Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulin-resistant diabetes in Goto-Kakizaki rats

Endocrinology

Volumn 150, Issue 6, 2009, Pages 2627-2636

  Ndisang, Joseph Fomusi ^a   Jadhav, Ashok ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE; ADIPONECTIN; ANTIDIABETIC AGENT; CATALASE; CHROMIUM; CHROMIUM MESOPORPHYRIN; CYCLIC AMP; CYCLIC GMP; GLUCOSE; GLUCOSE TRANSPORTER 4; HEME OXYGENASE; HEME OXYGENASE INHIBITOR; HEMIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; MESOPORPHYRIN; PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DIABETES MELLITUS; GASTROCNEMIUS MUSCLE; GLUCOSE TOLERANCE; GOTO KAKIZAKI RAT; HYPERGLYCEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ADIPONECTIN; ANIMALS; CYCLIC AMP; CYCLIC GMP; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GLUCOSE; GLUCOSE TRANSPORTER TYPE 4; HEME OXYGENASE-1; HEMIN; INSULIN; INSULIN RESISTANCE; MALE; MESOPORPHYRINS; MUSCLE, SKELETAL; NF-KAPPA B; PROTEIN KINASES; RATS; RATS, INBRED STRAINS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; TRANSCRIPTION FACTOR AP-1; UP-REGULATION;

EID: 66649132533     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1370     Document Type: Article

References (51)

1. Devangelio E, Santilli F, Formoso G, Ferroni P, Bucciarelli L, Michetti N, Clissa C, Ciabattoni G, Consoli A, Davì G 2007 Soluble RAGE in type 2 diabetes: association with oxidative stress. Free Radic Biol Med 43:511-518 (Pubitemid 47058227)
2. Rendell MS, Jovanovic L 2006 Targeting postprandial hyperglycemia. Metabolism 55:1263-1281 (Pubitemid 44215947)
3. Song P, Wu Y, Xu J, Xie Z, Dong Y, Zhang M, Zou MH 2007 Reactive nitrogen species induced by hyperglycemia suppresses Akt signaling and triggers apoptosis by upregulating phosphatase PTEN (phosphatase and tensin homologue deleted on chromosome 10) in an LKB1-dependent manner. Circulation 116:1585-1595 (Pubitemid 47511422)
4. Haluzik M 2005 Adiponectin and its potential in the treatment of obesity, diabetes and insulin resistance. Curr Opin Investig Drugs 6:988-993 (Pubitemid 41535782)
5. Kubota N, Terauchi Y, Yamauchi T, Kubota T, Moroi M, Matsui J, Eto K, Yamashita T, Kamon J, Satoh H, Yano W, Froguel P, Nagai R, Kimura S, Kadowaki T, Noda T 2002 Disruption of adiponectin causes insulin resistance and neointimal formation. J Biol Chem 277:25863-25866 (Pubitemid 34967064)
6. Tang C, Han P, Oprescu AI, Lee SC, Gyulkhandanyan AV, Chan GN, Wheeler MB, Giacca A 2007 Evidence for a role of superoxide generation in glucose-induced β-cell dysfunction in vivo. Diabetes 56:2722-2731 (Pubitemid 350044915)
7. Lundquist I, Alm P, Salehi A, Henningsson R, Grapengiesser E, Hellman B 2003 Carbon monoxide stimulates insulin release and propagates Ca2+ signals between pancreatic β-cells. Am J Physiol Endocrinol Metab 285:E1055-E1063 (Pubitemid 37296327)
8. Henriksen EJ, Dokken BB 2006 Role of glycogen synthase kinase-3 in insulin resistance and type 2 diabetes. Curr Drug Targets 7:1435-1441 (Pubitemid 44718303)
9. Guo Z, Xia Z, Yuen VG, McNeill JH 2007 Cardiac expression of adiponectin and its receptors in streptozotocin-induced diabetic rats. Metabolism 56:1363-1371 (Pubitemid 47404598)
10. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T 2002 Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8:1288-1295 (Pubitemid 35373562)
11. Holmes BF, Sparling DP, Olson AL, Winder WW, Dohm GL 2005 Regulation of muscle GLUT4 enhancer factor and myocyte enhancer factor 2 by AMP-activated protein kinase. Am J Physiol Endocrinol Metab 289:E1071-E1076 (Pubitemid 43671058)
12. Ouchi N, Kihara S, Arita Y, Okamoto Y, Maeda K, Kuriyama H, Hotta K, Nishida M, Takahashi M, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y 2000 Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-κB signaling through a cAMP-dependent pathway. Circulation 102:1296-1301
13. Chang L, Karin M 2001 Mammalian MAP kinase signalling cascades. Nature 410:37-40 (Pubitemid 32225829)
14. Kaneto H, Nakatani Y, Kawamori D, Miyatsuka T, Matsuoka TA, Matsuhisa M, Yamasaki Y 2006 Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic β-cell dysfunction and insulin resistance. Int J Biochem Cell Biol 38:782-793 (Pubitemid 43363411)
15. Bennett BL, Satoh Y, Lewis AJ 2003 JNK: a new therapeutic target for diabetes. Curr Opin Pharmacol 3:420-425 (Pubitemid 36908946)
16. Kamigaki M, Sakaue S, Tsujino I, Ohira H, Ikeda D, Itoh N, Ishimaru S, Ohtsuka Y, 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)
17. Soares AF, Guichardant M, Cozzone D, Bernoud-Hubac N, Bouzaïdi-Tiali N, Lagarde M, Géloën A 2005 Effects of oxidative stress on adiponectin secretion and lactate production in 3T3-L1 adipocytes. Free Radic Biol Med 38:882-889 (Pubitemid 40321080)
18. Mosén H, Salehi A, Alm P, Henningsson R, Jimenez-Feltström J, Ostenson CG, Efendic S, Lundquist I 2005 Defective glucose-stimulated insulin release in the diabetic Goto-Kakizaki (GK) rat coincides with reduced activity of the islet carbon monoxide signaling pathway. Endocrinology 146:1553-1558 (Pubitemid 40289346)
19. Bruce CR, Carey AL, Hawley JA, Febbraio MA 2003 Intramuscular heat shock protein 72 and heme oxygenase-1 mRNA are reduced in patients with type 2 diabetes: evidence that insulin resistance is associated with a disturbed antioxidant defense mechanism. Diabetes 52:2338-2345 (Pubitemid 37059505)
20. Li M, Kim DH, Tsenovoy PL, Peterson SJ, Rezzani R, Rodella LF, Aronow WS, Ikehara S, 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
21. Ndisang JF, Tabien HE, Wang R 2004 Carbon monoxide and hypertension. J Hypertens 22:1057-1074 (Pubitemid 38720993)
22. Mosén H, Salehi A, Henningsson R, Lundquist I 2006 Nitric oxide inhibits, and carbon monoxide activates, islet acid α-glucoside hydrolase activities in parallel with glucose-stimulated insulin secretion. J Endocrinol 190:681-693 (Pubitemid 44560243)
23. Lira VA, Soltow QA, Long JH, Betters JL, Sellman JE, Criswell DS 2007 Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am J Physiol Endocrinol Metab 293:E1062-E1068 (Pubitemid 47535838)
24. Zisman A, Peroni OD, Abel ED, Michael MD, Mauvais-Jarvis F, Lowell BB, Wojtaszewski JF, Hirshman MF, Virkamaki A, Goodyear LJ, Kahn CR, Kahn BB 2000 Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat Med 6:924-928 (Pubitemid 30644753)
25. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN 1987 Bilirubin is an antioxidant of possible physiological importance. Science 235:1043-1046 (Pubitemid 17049750)
26. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG 1994 Identification of binding sites for transcription factors NF-κB and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 91:5987-5991 (Pubitemid 24188267)
27. Henningsson R, Alm P, Ekström P, Lundquist I 1999 Heme oxygenase and carbon monoxide: regulatory roles in islet hormone release: a biochemical, immunohistochemical, and confocal microscopic study. Diabetes 48:66-76 (Pubitemid 29019354)
28. Sasaki T, Takahashi T, Maeshima K, Shimizu H, Toda Y, Morimatsu H, Takeuchi M, Yokoyama M, Akagi R, Morita K 2006 Heme arginate pretreatment attenuates pulmonary NF-κB and AP-1 activation induced by hemorrhagic shock via heme oxygenase-1 induction. Med Chem 2:271-274 (Pubitemid 44083145)
29. Piantadosi CA, Carraway MS, Babiker A, Suliman HB 2008 Heme oxygenase- 1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 103:1232-1240
30. Goodyear LJ, Hirshman MF, Valyou PM, Horton ES 1992 Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training. Diabetes 41:1091-1099
31. Song MK, Hwang IK, Rosenthal MJ, Harris DM, Yamaguchi DT, Yip I, Go VL 2003 Anti-hyperglycemic activity of zinc plus cyclo (his-pro) in genetically diabetic Goto-Kakizaki and aged rats. Exp Biol Med (Maywood) 228:1338-1345 (Pubitemid 37549238)
32. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M, Rodella LF, Ikehara S, Wolin MS, Abraham NG 2005 Antioxidant mechanism of heme oxygenase-1 involves an increase in superoxide dismutase and catalase in experimental diabetes. Am J Physiol Heart Circ Physiol 289:H701-H707 (Pubitemid 41129386)
33. Vreman HJ, Ekstrand BC, Stevenson DK 1993 Selection of metalloporphyrin heme oxygenase inhibitors based on potency and photoreactivity. Pediatr Res 33:195-200 (Pubitemid 23095754)
34. Ndisang JF, Lane N, Jadhav A 2008 Crosstalk between the heme oxygenase system, aldosterone, and phospholipase C in hypertension. J Hypertens 26:1188-1199
35. Ndisang JF, Zhao W, Wang R 2002 Selective regulation of blood pressure by heme oxygenase-1 in hypertension. Hypertension 40:315-321
36. Ndisang JF, Wu L, Zhao W, Wang R 2003 Induction of heme oxygenase-1 and stimulation of cGMP production by hemin in aortic tissues from hypertensive rats. Blood 101:3893-3900 (Pubitemid 36857864)
37. Delanty N, Reilly MP, Pratico D, Lawson JA, McCarthy JF, Wood AE, Ohnishi ST, Fitzgerald DJ, FitzGerald GA 1997 8-epi PGF2 α generation during coronary reperfusion. A potential quantitative marker of oxidant stress in vivo. Circulation 95:2492-2499 (Pubitemid 27233114)
38. Lastra G, Whaley-Connell A, Manrique C, Habibi J, Gutweiler AA, Appesh L, Hayden MR, Wei Y, Ferrario CM, Sowers JR 2008 Low-dose spironolactone reduces reactive oxygen species generation and improves insulin stimulated glucose transport in skeletal muscle in the TG(mRen2)27 rat. Am J Physiol Endocrinol Metab 295:E110-E116
39. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC 1985 Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412-419 (Pubitemid 15018832)
40. Atalay M, Oksala NK, Laaksonen DE, Khanna S, Nakao C, Lappalainen J, Roy S, Hanninen O, Sen CK 2004 Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol 97:605-611 (Pubitemid 38963131)
41. Desrois M, Sidell RJ, Gauguier D, King LM, Radda GK, Clarke K 2004 Initial steps of insulin signaling and glucose transport are defective in the type 2 diabetic rat heart. Cardiovasc Res 61:288-296 (Pubitemid 38091769)
42. Wei Y, Sowers JR, Clark SE, Li W, Ferrario CM, Stump CS 2008 Angiotensin II-induced skeletal muscle insulin resistance mediated by NF-κB activation via NADPH oxidase. Am J Physiol Endocrinol Metab 294:E345-E351
43. Jin UH, Kang YJ, Chang YC, Kim CH 2008 Secretion of atherogenic risk factor apolipoprotein B-100 is increased by a potential mechanism of JNK/PKC-mediated insulin resistance in liver cells. J Cell Biochem 103:908-919
44. de la Rosa LC, Vrenken TE, Hannivoort RA, Buist-Homana M, Havinga R, Slebos DJ, Kauffman HF, Faber KN, Jansen PL, Moshage H 2007 Carbon monoxide blocks oxidative stress-induced hepatocyte apoptosis via inhibition of the p54 JNK isoform. Free Radic Biol Med 44:1323-1333
45. L'Abbate A, Neglia D, Vecoli C, Novelli M, Ottaviano V, Baldi S, Barsacchi R, Paolicchi A, Masiello P, Drummond GS, McClung JA, Abraham NG 2007 Beneficial effect of heme oxygenase-1 expression on myocardial ischemia-reperfusion involves an increase in adiponectin in mildly diabetic rats. Am J Physiol Heart Circ Physiol 293:H3532-H3541 (Pubitemid 350230897)
46. Kim DH, Burgess AP, Li M, Tsenovoy PL, Addabbo F, McClung JA, Puri N, Abraham NG 2008 Heme oxygenase-mediated increases in adiponectin decrease fat content and inflammatory cytokines tumor necrosis factor-α and interleukin-6 in Zucker rats and reduce adipogenesis in human mesenchymal stem cells. J Pharmacol Exp Ther 325:833-840
47. Piantadosi CA 2002 Biological chemistry of carbon monoxide. Antioxid Redox Signal 4:259-270 (Pubitemid 34517177)
48. Kiemer AK, Vollmar AM, Bilzer M, Gerwig T, Gerbes AL 2000 Atrial natriuretic peptide reduces expression of TNF-α mRNA during reperfusion of the rat liver upon decreased activation of NF-κB and AP-1. J Hepatol 33:236-246 (Pubitemid 30485227)
49. Liu Y, Nakagawa Y, Wang Y, Liu L, Du H, Wang W, Ren X, Lutfy K, Friedman TC 2008 Reduction of hepatic glucocorticoid receptor and hexose-6-phosphate dehydrogenase expression ameliorates diet-induced obesity and insulin resistance in mice. J Mol Endocrinol 41:53-64
50. Keyse SM, Tyrrell RM 1989 Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci USA 86:99-103 (Pubitemid 19036341)
51. Jonas JC, Guiot Y, Rahier J, Henquin JC 2003 Haeme-oxygenase 1 expression in rat pancreatic β cells is stimulated by supraphysiological glucose concentrations and by cyclic AMP. Diabetologia 46:1234-1244 (Pubitemid 37214981)