Preserved endothelium-dependent dilatation of the coronary microvasculature at the early phase of diabetes mellitus despite the increased oxidative stress and depressed cardiac mechanical function ex vivo

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Mourmoura, Evangelia ^a,b   Vial, Guillaume ^a,b   Laillet, Brigitte ^c   Rigaudière, Jean Paul ^c   Hininger Favier, Isabelle ^a,b   Dubouchaud, Hervé ^a,b   Morio, Beatrice ^c   Demaison, Luc ^a,b,c  

^a Domaine Universitaire   (France)

^b UNIV GRENOBLE ALPES   (France)

^c INRA and University of Auvergne   (France)

Author keywords

Coronary reactivity; Diabetes mellitus; Insulin resistance; Mechanical function; Microvasculature; Oxidative stress

Indexed keywords

ARACHIDONIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; INSULIN; OMEGA 3 FATTY ACID; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BLOOD VESSEL REACTIVITY; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CORONARY BLOOD VESSEL; DIABETES MELLITUS; EX VIVO STUDY; GLUCOSE BLOOD LEVEL; HEART CONTRACTION; HEART FAILURE; HEART FUNCTION; HEART PERFUSION; HEMOGLOBIN BLOOD LEVEL; INSULIN BLOOD LEVEL; LEAN BODY WEIGHT; LIPID COMPOSITION; MALE; MICROVASCULATURE; NONHUMAN; OXIDATIVE STRESS; RAT; TRIACYLGLYCEROL BLOOD LEVEL; VASCULAR ENDOTHELIUM; VASODILATATION; ZUCKER DIABETIC FATTY RAT;

ANIMALS; CORONARY CIRCULATION; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; HEART; MALE; MICROVESSELS; ORGAN CULTURE TECHNIQUES; OXIDATIVE STRESS; RATS; RATS, ZUCKER; TIME FACTORS; VASODILATION;

EID: 84875301896     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-49     Document Type: Article

References (70)

1. 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 2004, 27(5):1047-1053. 10.2337/diacare.27.5.1047, 15111519.
2. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS medicine 2006, 3(11):e442. 10.1371/journal.pmed.0030442, 1664601, 17132052.
3. Funaki M. Saturated fatty acids and insulin resistance. J Med Invest 2009, 56(3-4):88-92.
4. Goldstein BJ. Insulin resistance as the core defect in type 2 diabetes mellitus. Am J Cardiol 2002, 90(5A):3G-10G.
5. Sowers JR, Epstein M, Frohlich ED. Diabetes, hypertension, and cardiovascular disease: an update. Hypertension 2001, 37(4):1053-1059. 10.1161/01.HYP.37.4.1053, 11304502.
6. Chinen I, Shimabukuro M, Yamakawa K, Higa N, Matsuzaki T, Noguchi K, Ueda S, Sakanashi M, Takasu N. Vascular lipotoxicity: endothelial dysfunction via fatty-acid-induced reactive oxygen species overproduction in obese zucker diabetic fatty rats. Endocrinology 2007, 148(1):160-165.
7. Heitzer T, Schlinzig T, Krohn K, Meinertz T, Munzel T. Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation 2001, 104(22):2673-2678. 10.1161/hc4601.099485, 11723017.
8. Thuillez C, Richard V. Targeting endothelial dysfunction in hypertensive subjects. J Hum Hypertens 2005, 19(Suppl 1):S21-S25.
9. Nitenberg A, Valensi P, Sachs R, Dali M, Aptecar E, Attali JR. Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes 1993, 42(7):1017-1025. 10.2337/diabetes.42.7.1017, 8513969.
10. Clark JB, Palmer CJ, Shaw WN. The diabetic zucker fatty rat. Proceedings of the Society for Experimental Biology and Medicine Society for Experimental Biology and Medicine 1983, 173(1):68-75.
11. Wang P, Chatham JC. Onset of diabetes in zucker diabetic fatty (ZDF) rats leads to improved recovery of function after ischemia in the isolated perfused heart. Am J Physiol Endocrinol Metab 2004, 286(5):E725-E736. 10.1152/ajpendo.00295.2003, 14722022.
12. Greenberg AS, McDaniel ML. Identifying the links between obesity, insulin resistance and beta-cell function: potential role of adipocyte-derived cytokines in the pathogenesis of type 2 diabetes. Eur J Clin Investig 2002, 32(Suppl 3):24-34.
13. Bastard JP, Maachi M, Van Nhieu JT, Jardel C, Bruckert E, Grimaldi A, Robert JJ, Capeau J, Hainque B. Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro. J Clin Endocrinol Metab 2002, 87(5):2084-2089. 10.1210/jc.87.5.2084, 11994345.
14. Erdos B, Snipes JA, Miller AW, Busija DW. Cerebrovascular dysfunction in zucker obese rats is mediated by oxidative stress and protein kinase C. Diabetes 2004, 53(5):1352-1359. 10.2337/diabetes.53.5.1352, 15111506.
15. Oltman CL, Coppey LJ, Gellett JS, Davidson EP, Lund DD, Yorek MA. Progression of vascular and neural dysfunction in sciatic nerves of zucker diabetic fatty and zucker rats. Am J Physiol Endocrinol Metab 2005, 289(1):E113-E122. 10.1152/ajpendo.00594.2004, 15727946.
16. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Yorek MA. Changes in endoneurial blood flow, motor nerve conduction velocity and vascular relaxation of epineurial arterioles of the sciatic nerve in ZDF-obese diabetic rats. Diabetes Metab Res Rev 2002, 18(1):49-56. 10.1002/dmrr.257, 11921418.
17. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000, 87(10):840-844. 10.1161/01.RES.87.10.840, 11073878.
18. Pieper GM, Langenstroer P, Siebeneich W. Diabetic-induced endothelial dysfunction in rat aorta: role of hydroxyl radicals. Cardiovasc Res 1997, 34(1):145-156. 10.1016/S0008-6363(96)00237-4, 9217884.
19. Winer N, Sowers JR. Diabetes and arterial stiffening. Adv Cardiol 2007, 44:245-251.
20. Hattori Y, Kawasaki H, Abe K, Kanno M. Superoxide dismutase recovers altered endothelium-dependent relaxation in diabetic rat aorta. Am J Physiol 1991, 261(4 Pt 2):H1086-H1094.
21. Chilian WM. Coronary microcirculation in health and disease. Summary of an NHLBI workshop. Circulation 1997, 95(2):522-528. 10.1161/01.CIR.95.2.522, 9008472.
22. Oltman CL, Richou LL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Progression of coronary and mesenteric vascular dysfunction in zucker obese and zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 2006, 291(4):H1780-H1787. 10.1152/ajpheart.01297.2005, 16714356.
23. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS biology 2010, 8(6):e1000412. 10.1371/journal.pbio.1000412, 2893951, 20613859.
24. Fu WJ, Haynes TE, Kohli R, Hu J, Shi W, Spencer TE, Carroll RJ, Meininger CJ, Wu G. Dietary L-arginine supplementation reduces fat mass in zucker diabetic fatty rats. J Nutr 2005, 135(4):714-721.
25. Skrzypiec-Spring M, Grotthus B, Szelag A, Schulz R. Isolated heart perfusion according to langendorff--still viable in the new millennium. Journal of pharmacological and toxicological methods 2007, 55(2):113-126. 10.1016/j.vascn.2006.05.006, 16844390.
26. Gobel FL, Norstrom LA, Nelson RR, Jorgensen CR, Wang Y. The rate-pressure product as an index of myocardial oxygen consumption during exercise in patients with angina pectoris. Circulation 1978, 57(3):549-556. 10.1161/01.CIR.57.3.549, 624164.
27. Faure P, Lafond J. Measurement of plasma sulfhydryl and carbonyl groups as a possible indicator of protein oxidation. Analysis of free radicals in biological systems 1995, 237-248. Basel: Birkhauser, Favier A, Cadet J, Kalnyanaraman M, Fontecave M, Pierre J.
28. Gunzler WA, Kremers H, Flohe L. An improved coupled test procedure for glutathione peroxidase (EC 1-11-1-9-) in blood. Z Klin Chem Klin Biochem 1974, 12(10):444-448.
29. Bergmeyer HU, Gawehn K, Williamson DH, Lund P. Methods of enzymatic analysis 1974, Weinheim New York; London: Verlag Chemie: Academic, 2 English.
30. Nuutinen EM. Subcellular origin of the surface fluorescence of reduced nicotinamide nucleotides in the isolated perfused rat heart. Basic Res Cardiol 1984, 79(1):49-58. 10.1007/BF01935806, 6233965.
31. Goodwin GW, Taylor CS, Taegtmeyer H. Regulation of energy metabolism of the heart during acute increase in heart work. J Biol Chem 1998, 273(45):29530-29539. 10.1074/jbc.273.45.29530, 9792661.
32. Baumberger JP, Jurgensen JJ, Bardwell K. The coupled redox potential of the lactate-enzyme-pyruvate system. J Gen Physiol 1933, 16(6):961-976. 10.1085/jgp.16.6.961, 2141256, 19872753.
33. Richard MJ, Portal B, Meo J, Coudray C, Hadjian A, Favier A. Malondialdehyde kit evaluated for determining plasma and lipoprotein fractions that react with thiobarbituric acid. Clin Chem 1992, 38(5):704-709.
34. Gardner PR, Nguyen DD, White CW. Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proc Natl Acad Sci U S A 1994, 91(25):12248-12252. 10.1073/pnas.91.25.12248, 45414, 7991614.
35. Mourmoura E, Leguen M, Dubouchaud H, Couturier K, Vitiello D, Lafond JL, Richardson M, Leverve X, Demaison L. Middle age aggravates myocardial ischemia through surprising upholding of complex II activity, oxidative stress, and reduced coronary perfusion. Age 2011, 33(3):321-336. 10.1007/s11357-010-9186-0, 3168590, 20878490.
36. Faloona GR, Srere PA. Escherichia coli citrate synthase. Purification and the effect of potassium on some properties. Biochemistry 1969, 8(11):4497-4503. 10.1021/bi00839a041, 4900996.
37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.
38. Demaison L, Moreau D, Vergely-Vandriesse C, Gregoire S, Degois M, Rochette L. Effects of dietary polyunsaturated fatty acids and hepatic steatosis on the functioning of isolated working rat heart under normoxic conditions and during post-ischemic reperfusion. Mol Cell Biochem 2001, 224(1-2):103-116.
39. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957, 226(1):497-509.
40. Juaneda P, Rocquelin G. Rapid and convenient separation of phospholipids and non phosphorus lipids from rat heart using silica cartridges. Lipids 1985, 20(1):40-41. 10.1007/BF02534360, 2982073.
41. Sudar E, Dobutovic B, Soskic S, Mandusic V, Zakula Z, Misirkic M, Vucicevic L, Janjetovic K, Trajkovic V, Mikhailidis DP. Regulation of inducible nitric oxide synthase activity/expression in rat hearts from ghrelin-treated rats. J Physiol Biochem 2011, 67(2):195-204. 10.1007/s13105-010-0063-1, 21107779.
42. Wang MX, Murrell DF, Szabo C, Warren RF, Sarris M, Murrell GA. Nitric oxide in skeletal muscle: inhibition of nitric oxide synthase inhibits walking speed in rats. Nitric oxide: biology and chemistry/official journal of the Nitric Oxide Society 2001, 5(3):219-232.
43. Okon EB, Szado T, Laher I, McManus B, van Breemen C. Augmented contractile response of vascular smooth muscle in a diabetic mouse model. J Vasc Res 2003, 40(6):520-530. 10.1159/000075238, 14646372.
44. Parise G, Brose AN, Tarnopolsky MA. Resistance exercise training decreases oxidative damage to DNA and increases cytochrome oxidase activity in older adults. Exp Gerontol 2005, 40(3):173-180. 10.1016/j.exger.2004.09.002, 15763394.
45. Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid Redox Signal 2005, 7(7-8):1021-1031. 1434604, 15998257.
46. Rupp H, Wagner D, Rupp T, Schulte LM, Maisch B. Risk stratification by the "EPA + DHA level" and the "EPA/AA ratio" focus on anti-inflammatory and antiarrhythmogenic effects of long-chain omega-3 fatty acids. Herz 2004, 29(7):673-685. 10.1007/s00059-004-2602-4, 15580322.
47. Pepe S, McLennan PL. Cardiac membrane fatty acid composition modulates myocardial oxygen consumption and postischemic recovery of contractile function. Circulation 2002, 105(19):2303-2308. 10.1161/01.CIR.0000015604.88808.74, 12010914.
48. Essop MF, Anna Chan WY, Valle A, Garcia-Palmer FJ, Du Toit EF. Impaired contractile function and mitochondrial respiratory capacity in response to oxygen deprivation in a rat model of pre-diabetes. Acta Physiol (Oxf) 2009, 197(4):289-296.
49. Wang P, Lloyd SG, Zeng H, Bonen A, Chatham JC. Impact of altered substrate utilization on cardiac function in isolated hearts from zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol 2005, 288(5):H2102-H2110. 10.1152/ajpheart.00935.2004, 15615844.
50. Finck BN, Han X, Courtois M, Aimond F, Nerbonne JM, Kovacs A, Gross RW, Kelly DP. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc Natl Acad Sci U S A 2003, 100(3):1226-1231. 10.1073/pnas.0336724100, 298755, 12552126.
51. Daniels A, van Bilsen M, Janssen BJ, Brouns AE, Cleutjens JP, Roemen TH, Schaart G, van der Velden J, van der Vusse GJ, van Nieuwenhoven FA. Impaired cardiac functional reserve in type 2 diabetic db/db mice is associated with metabolic, but not structural, remodelling. Acta Physiol (Oxf) 2010, 200(1):11-22.
52. Semeniuk LM, Kryski AJ, Severson DL. Echocardiographic assessment of cardiac function in diabetic db/db and transgenic db/db-hGLUT4 mice. Am J Physiol Heart Circ Physiol 2002, 283(3):H976-H982.
53. Barth AS, Tomaselli GF. Cardiac metabolism and arrhythmias. Circulation Arrhythmia and electrophysiology 2009, 2(3):327-335. 10.1161/CIRCEP.108.817320, 2744981, 19808483.
54. Fredersdorf S, Thumann C, Zimmermann WH, Vetter R, Graf T, Luchner A, Riegger GA, Schunkert H, Eschenhagen T, Weil J. Increased myocardial SERCA expression in early type 2 diabetes mellitus is insulin dependent: In vivo and in vitro data. Cardiovasc Diabetol 2012, 11:57. 10.1186/1475-2840-11-57, 3447673, 22621761.
55. Nakamura H, Matoba S, Iwai-Kanai E, Kimata M, Hoshino A, Nakaoka M, Katamura M, Okawa Y, Ariyoshi M, Mita Y. p53 Promotes cardiac dysfunction in diabetic mellitus caused by excessive mitochondrial respiration-mediated reactive oxygen species generation and lipid accumulation. Circ Heart Fail 2012, 5(1):106-115. 10.1161/CIRCHEARTFAILURE.111.961565, 22075967.
56. Sharma S, Adrogue JV, Golfman L, Uray I, Lemm J, Youker K, Noon GP, Frazier OH, Taegtmeyer H. Intramyocardial lipid accumulation in the failing human heart resembles the lipotoxic rat heart. FASEB J 2004, 18(14):1692-1700. 10.1096/fj.04-2263com, 15522914.
57. Wissler RW. The production of atheromatous lesions in the albino rat. Proc Inst Med Chic 1952, 19(4):79-80.
58. McCabe TJ, Fulton D, Roman LJ, Sessa WC. Enhanced electron flux and reduced calmodulin dissociation may explain "calcium-independent" eNOS activation by phosphorylation. J Biol Chem 2000, 275(9):6123-6128. 10.1074/jbc.275.9.6123, 10692402.
59. Nagareddy PR, Xia Z, McNeill JH, MacLeod KM. Increased expression of iNOS is associated with endothelial dysfunction and impaired pressor responsiveness in streptozotocin-induced diabetes. Am J Physiol Heart Circ Physiol 2005, 289(5):H2144-H2152. 10.1152/ajpheart.00591.2005, 16006542.
60. Chen CA, Druhan LJ, Varadharaj S, Chen YR, Zweier JL. Phosphorylation of endothelial nitric-oxide synthase regulates superoxide generation from the enzyme. J Biol Chem 2008, 283(40):27038-27047. 10.1074/jbc.M802269200, 2556006, 18622039.
61. Shimokawa H, Matoba T. Hydrogen peroxide as an endothelium-derived hyperpolarizing factor. Pharmacol Res 2004, 49(6):543-549. 10.1016/j.phrs.2003.10.016, 15026032.
62. Gao X, Picchi A, Zhang C. Upregulation of TNF-alpha and receptors contribute to endothelial dysfunction in zucker diabetic rats. Am J Biomed Sci 2010, 2(1):1-12. 2886289, 20559450.
63. Oltman CL, Kleinschmidt TL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Treatment of cardiovascular dysfunction associated with the metabolic syndrome and type 2 diabetes. Vascul Pharmacol 2008, 48(1):47-53. 10.1016/j.vph.2007.11.005, 18164667.
64. Oniki H, Fujii K, Kansui Y, Goto K, Iida M. Effects of angiotensin II receptor antagonist on impaired endothelium-dependent and endothelium-independent relaxations in type II diabetic rats. J Hypertens 2006, 24(2):331-338. 10.1097/01.hjh.0000200518.34980.cc, 16508581.
65. Spector AA, Hoak JC, Fry GL, Denning GM, Stoll LL, Smith JB. Effect of fatty acid modification on prostacyclin production by cultured human endothelial cells. J Clin Invest 1980, 65(5):1003-1012. 10.1172/JCI109752, 371430, 6767738.
66. Mori TA, Watts GF, Burke V, Hilme E, Puddey IB, Beilin LJ. Differential effects of eicosapentaenoic acid and docosahexaenoic acid on vascular reactivity of the forearm microcirculation in hyperlipidemic, overweight men. Circulation 2000, 102(11):1264-1269. 10.1161/01.CIR.102.11.1264, 10982541.
67. Brandes RP, Kim D, Schmitz-Winnenthal FH, Amidi M, Godecke A, Mulsch A, Busse R. Increased nitrovasodilator sensitivity in endothelial nitric oxide synthase knockout mice: role of soluble guanylyl cyclase. Hypertension 2000, 35(1 Pt 2):231-236.
68. Jebelovszki E, Kiraly C, Erdei N, Feher A, Pasztor ET, Rutkai I, Forster T, Edes I, Koller A, Bagi Z. High-fat diet-induced obesity leads to increased NO sensitivity of rat coronary arterioles: role of soluble guanylate cyclase activation. Am J Physiol Heart Circ Physiol 2008, 294(6):H2558-H2564. 10.1152/ajpheart.01198.2007, 18408126.
69. Radovits T, Korkmaz S, Loganathan S, Barnucz E, Bomicke T, Arif R, Karck M, Szabo G. Comparative investigation of the left ventricular pressure-volume relationship in rat models of type 1 and type 2 diabetes mellitus. Am J Physiol Heart Circ Physiol 2009, 297(1):H125-H133. 10.1152/ajpheart.00165.2009, 19429826.
70. Crandall DL, Goldstein BM, Lizzo FH, Gabel RA, Cervoni P. Hemodynamics of obesity: influence of pattern of adipose tissue cellularity. Am J Physiol 1986, 251(2 Pt 2):R314-R319.