Hemin therapy suppresses inflammation and retroperitoneal adipocyte hypertrophy to improve glucose metabolism in obese rats co-morbid with insulin-resistant type-2 diabetes

Diabetes, Obesity and Metabolism

Volumn 15, Issue 11, 2013, Pages 1029-1039

  Ndisang, J F ^a   Jadhav, A ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Adiponectin; Heme oxygenase; Inflammatory cytokines; Visceral adiposity

Indexed keywords

ADIPONECTIN; CYCLIC GMP; CYTOKINE; GLUCOSE; GLUCOSE TRANSPORTER 4; HEME OXYGENASE; HEME OXYGENASE 1; HEMIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPID; LIPOPROTEIN LIPASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN; PROTEIN KINASE B; STANNSOPORFIN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ADIPOCYTE HYPERTROPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COMORBIDITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLUCOSE METABOLISM; HISTOPATHOLOGY; HYPERGLYCEMIA; HYPERTROPHY; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; MALE; MEDIATOR; MORPHOMETRICS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROTEIN EXPRESSION; RAT; RETROPERITONEUM; SIGNAL TRANSDUCTION; SPECTROPHOTOMETRY; WESTERN BLOTTING; ZUCKER DIABETIC FATTY RAT;

ADIPONECTIN; HEME OXYGENASE; INFLAMMATORY CYTOKINES; VISCERAL ADIPOSITY;

ADIPONECTIN; ADIPOSITY; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; DIABETES MELLITUS, TYPE 2; ENZYME INDUCTION; HEME OXYGENASE-1; HEMIN; HYPERGLYCEMIA; HYPERTROPHY; HYPOGLYCEMIC AGENTS; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LIPID METABOLISM; MALE; METALLOPORPHYRINS; OBESITY; RANDOM ALLOCATION; RATS; RATS, ZUCKER; SIGNAL TRANSDUCTION;

EID: 84885324545     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12130     Document Type: Article

References (40)

1. Ndisang JF. Role of heme oxygenase in inflammation, insulin-signalling, diabetes and obesity. Mediators Inflamm 2010; 2010: 359732.
2. Gustafson B. Adipose tissue, inflammation and atherosclerosis. J Atheroscler Thromb 2010; 17: 332-341.
3. Cnop M, Welsh N, Jonas JC, Jorns A, Lenzen S, Eizirik DL. Mechanisms of pancreatic beta-cell death in type 1 and type 2 diabetes: many differences, few similarities. Diabetes 2005; 54(Suppl 2): S97-107.
4. Donath MY, Schumann DM, Faulenbach M, Ellingsgaard H, Perren A, Ehses JA. Islet inflammation in type 2 diabetes: from metabolic stress to therapy. Diabetes Care 2008; 31(Suppl 2): S161-164.
5. Yang J, Eliasson B, Smith U, Cushman SW, Sherman AS. The size of large adipose cells is a predictor of insulin resistance in first-degree relatives of type 2 diabetic patients. Obesity (Silver Spring) 2012; 20: 932-938.
6. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91.
7. Bluher M. Adipose tissue dysfunction in obesity. Exp Clin Endocrinol Diabetes 2009; 117: 241-250.
8. Hamdy O, Porramatikul S, Al-Ozairi E. Metabolic obesity: the paradox between visceral and subcutaneous fat. Curr Diabetes Rev 2006; 2: 367-373.
9. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860-867.
10. Ndisang JF, Lane N, Jadhav A. The heme oxygenase system abates hyperglycemia in Zucker diabetic fatty rats by potentiating insulin-sensitizing pathways. Endocrinology 2009; 150: 2098-2108.
11. Mosen H, Salehi A, Alm P et al. Defective glucose-stimulated insulin release in the diabetic Goto-Kakizaki (GK) rat coincides with reduced activity of the islet carbon monoxide signaling pathway. Endocrinology 2005; 146: 1553-1558.
12. Mosen H, Salehi A, Henningsson R, Lundquist I. Nitric oxide inhibits, and carbon monoxide activates, islet acid alpha-glucoside hydrolase activities in parallel with glucose-stimulated insulin secretion. J Endocrinol 2006; 190: 681-693.
13. Ndisang JF, Jadhav A. Heme oxygenase system enhances insulin sensitivity and glucose metabolism in streptozotocin-induced diabetes. Am J Physiol Endocrinol Metab 2009; 296: E829-841.
14. Ndisang JF, Lane N, Jadhav A. Upregulation of the heme oxygenase system ameliorates postprandial and fasting hyperglycemia in type 2 diabetes. Am J Physiol Endocrinol Metab 2009; 296: E1029-1041.
15. Ndisang JF, Lane N, Syed N, Jadhav A. Up-regulating the heme oxygenase system with hemin improves insulin sensitivity and glucose metabolism in adult spontaneously hypertensive rats. Endocrinology 2010; 151: 549-560.
16. Reed DR, Duke FF, Ellis HK et al. Body fat distribution and organ weights of 14 common strains and a 22-strain consomic panel of rats. Physiol Behav 2011; 103: 523-529.
17. Lee HJ, Choi SS, Park MK et al. Fenofibrate lowers abdominal and skeletal adiposity and improves insulin sensitivity in OLETF rats. Biochem Biophys Res Commun 2002; 296: 293-299.
18. Morel OE, Aubert R, Richalet JP, Chapelot D. Simulated high altitude selectively decreases protein intake and lean mass gain in rats. Physiol Behav 2005; 86: 145-153.
19. Afonso RA, Fernandes AB, Santos C et al. Postprandial insulin resistance in Zucker diabetic fatty rats is associated with parasympathetic-nitric oxide axis deficiencies. J Neuroendocrinol 2012; 24: 1346-1355.
20. Shoelson SE, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007; 132: 2169-2180.
21. Tam CS, Viardot A, Clement K et al. Short-term overfeeding may induce peripheral insulin resistance without altering subcutaneous adipose tissue macrophages in humans. Diabetes 2010; 59: 2164-2170.
22. Murdolo G, Nowotny B, Celi F et al. Inflammatory adipokines, high molecular weight adiponectin, and insulin resistance: a population-based survey in prepubertal schoolchildren. PLoS One 2011; 6: e17264.
23. Moro C, Klimcakova E, Lolmede K et al. Atrial natriuretic peptide inhibits the production of adipokines and cytokines linked to inflammation and insulin resistance in human subcutaneous adipose tissue. Diabetologia 2007; 50: 1038-1047.
24. Kralisch S, Sommer G, Stangl V et al. Secretory products from human adipocytes impair endothelial function via nuclear factor kappaB. Atherosclerosis 2008; 196: 523-531.
25. Capurso C, Capurso A. From excess adiposity to insulin resistance: The role of free fatty acids. Vascul Pharmacol 2012; 57: 91-97.
26. Greenstein AS, Khavandi K, Withers SB et al. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 2009; 119: 1661-1670.
27. Sommer G, Kralisch S, Stangl V et al. Secretory products from human adipocytes stimulate proinflammatory cytokine secretion from human endothelial cells. J Cell Biochem 2009; 106: 729-737.
28. Burgess AP, Vanella L, Bellner L et al. Heme oxygenase (HO-1) rescue of adipocyte dysfunction in HO-2 deficient mice via recruitment of epoxyeicosatrienoic acids (EETs) and adiponectin. Cell Physiol Biochem 2012; 29: 99-110.
29. Burgess A, Li M, Vanella L et al. Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice. Hypertension 2010; 56: 1124-1130.
30. Yamauchi T, Kamon J, Minokoshi Y et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 2002; 8: 1288-1295.
31. Liu F, Dallas-Yang Q, Castriota G et al. Development of a novel GLUT4 translocation assay for identifying potential novel therapeutic targets for insulin sensitization. Biochem J 2009; 418: 413-420.
32. Weinstock PH, Levak-Frank S, Hudgins LC et al. Lipoprotein lipase controls fatty acid entry into adipose tissue, but fat mass is preserved by endogenous synthesis in mice deficient in adipose tissue lipoprotein lipase. Proc Natl Acad Sci U S A 1997; 94: 10261-10266.
33. Kei AA, Filippatos TD, Tsimihodimos V, Elisaf MS. A review of the role of apolipoprotein C-II in lipoprotein metabolism and cardiovascular disease. Metabolism 2012; 61: 906-921.
34. Guo Z, Xia Z, Yuen VG, McNeill JH. Cardiac expression of adiponectin and its receptors in streptozotocin-induced diabetic rats. Metabolism 2007; 56: 1363-1371.
35. Holmes BF, Sparling DP, Olson AL, Winder WW, Dohm GL. Regulation of muscle GLUT4 enhancer factor and myocyte enhancer factor 2 by AMP-activated protein kinase. Am J Physiol Endocrinol Metab 2005; 289: E1071-1076.
36. Kaneto H, Nakatani Y, Kawamori D et al. 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 2006; 38: 782-793.
37. Li Y, Tong X, Maimaitiyiming H, Clemons K, Cao JM, Wang S. Overexpression of cGMP-dependent protein kinase I (PKG-I) attenuates ischemia-reperfusion-induced kidney injury. Am J Physiol Renal Physiol 2012; 302: F561-570.
38. Fu WJ, Haynes TE, Kohli R et al. Dietary L-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 2005; 135: 714-721.
39. Henningsson R, Alm P, Ekstrom P, Lundquist I. Heme oxygenase and carbon monoxide: regulatory roles in islet hormone release: a biochemical, immunohistochemical, and confocal microscopic study. Diabetes 1999; 48: 66-76.
40. Walter BF, Emile B. Medical Physiology. 2nd edn. Philadelphia, MA: Saunders Elsevier, 2009.