The heme oxygenase system selectively enhances the anti-inflammatory macrophage-m2 phenotype, reduces pericardial adiposity, and ameliorated cardiac injury in diabetic cardiomyopathy in zucker diabetic fatty rats

Journal of Pharmacology and Experimental Therapeutics

Volumn 345, Issue 2, 2013, Pages 239-249

  Jadhav, Ashok ^a   Tiwari, Shuchita ^a   Lee, Paul ^a   Ndisang, Joseph Fomusi ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

8 ISOPROSTANE; ENDOTHELIN 1; GLUCOSE; HEME OXYGENASE; HEMIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE; MACROPHAGE INFLAMMATORY PROTEIN 2; MESOPORPHYRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; ELECTROCARDIOGRAM; ENZYME ACTIVITY; ENZYME IMMUNOASSAY; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HEART EJECTION FRACTION; HEART FUNCTION; HEART HEMODYNAMICS; HEART INJURY; HEART MUSCLE FIBER MEMBRANE; HEART VENTRICLE HYPERTROPHY; MALE; MASS SPECTROMETRY; MUSCLE THICKNESS; NONHUMAN; OBESITY; PERICARDIAL ADIPOSITY; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; VASCULAR RESISTANCE; WESTERN BLOTTING; ZUCKER DIABETIC FATTY RAT;

ADIPOSITY; ALGORITHMS; ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; CORONARY CIRCULATION; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DIABETIC CARDIOMYOPATHIES; ENDOTHELIN-1; HEME OXYGENASE (DECYCLIZING); HEMIN; INSULIN RESISTANCE; ISOPROSTANES; MACROPHAGES; MALE; MYOCYTES, CARDIAC; PHENOTYPE; RATS; RATS, ZUCKER; TRANSCRIPTION FACTOR RELA; VENTRICULAR FUNCTION, LEFT;

EID: 84876569854     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.112.200808     Document Type: Article

References (55)

1. Achouh P, Simonet S, Badier-Commander C, Chardigny C, Vayssettes-Courchay C, Zegdi R, Khabbaz Z, Fabiani JN, and Verbeuren TJ (2005) The induction of heme oxygenase 1 decreases contractility in human internal thoracic artery and radial artery grafts. J Thorac Cardiovasc Surg 130:1573-1580. (Pubitemid 41676921)
2. Alexander D (2004) A method for interdicting the development of severe jaundice in newborns by inhibiting the production of bilirubin. Pediatrics 113:135. (Pubitemid 38057510)
3. Anderson KE, Bloomer JR, Bonkovsky HL, Kushner JP, Pierach CA, Pimstone NR, and Desnick RJ (2005) Recommendations for the diagnosis and treatment of the acute porphyrias. Ann Intern Med 142:439-450. (Pubitemid 40365431)
4. Anderson KE and Collins S (2006) Open-label study of hemin for acute porphyria: Clinical practice implications. Am J Med 119:801.e19-24.
5. Awan NA, DeMaria AN, Miller RR, Amsterdam EA, and Mason DT (1981) Beneficial effects of nitroprusside administration on left ventricular dysfunction and myocardial ischemia in severe aortic stenosis. Am Heart J 101:386-394.
6. Bazan NG, Eady TN, Khoutorova L, Atkins KD, Hong S, Lu Y, Zhang C, Jun B, Obenaus A, and Fredman G, et al. (2012) Novel aspirin-triggered neuroprotectin D1 attenuates cerebral ischemic injury after experimental stroke. Exp Neurol 236: 122-130.
7. Bennett BL, Satoh Y, and Lewis AJ (2003) JNK: A new therapeutic target for diabetes. Curr Opin Pharmacol 3:420-425. (Pubitemid 36908946)
8. Boron WF and Boulpaep E (2009) Medical Physiology, Saunders Elsevier, Philadelphia, MA.
9. Burgess A, Li M, Vanella L, Kim DH, Rezzani R, Rodella L, Sodhi K, Canestraro M, Martasek P, and Peterson SJ, et al. (2010) Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice. Hypertension 56:1124-1130.
10. Conrad CH, Brooks WW, Hayes JA, Sen S, Robinson KG, and Bing OH (1995) Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation 91:161-170.
11. Delanty N, Reilly MP, Pratico D, Lawson JA, McCarthy JF, Wood AE, Ohnishi ST, Fitzgerald DJ, and FitzGerald GA (1997) 8-epi PGF2 alpha generation during coronary reperfusion. A potential quantitative marker of oxidant stress in vivo. Circulation 95:2492-2499. (Pubitemid 27233114)
12. Farret A, Filhol R, Linck N, Manteghetti M, Vignon J, Gross R, and Petit P (2006) P2Y receptor mediated modulation of insulin release by a novel generation of 2-substituted-59-O-(1-boranotriphosphate)-adenosine analogues. Pharm Res 23: 2665-2671. (Pubitemid 44691613)
13. Feinstein R, Kanety H, Papa MZ, Lunenfeld B, and Karasik A (1993) Tumor necrosis factor-alpha suppresses insulin-induced tyrosine phosphorylation of insulin receptor and its substrates. J Biol Chem 268:26055-26058.
14. Fernández-Veledo S, Vila-Bedmar R, Nieto-Vazquez I, and Lorenzo M (2009) c-Jun N-terminal kinase 1/2 activation by tumor necrosis factor-alpha induces insulin resistance in human visceral but not subcutaneous adipocytes: Reversal by liver X receptor agonists. J Clin Endocrinol Metab 94:3583-3593.
15. Fukunaga M, Yura T, and Badr KF (1995) Stimulatory effect of 8-Epi-PGF2 alpha, an F2-isoprostane, on endothelin-1 release. J Cardiovasc Pharmacol 26 (Suppl 3): S51-S52.
16. Goodman AI, Chander PN, Rezzani R, Schwartzman ML, Regan RF, Rodella L, Turkseven S, Lianos EA, Dennery PA, and Abraham NG (2006) Heme oxygenase-2 deficiency contributes to diabetes-mediated increase in superoxide anion and renal dysfunction. J Am Soc Nephrol 17:1073-1081.
17. Gordon S and Martinez FO (2010) Alternative activation of macrophages: Mechanism and functions. Immunity 32:593-604.
18. Hamdy O, Porramatikul S, and Al-Ozairi E (2006) Metabolic obesity: The paradox between visceral and subcutaneous fat. Curr Diabetes Rev 2:367-373. (Pubitemid 44734225)
19. Heidenreich PA, Zhao X, Hernandez AF, Yancy CW and Fonarow GC (2012) Patient and hospital characteristics associated with traditional measures of inpatient quality of care for patients with heart failure. Am Heart J 163:239-245. 3.
20. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444: 860-867. (Pubitemid 46024993)
21. Hotamisligil GS, Shargill NS, and Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 259:87-91. (Pubitemid 23036092)
22. Hotamisligil GS and Spiegelman BM (1994) Tumor necrosis factor alpha: A key component of the obesity-diabetes link. Diabetes 43:1271-1278.
23. Jadhav A and Ndisang JF (2009) Heme arginate suppresses cardiac lesions and hypertrophy in deoxycorticosterone acetate-salt hypertension. Exp Biol Med (Maywood) 234:764-778.
24. Jadhav A, Torlakovic E, and Ndisang JF (2008) Interaction among heme oxygenase, nuclear factor-kappaB, and transcription activating factors in cardiac hypertrophy in hypertension. Hypertension 52:910-917.
25. Kamigaki M, Sakaue S, Tsujino I, Ohira H, Ikeda D, Itoh N, Ishimaru S, Ohtsuka Y, and Nishimura M (2006) Oxidative stress provokes atherogenic changes in adipokine gene expression in 3T3-L1 adipocytes. Biochem Biophys Res Commun 339: 624-632. (Pubitemid 41739713)
26. Kaneto H, Nakatani Y, Kawamori D, Miyatsuka T, Matsuoka TA, Matsuhisa M, and Yamasaki Y (2006) Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic beta-cell dysfunction and insulin resistance. Int J Biochem Cell Biol 38:782-793. (Pubitemid 43363411)
27. Kappas A (2004) A method for interdicting the development of severe jaundice in newborns by inhibiting the production of bilirubin. Pediatrics 113: 119-123. (Pubitemid 38057504)
28. Karalis KP, Giannogonas P, Kodela E, Koutmani Y, Zoumakis M, and Teli T (2009) Mechanisms of obesity and related pathology: Linking immune responses to metabolic stress. FEBS J 276:5747-5754.
29. Li M, Kim DH, Tsenovoy PL, Peterson SJ, Rezzani R, Rodella LF, Aronow WS, Ikehara S, and Abraham NG (2008) Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes 57: 1526-1535.
30. Li Y, Takemura G, Okada H, Miyata S, Maruyama R, Li L, Higuchi M, Minatoguchi S, Fujiwara T, and Fujiwara H (2006) Reduction of inflammatory cytokine expression and oxidative damage by erythropoietin in chronic heart failure. Cardiovasc Res 71:684-694. (Pubitemid 44848006)
31. McAuley PA, Hsu FC, Loman KK, Carr JJ, Budoff MJ, Szklo M, Sharrett AR, and Ding J (2011) Liver attenuation, pericardial adipose tissue, obesity, and insulin resistance: The Multi-Ethnic Study of Atherosclerosis (MESA). Obesity (Silver Spring) 19:1855-1860.
32. Ndisang JF (2010) Role of heme oxygenase in inflammation, insulin-signalling, diabetes and obesity. Mediators Inflamm 2010:359732.
33. Ndisang JF and Jadhav A (2009a) Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulin-resistant diabetes in Goto-Kakizaki rats. Endocrinology 150:2627-2636.
34. Ndisang JF and Jadhav A (2009b) Upregulating the heme oxygenase system suppresses left ventricular hypertrophy in adult spontaneously hypertensive rats for 3 months. J Card Fail 15:616-628.
35. Ndisang JF and Jadhav A (2010) Heme arginate therapy enhanced adiponectin and atrial natriuretic peptide, but abated endothelin-1 with attenuation of kidney histopathological lesions in mineralocorticoid-induced hypertension. J Pharmacol Exp Ther 334:87-98.
36. Ndisang JF, Lane N, and Jadhav A (2008) Crosstalk between the heme oxygenase system, aldosterone, and phospholipase C in hypertension. J Hypertens 26: 1188-1199. (Pubitemid 351698808)
37. Ndisang JF, Lane N, and Jadhav A (2009) The heme oxygenase system abates hyperglycemia in Zucker diabetic fatty rats by potentiating insulin-sensitizing pathways. Endocrinology 150:2098-2108.
38. Ndisang JF, Lane N, Syed N, and Jadhav A (2010) Up-regulating the heme oxygenase system with hemin improves insulin sensitivity and glucose metabolism in adult spontaneously hypertensive rats. Endocrinology 151:549-560.
39. Permana PA, Menge C, and Reaven PD (2006) Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 341:507-514. (Pubitemid 43152134)
40. Pingitore A, Aquaro GD, Lorenzoni V, Gallotta M, De Marchi D, Molinaro S, Cospite V, Passino C, Emdin M, and Lombardi M, et al. (2011) Influence of preload and afterload on stroke volume response to low-dose dobutamine stress in patients with non-ischemic heart failure: A cardiac MR study. Int J Cardiol [Epub ahead of print].
41. Poornima IG, Parikh P, and Shannon RP (2006) Diabetic cardiomyopathy: The search for a unifying hypothesis. Circ Res 98:596-605.
42. Ram R, Mickelsen DM, Theodoropoulos C, and Blaxall BC (2011) New approaches in small animal echocardiography: Imaging the sounds of silence. Am J Physiol Heart Circ Physiol 301:H1765-H1780.
43. Rodriguez F, Langer F, Harrington KB, Cheng A, Daughters GT, Criscione JC, Ingels NB, and Miller DC (2005) Alterations in transmural strains adjacent to ischemic myocardium during acute midcircumflex occlusion. J Thorac Cardiovasc Surg 129: 791-803. (Pubitemid 40487879)
44. Rosito GA, Massaro JM, Hoffmann U, Ruberg FL, Mahabadi AA, Vasan RS, O'Donnell CJ, and Fox CS (2008) Pericardial fat, visceral abdominal fat, cardiovascular disease risk factors, and vascular calcification in a community-based sample: The Framingham Heart Study. Circulation 117:605-613.
45. Sabio G, Das M, Mora A, Zhang Z, Jun JY, Ko HJ, Barrett T, Kim JK, and Davis RJ (2008) A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322:1539-1543.
46. Sammut IA, Foresti R, Clark JE, Exon DJ, Vesely MJ, Sarathchandra P, Green CJ, and Motterlini R (1998) Carbon monoxide is a major contributor to the regulation of vascular tone in aortas expressing high levels of haeme oxygenase-1. Br J Pharmacol 125:1437-1444. (Pubitemid 28548555)
47. Scazzocchio B, Varì R, D'Archivio M, Santangelo C, Filesi C, Giovannini C, and Masella R (2009) Oxidized LDL impair adipocyte response to insulin by activating serine/threonine kinases. J Lipid Res 50:832-845.
48. Senanayake GV, Banigesh A, Wu L, Lee P, and Juurlink BH (2012) The dietary phase 2 protein inducer sulforaphane can normalize the kidney epigenome and improve blood pressure in hypertensive rats. Am J Hypertens 25: 229-235.
49. Tilg H and Moschen AR (2008) Inflammatory mechanisms in the regulation of insulin resistance. Mol Med 14:222-231. (Pubitemid 351481853)
50. Tuncman G, Hirosumi J, Solinas G, Chang L, Karin M, and Hotamisligil GS (2006) Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci USA 103:10741-10746. (Pubitemid 44078046)
51. Uysal KT, Wiesbrock SM, Marino MW, and Hotamisligil GS (1997) Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614. (Pubitemid 27446179)
52. van den Brom CE, Bosmans JW, Vlasblom R, Handoko LM, Huisman MC, Lubberink M, Molthoff CF, Lammertsma AA, Ouwens MD, and Diamant M, et al. (2010) Diabetic cardiomyopathy in Zucker diabetic fatty rats: The forgotten right ventricle. Cardiovasc Diabetol 9:25.
53. Weis N, Weigert A, von Knethen A, and Brüne B (2009) Heme oxygenase-1 contributes to an alternative macrophage activation profile induced by apoptotic cell supernatants. Mol Biol Cell 20:1280-1288.
54. Yura T, Fukunaga M, Khan R, Nassar GN, Badr KF, and Montero A (1999) Freeradical-generated F2-isoprostane stimulates cell proliferation and endothelin-1 expression on endothelial cells. Kidney Int 56:471-478. (Pubitemid 29353144)
55. Zhang X, Lam KS, Ye H, Chung SK, Zhou M, Wang Y, and Xu A (2010) Adipose tissuespecific inhibition of hypoxia-inducible factor 1alpha induces obesity and glucose intolerance by impeding energy expenditure in mice. J Biol Chem 285:32869-32877.