastukh, S. Wu, C. Ricci, M. Mozaffari, and S. Schaffer
Reversal of hyperglycemic preconditioning by angiotensin II: role of calcium transport
Am J Physiol Heart Circ Physiol, April 1, 2005; 288(4): H1965 - H1975.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
A. Modesti, I. Bertolozzi, T. Gamberi, M. Marchetta, C. Lumachi, M. Coppo, F. Moroni, T. Toscano, G. Lucchese, G. F. Gensini, et al.
Hyperglycemia Activates JAK2 Signaling Pathway in Human Failing Myocytes via Angiotensin II-Mediated Oxidative Stress
Diabetes, February 1, 2005; 54(2): 394 - 401.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
T.-L. Yue, W. Bao, J.-L. Gu, J. Cui, L. Tao, X.-L. Ma, E. H. Ohlstein, and B. M. Jucker
Rosiglitazone Treatment in Zucker Diabetic Fatty Rats Is Associated With Ameliorated Cardiac Insulin Resistance and Protection From Ischemia/Reperfusion-Induced Myocardial Injury
Diabetes, February 1, 2005; 54(2): 554 - 562.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
R. Pop-Busui, I. Kirkwood, H. Schmid, V. Marinescu, J. Schroeder, D. Larkin, E. Yamada, D. M. Raffel, and M. J. Stevens
Sympathetic dysfunction in type 1 diabetes: Association with impaired myocardial blood flow reserve and diastolic dysfunction
J. Am. Coll. Cardiol., December 21, 2004; 44(12): 2368 - 2374.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
S. Ghosh, D. Qi, D. An, T. Pulinilkunnil, A. Abrahani, K.-H. Kuo, R. B. Wambolt, M. Allard, S. M. Innis, and B. Rodrigues
Brief episode of STZ-induced hyperglycemia produces cardiac abnormalities in rats fed a diet rich in n-6 PUFA
Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2518 - H2527.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
R. L. DeBiasi, B. A. Robinson, B. Sherry, R. Bouchard, R. D. Brown, M. Rizeq, C. Long, and K. L. Tyler
Caspase Inhibition Protects against Reovirus-Induced Myocardial Injury In Vitro and In Vivo
J. Virol., October 15, 2004; 78(20): 11040 - 11050.
[Abstract] [Full Text] [PDF]


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Nephrol Dial TransplantHome page
M. Nishimura, T. Hashimoto, H. Kobayashi, T. Fukuda, K. Okino, N. Yamamoto, N. Nakamura, T. Yoshikawa, H. Takahashi, and T. Ono
Association between cardiovascular autonomic neuropathy and left ventricular hypertrophy in diabetic haemodialysis patients
Nephrol. Dial. Transplant., October 1, 2004; 19(10): 2532 - 2538.
[Abstract] [Full Text] [PDF]


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Arch Intern MedHome page
H. S. Lim, R. J. MacFadyen, and G. Y. H. Lip
Diabetes Mellitus, the Renin-Angiotensin-Aldosterone System, and the Heart
Arch Intern Med, September 13, 2004; 164(16): 1737 - 1748.
[Abstract] [Full Text] [PDF]


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Endocr. Rev.Home page
Z. Y. Fang, J. B. Prins, and T. H. Marwick
Diabetic Cardiomyopathy: Evidence, Mechanisms, and Therapeutic Implications
Endocr. Rev., August 1, 2004; 25(4): 543 - 567.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
L. Raimondi, P. De Paoli, E. Mannucci, G. Lonardo, L. Sartiani, G. Banchelli, R. Pirisino, A. Mugelli, and E. Cerbai
Restoration of Cardiomyocyte Functional Properties by Angiotensin II Receptor Blockade in Diabetic Rats
Diabetes, July 1, 2004; 53(7): 1927 - 1933.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
Y. Shimoni and X.-F. Liu
Gender differences in ANG II levels and action on multiple K+ current modulation pathways in diabetic rats
Am J Physiol Heart Circ Physiol, July 1, 2004; 287(1): H311 - H319.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
J. I. Barzilay, R. A. Kronmal, J. S. Gottdiener, N. L. Smith, G. L. Burke, R. Tracy, P. J. Savage, and M. Carlson
The association of fasting glucose levels with congestive heart failure in diabetic adults >=65 years: The Cardiovascular Health Study
J. Am. Coll. Cardiol., June 16, 2004; 43(12): 2236 - 2241.
[Abstract] [Full Text] [PDF]


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ICVTSHome page
K. Doi, K. Hasegawa, M. Fujita, A. Yamazato, K. Yamanaka, M. Watanabe, K. Tambara, and M. Komeda
Clinical characteristics relevant to myocardial cell apoptosis: analysis of pericardial fluid
Interactive CardioVascular and Thoracic Surgery, June 1, 2004; 3(2): 359 - 362.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
R. Liu, T. Desta, H. He, and D. T. Graves
Diabetes Alters the Response to Bacteria by Enhancing Fibroblast Apoptosis
Endocrinology, June 1, 2004; 145(6): 2997 - 3003.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
Y. Pang, P. Bounelis, J. C. Chatham, and R. B. Marchase
Hexosamine Pathway Is Responsible for Inhibition by Diabetes of Phenylephrine-Induced Inotropy
Diabetes, April 1, 2004; 53(4): 1074 - 1081.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
D. Torella, M. Rota, D. Nurzynska, E. Musso, A. Monsen, I. Shiraishi, E. Zias, K. Walsh, A. Rosenzweig, M. A. Sussman, et al.
Cardiac Stem Cell and Myocyte Aging, Heart Failure, and Insulin-Like Growth Factor-1 Overexpression
Circ. Res., March 5, 2004; 94(4): 514 - 524.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
Y. Shimoni, M. Chuang, E. D. Abel, and David. L. Severson
Gender-dependent attenuation of cardiac potassium currents in type 2 diabetic db/db mice
J. Physiol., March 1, 2004; 555(2): 345 - 354.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
R. Marfella, C. Di Filippo, K. Esposito, F. Nappo, E. Piegari, S. Cuzzocrea, L. Berrino, F. Rossi, D. Giugliano, and M. D'Amico
Absence of Inducible Nitric Oxide Synthase Reduces Myocardial Damage During Ischemia Reperfusion in Streptozotocin-Induced Hyperglycemic Mice
Diabetes, February 1, 2004; 53(2): 454 - 462.
[Abstract] [Full Text]


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J Am Coll CardiolHome page
Y. Chandrashekhar, S. Sen, R. Anway, A. Shuros, and I. Anand
Long-Term caspase inhibition ameliorates apoptosis, reduces myocardial troponin-I cleavage, protects left ventricular function, and attenuates remodeling in rats with myocardial infarction
J. Am. Coll. Cardiol., January 21, 2004; 43(2): 295 - 301.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
L. Quagliaro, L. Piconi, R. Assaloni, L. Martinelli, E. Motz, and A. Ceriello
Intermittent High Glucose Enhances Apoptosis Related to Oxidative Stress in Human Umbilical Vein Endothelial Cells: The Role of Protein Kinase C and NAD(P)H-Oxidase Activation
Diabetes, November 1, 2003; 52(11): 2795 - 2804.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
C.-H. Huang, S. F. Vatner, A. P. Peppas, G. Yang, and R. K. Kudej
Cardiac Nerves Affect Myocardial Stunning Through Reactive Oxygen and Nitric Oxide Mechanisms
Circ. Res., October 31, 2003; 93(9): 866 - 873.
[Abstract] [Full Text] [PDF]


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HeartHome page
T Hayashi, K Sohmiya, A Ukimura, S Endoh, T Mori, H Shimomura, M Okabe, F Terasaki, and Y Kitaura
Angiotensin II receptor blockade prevents microangiopathy and preserves diastolic function in the diabetic rat heart
Heart, October 1, 2003; 89(10): 1236 - 1242.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
C. Cheng and D. W. Zochodne
Sensory Neurons With Activated Caspase-3 Survive Long-Term Experimental Diabetes
Diabetes, September 1, 2003; 52(9): 2363 - 2371.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
A. Gonzalez, M. A Fortuno, R. Querejeta, S. Ravassa, B. Lopez, N. Lopez, and J. Diez
Cardiomyocyte apoptosis in hypertensive cardiomyopathy
Cardiovasc Res, September 1, 2003; 59(3): 549 - 562.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
E. Picano
Diabetic cardiomyopathy: the importance of being earliest
J. Am. Coll. Cardiol., August 6, 2003; 42(3): 454 - 457.
[Full Text] [PDF]


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Diabetes CareHome page
A. Ceriello
New Insights on Oxidative Stress and Diabetic Complications May Lead to a "Causal" Antioxidant Therapy
Diabetes Care, May 1, 2003; 26(5): 1589 - 1596.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
M. A. Fortuno, A. Gonzalez, S. Ravassa, B. Lopez, and J. Diez
Clinical implications of apoptosis in hypertensive heart disease
Am J Physiol Heart Circ Physiol, May 1, 2003; 284(5): H1495 - H1506.
[Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
A. S. Neitzel, A. N. Carley, and D. L. Severson
Chylomicron and palmitate metabolism by perfused hearts from diabetic mice
Am J Physiol Endocrinol Metab, February 1, 2003; 284(2): E357 - E365.
[Abstract] [Full Text] [PDF]


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Pharmacol. Rev.Home page
I. V. Turko and F. Murad
Protein Nitration in Cardiovascular Diseases
Pharmacol. Rev., December 1, 2002; 54(4): 619 - 634.
[Abstract] [Full Text] [PDF]