Intermedin protects against myocardial ischemia-reperfusion injury in diabetic rats

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Li, Hong ^a   Bian, Yunfei ^a   Zhang, Nana ^a   Guo, Jia ^a   Wang, Cheng ^a   Lau, Wayne Bond ^b   Xiao, Chuanshi ^a  

^a SHANXI MEDICAL UNIVERSITY   (China)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Apoptosis; Diabetes; Inflammatory; Intermedin; Ischemia reperfusion; Oxidative stress

Indexed keywords

CREATINE KINASE MB; GLUCOSE; GLYCOPROTEIN GP 91; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERMEDIN; LACTATE DEHYDROGENASE; MALONALDEHYDE; PROTEIN P22; PROTEIN P67; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; ADRENOMEDULLIN; AUTACOID; CARDIOTONIC AGENT; CYTOKINE; INTERMEDIN PROTEIN, RAT; NEUROPEPTIDE; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTERY LIGATION; ARTICLE; BLOOD SAMPLING; CELL DEATH; CONTROLLED STUDY; CORONARY ARTERY CIRCUMFLEX BRANCH; CYTOKINE RELEASE; GLUCOSE BLOOD LEVEL; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE ISCHEMIA; HEART PROTECTION; INFLAMMATION; MALE; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; RAT; REPERFUSION INJURY; STREPTOZOCIN DIABETES; ANIMAL; CHEMICALLY INDUCED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC CARDIOMYOPATHIES; DRUG EFFECTS; HEART MUSCLE CELL; METABOLISM; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME;

ADRENOMEDULLIN; ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC CARDIOMYOPATHIES; INFLAMMATION MEDIATORS; MALE; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NEUROPEPTIDES; OXIDATIVE STRESS; RATS, SPRAGUE-DAWLEY; STREPTOZOCIN; TIME FACTORS; VENTRICULAR FUNCTION, LEFT;

EID: 84879040386     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-91     Document Type: Article

References (67)

1. Gross ER, Hsu AK, Gross GJ. Diabetes abolishes morphine-induced cardioprotection via multiple pathways upstream of glycogen synthase kinase-3beta. Diab 2007, 56(1):127-136.
2. Ametov AS, P'Ianykh OP, Aslandziia EN. Acute coronary syndrome in patients with type 2 diabetes mellitus. Ter Arkh 2011, 83(9):66-70.
3. Kappert K, Bohm M, Schmieder R, Schumacher H, Teo K, Yusuf S, Sleight P, Unger T. Impact of sex on cardiovascular outcome in patients at high cardiovascular risk: analysis of the Telmisartan Randomized Assessment Study in ACE-Intolerant Subjects With Cardiovascular Disease (TRANSCEND) and the Ongoing Telmisartan Alone and in Combination With Ramipril Global End Point Trial (ONTARGET). Circ 2012, 126(8):934-941.
4. Tanaka K, Kehl F, Gu W, Krolikowski JG, Pagel PS, Warltier DC, Kersten JR. Isoflurane-induced preconditioning is attenuated by diabetes. Am J Physiol Heart Circ Physiol 2002, 282(6):H2018-2023.
5. Hotta H, Miura T, Miki T, Togashi N, Maeda T, Kim SJ, Tanno M, Yano T, Kuno A, Itoh T, et al. Angiotensin II type 1 receptor-mediated upregulation of calcineurin activity underlies impairment of cardioprotective signaling in diabetic hearts. Circ Res 2010, 106(1):129-132. 10.1161/CIRCRESAHA.109.205385, 19910577.
6. Winer N, Sowers JR. Epidemiology of diabetes. J Clin Pharmacol 2004, 44(4):397-405. 10.1177/0091270004263017, 15051748.
7. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA 1979, 241(19):2035-2038. 10.1001/jama.1979.03290450033020, 430798.
8. Danaei G, Friedman AB, Oza S, Murray CJ, Ezzati M. Diabetes prevalence and diagnosis in US states: analysis of health surveys. Popul health metrics 2009, 7:16.
9. Potier L, Waeckel L, Vincent MP, Chollet C, Gobeil F, Marre M, Bruneval P, Richer C, Roussel R, Alhenc-Gelas F, et al. Selective kinin receptor agonists as cardioprotective agents in myocardial ischemia and diabetes. J Pharmacol Exp Ther 2013, [Epub ahead of print].
10. Roh J, Chang CL, Bhalla A, Klein C, Hsu SY. Intermedin is a calcitonin/calcitonin gene-related peptide family peptide acting through the calcitonin receptor-like receptor/receptor activity-modifying protein receptor complexes. J Biol Chem 2004, 279(8):7264-7274.
11. Yang JH, Qi YF, Jia YX, Pan CS, Zhao J, Yang J, Chang JK, Tang CS. Protective effects of intermedin/adrenomedullin2 on ischemia/reperfusion injury in isolated rat hearts. Pept 2005, 26(3):501-507.
12. Bell D, Campbell M, Ferguson M, Sayers L, Donaghy L, O'Regan A, Jewhurst V, Harbinson M. AM(1)-receptor-dependent protection by intermedin of human vascular and cardiac non-vascular cells from ischaemia-reperfusion injury. J Physiol 2012, 590(Pt 5):1181-1197. 3381824, 22183724.
13. Hirose T, Totsune K, Mori N, Morimoto R, Hashimoto M, Nakashige Y, Metoki H, Asayama K, Kikuya M, Ohkubo T, et al. Increased expression of adrenomedullin 2/intermedin in rat hearts with congestive heart failure. Eur J Heart Fail 2008, 10(9):840-849. 10.1016/j.ejheart.2008.06.020, 18692436.
14. Dong F, Taylor MM, Samson WK, Ren J. Intermedin (adrenomedullin-2) enhances cardiac contractile function via a protein kinase C- and protein kinase A-dependent pathway in murine ventricular myocytes. J Appl Physiol (Bethesda, Md : 1985) 2006, 101(3):778-784.
15. Yang JH, Cai Y, Duan XH, Ma CG, Wang X, Tang CS, Qi YF. Intermedin 1-53 inhibits rat cardiac fibroblast activation induced by angiotensin II. Regul Pept 2009, 158(1-3):19-25.
16. Pan CS, Yang JH, Cai DY, Zhao J, Gerns H, Yang J, Chang JK, Tang CS, Qi YF. Cardiovascular effects of newly discovered peptide intermedin/adrenomedullin 2. Pept 2005, 26(9):1640-1646.
17. Du QX, Yue W, Wang YY. [Effect and mechanism of intermedin in acute rat cardiac ischemic injury]. Fa yi xue za zhi 2011, 27(3):164-168.
18. Teng X, Song J, Zhang G, Cai Y, Yuan F, Du J, Tang C, Qi Y. Inhibition of endoplasmic reticulum stress by intermedin(1-53) protects against myocardial injury through a PI3 kinase-Akt signaling pathway. J Mol Med (Berlin, Germany) 2011, 89(1205):1195.
19. Song JQ, Teng X, Cai Y, Tang CS, Qi YF. Activation of Akt/GSK-3beta signaling pathway is involved in intermedin(1-53) protection against myocardial apoptosis induced by ischemia/reperfusion. Apoptosis 2009, 14(11):1299-1307. 10.1007/s10495-009-0398-7, 19757065.
20. He RX, Gu CL, Shen F, Zhang XM. Changes in expression of adrenomedullin in the myocardium of streptozotocin-induced diabetic rats. Chin Med J 2007, 120(3):187-191.
21. Soetikno V, Watanabe K, Sari FR, Harima M, Thandavarayan RA, Veeraveedu PT, Arozal W, Sukumaran V, Lakshmanan AP, Arumugam S, et al. Curcumin attenuates diabetic nephropathy by inhibiting PKC-alpha and PKC-beta1 activity in streptozotocin-induced type I diabetic rats. Mol Nutr Food Res 2011, 55(11):1655-1665. 10.1002/mnfr.201100080, 22045654.
22. Kromann H, Christy M, Lernmark A, Nedergaard M, Nerup J. The low dose streptozotocin murine model of type 1 (insulin-dependent) diabetes mellitus: studies in vivo and in vitro of the modulating effect of sex hormones. Diabetologia 1982, 22(3):194-198.
23. Fang J, Chen L, Wu L, Li W. Intra-cardiac remote ischemic post-conditioning attenuates ischemia-reperfusion injury in rats. Scand Cardiovas J: SCJ 2009, 43(6):386-394.
24. Gao Y, Yao X, Zhang Y, Li W, Kang K, Sun L, Sun X. The protective role of hydrogen sulfide in myocardial ischemia-reperfusion-induced injury in diabetic rats. Int J Cardiol 2011, 152(2):177-183. 10.1016/j.ijcard.2010.07.012, 21316771.
25. Zhang HY, Jiang W, Liu JY, Li Y, Chen CL, Xin HB, Huang DJ. Intermedin is upregulated and has protective roles in a mouse ischemia/reperfusion model. Hypertens Res 2009, 32(10):861-868. 10.1038/hr.2009.120, 19680258.
26. Zhang L, Ma J, Liu H. Protective effect of ischemic postconditioning against ischemia reperfusion-induced myocardium oxidative injury in IR rats. Mol 2012, 17(4):3805-3817.
27. Cao J, Vecoli C, Neglia D, Tavazzi B, Lazzarino G, Novelli M, Masiello P, Wang YT, Puri N, Paolocci N, et al. Cobalt-Protoporphyrin Improves Heart Function by Blunting Oxidative Stress and Restoring NO Synthase Equilibrium in an Animal Model of Experimental Diabetes. Front Physiol 2012, 3:160. 3366474, 22675305.
28. Okazaki T, Otani H, Shimazu T, Yoshioka K, Fujita M, Iwasaka T. Ascorbic acid and N-acetyl cysteine prevent uncoupling of nitric oxide synthase and increase tolerance to ischemia/reperfusion injury in diabetic rat heart. Free Radic Res 2011, 45(10):1173-1183. 10.3109/10715762.2011.605361, 21756052.
29. Rajesh M, Mukhopadhyay P, Batkai S, Patel V, Saito K, Matsumoto S, Kashiwaya Y, Horvath B, Mukhopadhyay B, Becker L, et al. Cannabidiol attenuates cardiac dysfunction, oxidative stress, fibrosis, and inflammatory and cell death signaling pathways in diabetic cardiomyopathy. J Am Coll Cardiol 2010, 56(25):2115-2125. 10.1016/j.jacc.2010.07.033, 3026637, 21144973.
30. De Waard MC, van der Velden J, Boontje NM, Dekkers DH, Van Haperen R, Kuster DW, Lamers JM, De Crom R, Duncker DJ. Detrimental effect of combined exercise training and eNOS overexpression on cardiac function after myocardial infarction. Am J Physiol Heart Circ Physiol 2009, 296(5):H1513-1523. 10.1152/ajpheart.00485.2008, 19286956.
31. Qin YW, Teng X, He JQ, Du J, Tang CS, Qi YF. Increased plasma levels of intermedin and brain natriuretic peptide associated with severity of coronary stenosis in acute coronary syndrome. Pept 2013, 42:84-88.
32. Feuvray D, Lopaschuk GD. Controversies on the sensitivity of the diabetic heart to ischemic injury: the sensitivity of the diabetic heart to ischemic injury is decreased. Cardiovasc Res 1997, 34(1):113-120. 10.1016/S0008-6363(97)00037-0, 9217880.
33. Ravingerova T, Neckar J, Kolar F, Stetka R, Volkovova K, Ziegelhoffer A, Styk J. Ventricular arrhythmias following coronary artery occlusion in rats: is the diabetic heart less or more sensitive to ischaemia?. Basic Res Cardiol 2001, 96(2):160-168. 10.1007/s003950170066, 11327334.
34. Backlund T, Palojoki E, Saraste A, Eriksson A, Finckenberg P, Kyto V, Lakkisto P, Mervaala E, Voipio-Pulkki LM, Laine M, et al. Sustained cardiomyocyte apoptosis and left ventricular remodelling after myocardial infarction in experimental diabetes. Diabetologia 2004, 47(2):325-330. 10.1007/s00125-003-1311-5, 14722653.
35. Miki T, Itoh T, Sunaga D, Miura T. Effects of diabetes on myocardial infarct size and cardioprotection by preconditioning and postconditioning. Cardiovasc Diabetol 2012, 11:67. 10.1186/1475-2840-11-67, 3461466, 22694800.
36. Rodrigues B, Rosa KT, Medeiros A, Schaan BD, Brum PC, De Angelis K, Irigoyen MC. Hyperglycemia can delay left ventricular dysfunction but not autonomic damage after myocardial infarction in rodents. Cardiovasc Diabetol 2011, 10:26. 10.1186/1475-2840-10-26, 3084163, 21470409.
37. Chu LM, Osipov RM, Robich MP, Feng J, Oyamada S, Bianchi C, Sellke FW. Is hyperglycemia bad for the heart during acute ischemia?. J Thorac Cardiovasc Surg 2010, 140(6):1345-1352. 10.1016/j.jtcvs.2010.05.009, 2949689, 20542299.
38. Lekli I, Szabo G, Juhasz B, Das S, Das M, Varga E, Szendrei L, Gesztelyi R, Varadi J, Bak I, et al. Protective mechanisms of resveratrol against ischemia-reperfusion-induced damage in hearts obtained from Zucker obese rats: the role of GLUT-4 and endothelin. Am J Physiol Heart Circ Physiol 2008, 294(2):H859-866. 10.1152/ajpheart.01048.2007, 18065527.
39. Chu LM, Osipov RM, Robich MP, Feng J, Sheller MR, Sellke FW. Effect of thrombin fragment (TP508) on myocardial ischemia reperfusion injury in a model of type 1 diabetes mellitus. Circ 2010, 122(11 Suppl):S162-169.
40. Marso SP, Miller T, Rutherford BD, Gibbons RJ, Qureshi M, Kalynych A, Turco M, Schultheiss HP, Mehran R, Krucoff MW, et al. Comparison of myocardial reperfusion in patients undergoing percutaneous coronary intervention in ST-segment elevation acute myocardial infarction with versus without diabetes mellitus (from the EMERALD Trial). Am J Cardiol 2007, 100(2):206-210. 10.1016/j.amjcard.2007.02.080, 17631071.
41. Alegria JR, Miller TD, Gibbons RJ, Yi QL, Yusuf S. Infarct size, ejection fraction, and mortality in diabetic patients with acute myocardial infarction treated with thrombolytic therapy. Am Heart J 2007, 154(4):743-750. 10.1016/j.ahj.2007.06.020, 17893003.
42. Sarkozy M, Zvara A, Gyemant N, Fekete V, Kocsis GF, Pipis J, Szucs G, Csonka C, Puskas LG, Ferdinandy P, et al. Metabolic syndrome influences cardiac gene expression pattern at the transcript level in male ZDF rats. Cardiovasc Diabetol 2013, 12:16. 10.1186/1475-2840-12-16, 3599923, 23320804.
43. Hu ZC, Chen YD, Ren YH. Methylprednisolone improves microcirculation in streptozotocin-induced diabetic rats after myocardial ischemia/reperfusion. Chin Med J 2011, 124(6):923-929.
44. Wu Y, Xia ZY, Dou J, Zhang L, Xu JJ, Zhao B, Lei S, Liu HM. Protective effect of ginsenoside Rb1 against myocardial ischemia/reperfusion injury in streptozotocin-induced diabetic rats. Mol Biol Rep 2011, 38(7):4327-4335. 10.1007/s11033-010-0558-4, 21113666.
45. Kain V, Kumar S, Sitasawad SL. Azelnidipine prevents cardiac dysfunction in streptozotocin-diabetic rats by reducing intracellular calcium accumulation, oxidative stress and apoptosis. Cardiovasc Diabetol 2011, 10:97. 10.1186/1475-2840-10-97, 3234183, 22054019.
46. Bell D, Zhao Y, McCoy FP, Devine A, McDermott BJ. Expression of the counter-regulatory peptide intermedin is augmented in the presence of oxidative stress in hypertrophied cardiomyocytes. Cell Physiol Biochem 2008, 21(5-6):409-420.
47. Cifuentes ME, Pagano PJ. Targeting reactive oxygen species in hypertension. Curr Opin Nephrol Hypertens 2006, 15(2):179-186. 10.1097/01.mnh.0000214776.19233.68, 16481886.
48. Ibrahim HM, El-Elaimy IA, Saad Eldien HM, Badr BM, Rabah DM, Badr G. Blocking type I interferon signaling rescues lymphocytes from oxidative stress, exhaustion, and apoptosis in a streptozotocin-induced mouse model of type I diabetes. Oxid Med Cell Longev 2013, 2013:148725. 3606800, 23533683.
49. Isabelle M, Vergeade A, Moritz F, Dautreaux B, Henry JP, Lallemand F, Richard V, Mulder P, Thuillez C, Monteil C. NADPH oxidase inhibition prevents cocaine-induced up-regulation of xanthine oxidoreductase and cardiac dysfunction. J Mol Cell Cardiol 2007, 42(2):326-332. 10.1016/j.yjmcc.2006.11.011, 17217956.
50. Heymes C, Bendall JK, Ratajczak P, Cave AC, Samuel JL, Hasenfuss G, Shah AM. Increased myocardial NADPH oxidase activity in human heart failure. J Am Coll Cardiol 2003, 41(12):2164-2171. 10.1016/S0735-1097(03)00471-6, 12821241.
51. Li JM, Gall NP, Grieve DJ, Chen M, Shah AM. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertens 2002, 40(4):477-484.
52. Xiao L, Pimentel DR, Wang J, Singh K, Colucci WS, Sawyer DB. Role of reactive oxygen species and NAD(P)H oxidase in alpha(1)-adrenoceptor signaling in adult rat cardiac myocytes. Am J Physiol Cell Physiol 2002, 282(4):C926-934. 10.1152/ajpcell.00254.2001, 11880281.
53. Soetikno V, Sari FR, Sukumaran V, Lakshmanan AP, Mito S, Harima M, Thandavarayan RA, Suzuki K, Nagata M, Takagi R, et al. Curcumin prevents diabetic cardiomyopathy in streptozotocin-induced diabetic rats: possible involvement of PKC-MAPK signaling pathway. Eur J Pharm Sci 2012, 47(3):604-614. 10.1016/j.ejps.2012.04.018, 22564708.
54. Yoshida K, Kobayashi N, Ohno T, Fukushima H, Matsuoka H. Cardioprotective effect of angiotensin II type 1 receptor antagonist associated with bradykinin-endothelial nitric oxide synthase and oxidative stress in Dahl salt-sensitive hypertensive rats. J Hypertens 2007, 25(8):1633-1642. 10.1097/HJH.0b013e32814db89f, 17620960.
55. Becher PM, Lindner D, Frohlich M, Savvatis K, Westermann D, Tschope C. Assessment of cardiac inflammation and remodeling during the development of streptozotocin-induced diabetic cardiomyopathy in vivo: A time course analysis. Int J Mol Med 2013,
56. El-Benna J, Dang PM, Perianin A. Towards specific NADPH oxidase inhibition by small synthetic peptides. Cell Mol Life Sci 2012, 69(14):2307-2314. 10.1007/s00018-012-1008-3, 22562604.
57. Munzel G, Schlier A, Schreckenberg R, Abdallah Y, Schluter KD. Rat intermedin1-47 does not improve functional recovery in postischemic hearts. Naunyn Schmiedebergs Arch Pharmacol 2011, 384(6):535-542. 10.1007/s00210-011-0680-4, 21881857.
58. Pires AL, Pinho M, Alves BS, Pinho S, Sena C, Seica RM, Leite-Moreira AF. Reverse myocardial effects of intermedin in pressure-overloaded hearts: role of endothelial nitric oxide synthase activity. J Physiol 2013, 591(Pt 3):677-687.
59. Ou HC, Tzang BS, Chang MH, Liu CT, Liu HW, Lii CK, Bau DT, Chao PM, Kuo WW. Cardiac contractile dysfunction and apoptosis in streptozotocin-induced diabetic rats are ameliorated by garlic oil supplementation. J Agric Food Chem 2010, 58(19):10347-10355. 10.1021/jf101606s, 20836552.
60. Li CJ, Zhang QM, Li MZ, Zhang JY, Yu P, Yu DM. Attenuation of myocardial apoptosis by alpha-lipoic acid through suppression of mitochondrial oxidative stress to reduce diabetic cardiomyopathy. Chin Med J 2009, 122(21):2580-2586.
61. Shirpoor A, Salami S, Khadem-Ansari MH, Ilkhanizadeh B, Pakdel FG, Khademvatani K. Cardioprotective effect of vitamin E: rescues of diabetes-induced cardiac malfunction, oxidative stress, and apoptosis in rat. J Diabetes Complications 2009, 23(5):310-316. 10.1016/j.jdiacomp.2008.02.009, 18394933.
62. Teng X, Bian Y, Cai Y, Duan X, Yuan F, Du J, Wu W, Wang X, Tang C, Qi Y. Downregulation of endogenous intermedin augmented myocardial injury in rats with ischemia/reperfusion. Horm Metab Res 2013, 45(3):206-212.
63. Xiao CY, Chen M, Zsengeller Z, Szabo C. Poly(ADP-ribose) polymerase contributes to the development of myocardial infarction in diabetic rats and regulates the nuclear translocation of apoptosis-inducing factor. J Pharmacol Exp Ther 2004, 310(2):498-504. 10.1124/jpet.104.066803, 15054118.
64. Di Filippo C, Marfella R, Cuzzocrea S, Piegari E, Petronella P, Giugliano D, Rossi F, D'Amico M. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes 2005, 54(3):803-810. 10.2337/diabetes.54.3.803, 15734859.
65. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circ 2005, 111(11):1448-1454.
66. Turer AT, Hill JA. Pathogenesis of myocardial ischemia-reperfusion injury and rationale for therapy. Am J Cardiol 2010, 106(3):360-368. 10.1016/j.amjcard.2010.03.032, 2957093, 20643246.
67. Wang Y, Schmeichel AM, Iida H, Schmelzer JD, Low PA. Enhanced inflammatory response via activation of NF-kappaB in acute experimental diabetic neuropathy subjected to ischemia-reperfusion injury. J Neurol Sci 2006, 247(1):47-52. 10.1016/j.jns.2006.03.011, 16631800.