Beneficial effect of heme oxygenase-1 expression on myocardial ischemia-reperfusion involves an increase in adiponectin in mildly diabetic rats

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 6, 2007, Pages

  L'Abbate, Antonio ^a,c   Neglia, Danilo ^a   Vecoli, Cecilia ^a   Novelli, Michela ^a   Ottaviano, Virginia ^a   Baldi, Simona ^a   Barsacchi, Renata ^a   Paolicchi, Aldo ^a   Masiello, Pellegrino ^a   Drummond, George S ^b   McClung, John A ^b   Abraham, Nader G ^b  

^a UNIVERSITY OF PISA   (Italy)

^b NEW YORK MEDICAL COLLEGE   (United States)

^c INSTITUTE OF CLINICAL PHYSIOLOGY   (Italy)

Author keywords

Antiapoptotic signaling protein; Phosphoactivator protein kinase; Superoxide anion

Indexed keywords

ADIPONECTIN; COBALT; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTIC ACID; MALONALDEHYDE; NICOTINAMIDE; OXYGEN; PROTOPORPHYRIN; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LEUKEMIA; B CELL LYMPHOMA; CONTROLLED STUDY; CORONARY VASCULAR RESISTANCE; ENZYME ACTIVITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; MALE; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES; VASOCONSTRICTION; WISTAR RAT;

ADIPONECTIN; ANIMALS; BCL-X PROTEIN; CARDIOVASCULAR AGENTS; CORONARY VESSELS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; ENZYME INDUCTION; HEME OXYGENASE (DECYCLIZING); LACTIC ACID; MALE; MALONDIALDEHYDE; MICROCIRCULATION; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NIACINAMIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTOPORPHYRINS; RATS; RATS, WISTAR; SEVERITY OF ILLNESS INDEX; STREPTOZOCIN; SUPEROXIDES; TIME FACTORS; UP-REGULATION; VASCULAR RESISTANCE; VASOCONSTRICTION;

EID: 36849047950     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00826.2007     Document Type: Article

References (64)

1. Abraham NG, Kappas A. Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med 39: 1-25, 2005.
2. Abraham NG, Kushida T, McClung J, Weiss M, Quan S, Lafaro R, Darzynkiewicz Z, Wolin M. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ Res 93: 507-514, 2003.
3. Abraham NG, Pinto A, Levere RD, Mullane K. Identification of heme oxygenase and cytochrome P-450 in the rabbit heart. J Mol Cell Cardiol 19: 73-81, 1987.
4. Bahia L, Aguiar LG, Villela N, Bottino D, Godoy-Matos AF, Geloneze B, Tambascia M, Bouskela E. Adiponectin is associated with improvement of endothelial function after rosiglitazone treatment in non-diabetic individuals with metabolic syndrome. Atherosclerosis [epub ahead of print]: 2006.
5. Botros FT, Laniado-Schwartzman M, Abraham NG. Regulation of cyclooxygenase- and cytochrome p450-derived eicosanoids by heme oxygenase in the rat kidney. Hypertension 39: 639-644, 2002.
6. Broedl UC, Lehrke M, Fleischer-Brielmaier E, Tietz AB, Nagel JM, Goke B, Lohse P, Parhofer KG. Genetic variants of adiponectin receptor 2 are associated with increased adiponectin levels and decreased triglyceride/VLDL levels in patients with metabolic syndrome. Cardiovasc Diabetol 5: 11, 2006.
7. Brunner EJ, Davey Smith G, Marmot MG, Canner R, Beksinska M, O'Brien J. Childhood social circumstances and psychosocial and behavioural factors as determinants of plasma fibrinogen. Lancet 347: 1008-1013, 1996.
8. Cannon WB. Organization for physiological homeostasis. Physiol Rev 9: 399-431, 1929.
9. Chi TC, Chen WP, Chi TL, Kuo TF, Lee SS, Cheng JT, Su MJ. Phosphatidylinositol-3-kinase is involved in the antihyperglycemic effect induced by resveratrol in streptozotocin-induced diabetic rats. Life Sci 80: 1713-1720, 2007.
10. Clark JE, Foresti R, Sarathchandra P, Kaur H, Green CJ, Motterlini R. Heme oxygenase-1-derived bilirubin ameliorates postischemic myocardial dysfunction. Am J Physiol Heart Circ Physiol 278: H643-H651, 2000.
11. Clark JE, Naughton P, Shurey S, Green CJ, Johnson TR, Mann BE, Foresti R, Motterlini R. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res 93: e2-e8, 2003.
12. Di FC, Cuzzocrea S, Marfella R, Fabbroni V, Scollo G, Berrino L, Giugliano D, Rossi F, D'Amico M. M40403 prevents myocardial injury induced by acute hyperglycaemia in perfused rat heart. Eur J Pharmacol 497: 65-74, 2004.
13. Di PM, Rodella L, Sacerdoti D, Bolognesi M, Turkseven S, Abraham NG. Chronic CO levels has a beneficial effect on vascular relaxation in diabetes. Biochem Biophys Res Commun 340: 935-943, 2006.
14. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101: 660-667, 2000.
15. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 274: 16349-16354, 1999.
16. Guo Y, Stein AB, Wu WJ, Tan W, Zhu X, Li QH, Dawn B, Motterlini R, Bolli R. Administration of a CO-releasing molecule at the time of reperfusion reduces infarct size in vivo. Am J Physiol Heart Circ Physiol 286: H1649-H1653, 2004.
17. Gutmann I, Wahlefed ALLactate. Determination with lactate dehydrogenase and NAD. In: Methods of Enzymatic Analysis, edited by Bergmeyer H. New York, London: Academic Press, 1974, p. 1465.
18. Hill-Kapturczak N, Chang SH, Agarwal A. Heme oxygenase and the kidney. DNA Cell Biol 21: 307-321, 2002.
19. Hopkins TA, Ouchi N, Shibata R, Walsh K. Adiponectin actions in the cardiovascular system. Cardiovasc Res 74: 11-18, 2007.
20. Jung TW, Lee JY, Shim WS, Kang ES, Kim JS, Ahn CW, Lee HC, Cha BS. Adiponectin protects human neuroblastoma SH-SY5Y cells against acetaldehyde-induced cytotoxicity. Biochem Pharmacol 72: 616-623, 2006.
21. Kong D, Melo LG, Mangi AA, Zhang L, Lopez-Ilasaca M, Perrella MA, Liew CC, Pratt RE, Dzau VJ. Enhanced inhibition of neointimal hyperplasia by genetically engineered endothelial progenitor cells. Circulation 109: 1769-1775, 2004.
22. Kossenjans W, Eis A, Sahay R, Brockman D, Myatt L. Role of peroxynitrite in altered fetal-placental vascular reactivity in diabetes or preeclampsia. Am J Phyisiol Heart Circ Physiol 278: H1311-H1319, 2000.
23. Kovacic S, Soltys CL, Barr AJ, Shiojima I, Walsh K, Dyck JR. Akt activity negatively regulates phosphorylation of AMP-activated protein kinase in the heart. J Biol Chem 278: 39422-39427, 2003.
24. Kruger AL, Peterson S, Turkseven S, Kaminski PM, Zhang FF, Quan S, Wolin MS, Abraham NG. D-4F induces heme oxygenase-1 and extracellular superoxide dismutase, decreases endothelial cell sloughing and improves vascular reactivity in rat model of diabetes. Circulation 23: 3126-3134, 2005.
25. Kumada M, Kihara S, Ouchi N, Kobayashi H, Okamoto Y, Ohashi K, Maeda K, Nagaretani H, Kishida K, Maeda N, Nagasawa A, Funahashi T, Matsuzawa Y. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation 109: 2046-2049, 2004.
26. Kusmic C, Lazzerini G, Coceani F, Barsacchi R, L'Abbate A, Sambuceti G. Paradoxical coronary microcirculatory constriction during ischemia: a synergic function for nitric oxide and endothelin. Am J Physiol Heart Circ Physiol 291: H1814-H1821, 2006.
27. Li Volti G, Sacerdoti D, Sangras B, Vanella A, Mezentsev A, Scapagnini G, Falck JR, Abraham NG. Carbon monoxide signaling in promoting angiogenesis in human microvessel endothelial cells. Antioxid Redox Signal 7: 704-710, 2005.
28. Masiello P. Animal models of type 2 diabetes with reduced pancreatic beta-cell mass. Int J Biochem Cell Biol 38: 873-893, 2006.
29. Masiello P, Broca C, Gross R, Roye M, Manteghetti M, Hillaire-Buys D, Novelli M, Ribes G. Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 47: 224-229, 1998.
30. Matsui T, Tao J, del MF, Lee KH, Li L, Picard M, Force TL, Franke TF, Hajjar RJ, Rosenzweig A. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation 104: 330-335, 2001.
31. Mehta JL, Rasouli N, Sinha AK, Molavi B. Oxidative stress in diabetes: a mechanistic overview of its effects on atherogenesis and myocardial dysfunction. Int J Biochem Cell Biol 38: 794-803, 2006.
32. Menzaghi C, Trischitta V, Doria A. Genetic influences of adiponectin on insulin resistance, type 2 diabetes, and cardiovascular disease. Diabetes 56: 1198-1209, 2007.
33. Milstien S, Katusic Z. Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function. Biochem Biophys Res Commun 263: 681-684, 1999.
34. Morales-Ruiz M, Fulton D, Sowa G, Languino LR, Fujio Y, Walsh K, Sessa WC. Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ Res 86: 892-896, 2000.
35. Moreira TJ, Cebere A, Cebers G, Ostenson CG, Efendic S, Liljequist S. Reduced HO-1 protein expression is associated with more severe neurodegeneration after transient ischemia induced by cortical compression in diabetic Goto-Kakizaki rats. J Cereb Blood Flow Metab 27: 1710-1723, 2007.
36. Nair V, Cooper CS, Vietti DE, Turner GA. The chemistry of lipid peroxidation metabolites: crosslinking reactions of malondialdehyde. Lipids 21: 6-10, 1986.
37. Nath KA, Haggard JJ, Croatt AJ, Grande JP, Poss KD, Alam J. The indispensability of heme oxygenase-1 in protecting against acute heme protein-induced toxicity in vivo. Am J Pathol 156: 1527-1535, 2000.
38. Neil TK, Abraham NG, Levere RD, Kappas A. Differential heme oxygenase induction by stannous and stannic ions in the heart. J Cell Biochem 57: 409-414, 1995.
39. Nishikawa Y, Stepp DW, Merkus D, Jones D, Chilian WM. In vivo role of heme oxygenase in ischemic coronary vasodilation. Am J Phyisiol Heart Circ Physiol 286: H2296-H2304, 2004.
40. Norhammar A, Tenerz A, Nilsson G, Hamsten A, Efendic S, Ryden L, Malmberg K. Glucose metabolism in patients with acute myocardial infarction and no previous diagnosis of diabetes mellitus: a prospective study. Lancet 359: 2140-2144, 2002.
41. Ohashi K, Kihara S, Ouchi N, Kumada M, Fujita K, Hiuge A, Hibuse T, Ryo M, Nishizawa H, Maeda N, Maeda K, Shibata R, Walsh K, Funahashi T, Shimomura I. Adiponectin replenishment ameliorates obesity-related hypertension. Hypertension 47: 1108-1116, 2006.
42. Ouchi N, Kihara S, Arita Y, Maeda K, Kuriyama H, Okamoto Y, Hotta K, Nishida M, Takahashi M, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation 100: 2473-2476, 1999.
43. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, Walsh K. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 279: 1304-1309, 2004.
44. Prior JO, Quinones MJ, Hernandez-Pampaloni M, Facta AD, Schindler TH, Sayre JW, Hsueh WA, Schelbert HR. Coronary circulatory dysfunction in insulin resistance, impaired glucose tolerance, and type 2 diabetes mellitus. Circulation 111: 2291-2298, 2005.
45. Quinones MJ, Hernandez-Pampaloni M, Schelbert H, Bulnes-Enriquez I, Jimenez X, Hernandez G, De La RR, Chon Y, Yang H, Nicholas SB, Modilevsky T, Yu K, Van HK, Castellani LW, Elashoff R, Hsueh WA. Coronary vasomotor abnormalities in insulin-resistant individuals. Ann Intern Med 140: 700-708, 2004.
46. Rodella L, Lamon BD, Rezzani R, Sangras B, Goodman AI, Falck JR, Abraham NG. Carbon monoxide and biliverdin prevent endothelial cell sloughing in rats with type I diabetes. Free Radic Biol Med 40: 2198-2205, 2006.
47. Rossig L, Jadidi AS, Urbich C, Badorff C, Zeiher AM, Dimmeler S. Akt-dependent phosphorylation of p21(Cip1) regulates PCNA binding and proliferation of endothelial cells. Mol Cell Biol 21: 5644-5657, 2001.
48. Sambuceti G, Marzilli M, Mari A, Marini C, Schluter M, Testa R, Papini M, Marraccini P, Ciriello G, Marzullo P, L'Abbate A. Coronary microcirculatory vasoconstriction is heterogeneously distributed in acutely ischemic myocardium. Am J Physiol Heart Circ Physiol 288: H2298-H2305, 2005.
49. Sano K, Nakamura H, Matsuo T. Mode of inhibitory action of bilirubin on protein kinase C. Pediatr Res 19: 587-590, 1985.
50. Secchiero P, Gonelli A, Carnevale E, Milani D, Pandolfi A, Zella D, Zauli G. TRAIL promotes the survival and proliferation of primary human vascular endothelial cells by activating the Akt and ERK pathways. Circulation 107: 2250-2256, 2003.
51. Stocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 235: 1043-1046, 1987.
52. Tamura T, Furukawa Y, Taniguchi R, Sato Y, Ono K, Horiuchi H, Nakagawa Y, Kita T, Kimura T. Serum adiponectin level as an independent predictor of mortality in patients with congestive heart failure. Circ J 71: 623-630, 2007.
53. Turkseven S, Kruger A, Mingone CJ, Kaminski P, Inaba M, Rodella L, Ikehara S, Wolin MS, Abraham NG. 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, 2005.
54. Vasa M, Fichtlscherer S, Aicher A, Adler K, Urbich C, Martin H, Zeiher AM, Dimmeler S. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res 89: E1-E7, 2001.
55. Vulapalli SR, Chen Z, Chua BH, Wang T, Liang CS. Cardioselective overexpression of HO-1 prevents I/R-induced cardiac dysfunction and apoptosis. Am J Physiol Heart Circ Physiol 283: H688-H694, 2002.
56. Wang Q, Bilan PJ, Klip A. Opposite effects of insulin on focal adhesion proteins in 3T3-L1 adipocytes and in cells overexpressing the insulin receptor. Mol Biol Cell 9: 3057-3069, 1998.
57. Wellen KE, Hotamisligil GS. Inflammation stress, and diabetes. J Clin Invest 115: 1111-1119, 2005.
58. Wever RM, Luscher TF, Cosentino F, Rabelink TJ. Atherosclerosis and the two faces of endothelial nitric oxide synthase. Circulation 97: 108-112, 1998.
59. Wiesel P, Patel AP, DiFonzo N, Marria PB, Sim CU, Pellacani A, Maemura K, LeBlanc BW, Marino K, Doerschuk CM, Yet SF, Lee ME, Perrella MA. Endotoxin-induced mortality is related to increased oxidative stress and end-organ dysfunction, not refractory hypotension, in heme oxygenase-1-deficient mice. Circulation 102: 3015-3022, 2000.
60. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 1047-1053, 2004.
61. Yet SF, Perrella MA, Layne MD, Hsieh CM, Maemura K, Kobzik L, Wiesel P, Christou H, Kourembanas S, Lee ME. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J Clin Invest 103: R23-R29, 1999.
62. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, Ith B, Melo LG, Zhang L, Ingwall JS, Dzau VJ, Lee ME, Perrella MA. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res 89: 168-173, 2001.
63. Yilmaz MI, Sonmez A, Caglar K, Celik T, Yenicesu M, Eyileten T, Acikel C, Oguz Y, Yavuz I, Vural A. Effect of antihypertensive agents on plasma adiponectin levels in hypertensive patients with metabolic syndrome. Nephrology (Carlton ) 12: 147-153, 2007.
64. Zhang F, Cheng J, Hackett NR, Lam G, Shido K, Pergolizzi R, Jin DK, Crystal RG, Rafii S. Adenovirus E4 gene promotes selective endothelial cell survival and angiogenesis via activation of the vascular endothelial-cadherin/ Akt signaling pathway. J Biol Chem 279: 11760-11766, 2004.