COX-2-Derived Prostanoids and Oxidative Stress Additionally Reduce Endothelium-Mediated Relaxation in Old Type 2 Diabetic Rats

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Vessières, Emilie ^a,d   Guihot, Anne Laure ^a,b   Toutain, Bertrand ^a   Maquigneau, Maud ^a   Fassot, Céline ^a,c   Loufrani, Laurent ^a,b   Henrion, Daniel ^a,c,d  

^a UNIVERSITÉ D'ANGERS   (France)

^b CNRS   (France)

^c INSERM   (France)

^d ANGERS UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CYCLOOXYGENASE 2; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PROSTANOID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SUPEROXIDE; TEMPOL;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BLOOD VESSEL TONE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; ENZYME INHIBITION; ISOLATED ARTERY; JUVENILE ANIMAL; MALE; MESENTERIC ARTERY; MYOGRAPHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORGAN PERFUSION; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; RAT STRAIN; RESISTANCE BLOOD VESSEL; VASODILATATION; WESTERN BLOTTING; ZUCKER DIABETIC FATTY RAT;

ACETYLCHOLINE; ANIMALS; BLOOD GLUCOSE; BLOOD PRESSURE; BODY WEIGHT; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; ENDOTHELIUM, VASCULAR; MALE; OXIDATIVE STRESS; PHENYLEPHRINE; PROSTAGLANDINS; RATS; REACTIVE OXYGEN SPECIES; VASOCONSTRICTION; VASODILATION;

RATTUS;

EID: 84879942905     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068217     Document Type: Article

References (66)

1. Wild S, Roglic G, Green A, Sicree R, King H, (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 1047-1053.
2. Eckel RH, Grundy SM, Zimmet PZ, (2005) The metabolic syndrome. Lancet 365: 1415-1428.
3. Adams KF, Schatzkin A, Harris TB, Kipnis V, Mouw T, et al. (2006) Overweight, obesity, and mortality in a large prospective cohort of persons 50 to 71 years old. N Engl J Med 355: 763-778.
4. Ford ES, (2005) Risks for all-cause mortality, cardiovascular disease, and diabetes associated with the metabolic syndrome: a summary of the evidence. Diabetes Care 28: 1769-1778.
5. Mokdad AH, Bowman BA, Ford ES, Vinicor F, Marks JS, et al. (2001) The continuing epidemics of obesity and diabetes in the United States. Jama 286: 1195-1200.
6. Pieper GM, Siebeneich W, (1997) Diabetes-induced endothelial dysfunction is prevented by long-term treatment with the modified iron chelator, hydroxyethyl starch conjugated-deferoxamine. J Cardiovasc Pharmacol 30: 734-738.
7. Winer N, Sowers JR, (2007) Diabetes and arterial stiffening. Adv Cardiol 44: 245-251.
8. Grundy SM, (2008) Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol 28: 629-636.
9. Barton M, (2010) Obesity and aging: determinants of endothelial cell dysfunction and atherosclerosis. Pflugers Arch 460: 825-837.
10. Vessieres E, Freidja ML, Loufrani L, Fassot C, Henrion D, (2012) Flow (shear stress)-mediated remodeling of resistance arteries in diabetes. Vascul Pharmacol 57: 173-178.
11. Tousoulis D, Kampoli AM, Stefanadis C, (2012) Diabetes mellitus and vascular endothelial dysfunction: current perspectives. Curr Vasc Pharmacol 10: 19-32.
12. Retailleau K, Belin de Chantemele EJ, Chanoine S, Guihot AL, Vessieres E, et al. (2010) Reactive oxygen species and cyclooxygenase 2-derived thromboxane A2 reduce angiotensin II type 2 receptor vasorelaxation in diabetic rat resistance arteries. Hypertension 55: 339-344.
13. Sharma A, Bernatchez PN, de Haan JB, (2012) Targeting endothelial dysfunction in vascular complications associated with diabetes. Int J Vasc Med 2012: 750126.
14. Portik-Dobos V, Anstadt MP, Hutchinson J, Bannan M, Ergul A, (2002) Evidence for a matrix metalloproteinase induction/activation system in arterial vasculature and decreased synthesis and activity in diabetes. Diabetes 51: 3063-3068.
15. Ding H, Aljofan M, Triggle CR, (2007) Oxidative stress and increased eNOS and NADPH oxidase expression in mouse microvessel endothelial cells. J Cell Physiol 212: 682-689.
16. Toda N, (2012) Age-related changes in endothelial function and blood flow regulation. Pharmacol Ther 133: 159-176.
17. Dumont O, Pinaud F, Guihot AL, Baufreton C, Loufrani L, et al. (2008) Alteration in flow (shear stress)-induced remodelling in rat resistance arteries with aging: improvement by a treatment with hydralazine. Cardiovasc Res 77: 600-608.
18. Pinaud F, Bocquet A, Dumont O, Retailleau K, Baufreton C, et al. (2007) Paradoxical role of angiotensin II type 2 receptors in resistance arteries of old rats. Hypertension 50: 96-102.
19. Kampoli AM, Tousoulis D, Briasoulis A, Latsios G, Papageorgiou N, et al. (2011) Potential pathogenic inflammatory mechanisms of endothelial dysfunction induced by type 2 diabetes mellitus. Curr Pharm Des 17: 4147-4158.
20. Driss A, Devaux C, Henrion D, Duriez M, Thuillez C, et al. (2000) Hemodynamic stresses induce endothelial dysfunction and remodeling of pulmonary artery in experimental compensated heart failure. Circulation 101: 2764-2770.
21. Bouvet C, Belin de Chantemele E, Guihot AL, Vessieres E, Bocquet A, et al. (2007) Flow-induced remodeling in resistance arteries from obese Zucker rats is associated with endothelial dysfunction. Hypertension 50: 248-254.
22. Vessieres E, Belin de Chantemele EJ, Toutain B, Guihot AL, Jardel A, et al. (2010) Cyclooxygenase-2 inhibition restored endothelium-mediated relaxation in old obese zucker rat mesenteric arteries. Front Physiol 1: 145.
23. Dowell FJ, Henrion D, Benessiano J, Poitevin P, Levy B, (1996) Chronic infusion of low-dose angiotensin II potentiates the adrenergic response in vivo. J Hypertens 14: 177-182.
24. Henrion D, Laher I, Laporte R, Bevan JA, (1992) Further evidence from an elastic artery that angiotensin II amplifies noradrenaline-induced contraction through activation of protein kinase C. Eur J Pharmacol. 224: 13-20.
25. Mulvany MJ, Halpern W, (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41: 19-26.
26. Henrion D, Laher I, Bevan JA, (1992) Intraluminal flow increases vascular tone and 45Ca2+ influx in the rabbit facial vein. Circ Res 71: 339-345.
27. Bolla M, Matrougui K, Loufrani L, Maclouf J, Levy B, et al. (2002) p38 mitogen-activated protein kinase activation is required for thromboxane- induced contraction in perfused and pressurized rat mesenteric resistance arteries. J Vasc Res 39: 353-360.
28. Loufrani L, Retailleau K, Bocquet A, Dumont O, Danker K, et al. (2008) Key role of alpha(1)beta(1)-integrin in the activation of PI3-kinase-Akt by flow (shear stress) in resistance arteries. Am J Physiol Heart Circ Physiol 294: H1906-1913.
29. Cousin M, Custaud MA, Baron-Menguy C, Toutain B, Dumont O, et al. (2010) Role of angiotensin II in the remodeling induced by a chronic increase in flow in rat mesenteric resistance arteries. Hypertension 55: 109-115.
30. Freidja ML, Toutain B, Caillon A, Desquiret V, Lambert D, et al. (2011) Heme oxygenase 1 is differentially involved in blood flow-dependent arterial remodeling: role of inflammation, oxidative stress, and nitric oxide. Hypertension 58: 225-231.
31. Baron-Menguy C, Bocquet A, Guihot AL, Chappard D, Amiot MJ, et al. (2007) Effects of red wine polyphenols on postischemic neovascularization model in rats: low doses are proangiogenic, high doses anti-angiogenic. FASEB J 21: 3511-3521.
32. Tarhouni K, Guihot AL, Freidja ML, Toutain B, Henrion B, et al. (2013) Key role of estrogens and endothelial estrogen receptor alpha in blood flow-mediated remodeling of resistance arteries. Arterioscler Thromb Vasc Biol 33: 605-611.
33. Doisaki M, Katano Y, Nakano I, Hirooka Y, Itoh A, et al. (2010) Regulation of hepatic branched-chain alpha-keto acid dehydrogenase kinase in a rat model for type 2 diabetes mellitus at different stages of the disease. Biochem Biophys Res Commun 393: 303-307.
34. Howarth FC, Al Kitbi MK, Hameed RS, Adeghate E, (2011) Pancreatic peptides in young and elderly Zucker type 2 diabetic fatty rats. JOP 12: 567-573.
35. Oltman CL, Richou LL, Davidson EP, Coppey LJ, Lund DD, et al. (2006) Progression of Coronary and Mesenteric Vascular Dysfunction in Zucker Obese and Zucker Diabetic Fatty Rats. Am J Physiol Heart Circ Physiol.
36. Naka KK, Papathanassiou K, Bechlioulis A, Kazakos N, Pappas K, et al. (2012) Determinants of vascular function in patients with type 2 diabetes. Cardiovasc Diabetol 11: 127.
37. Najjar SS, Scuteri A, Lakatta EG, (2005) Arterial aging: is it an immutable cardiovascular risk factor? Hypertension 46: 454-462.
38. Freidja ML, Tarhouni K, Toutain B, Fassot C, Loufrani L, et al. (2012) The AGE-breaker ALT-711 restores high blood flow-dependent remodeling in mesenteric resistance arteries in a rat model of type 2 diabetes. Diabetes 61: 1562-1572.
39. Dowell FJ, Henrion D, Duriez M, Michel JB, (1996) Vascular reactivity in mesenteric resistance arteries following chronic nitric oxide synthase inhibition in Wistar rats. Br J Pharmacol 117: 341-346.
40. Loufrani L, Levy BI, Henrion D, (2002) Defect in microvascular adaptation to chronic changes in blood flow in mice lacking the gene encoding for dystrophin. Circ Res 91: 1183-1189.
41. Henrion D, Dechaux E, Dowell FJ, Maclour J, Samuel JL, et al. (1997) Alteration of flow-induced dilatation in mesenteric resistance arteries of L-NAME treated rats and its partial association with induction of cyclo-oxygenase-2. Br J Pharmacol 121: 83-90.
42. Matrougui K, Levy BI, Henrion D, (2000) Tissue angiotensin II and endothelin-1 modulate differently the response to flow in mesenteric resistance arteries of normotensive and spontaneously hypertensive rats. Br J Pharmacol 130: 521-526.
43. Matsumoto T, Ishida K, Nakayama N, Taguchi K, Kobayashi T, et al. (2010) Mechanisms underlying the losartan treatment-induced improvement in the endothelial dysfunction seen in mesenteric arteries from type 2 diabetic rats. Pharmacol Res 62: 271-281.
44. Belin de Chantemele EJ, Vessieres E, Guihot AL, Toutain B, Maquignau M, et al. (2009) Type 2 diabetes severely impairs structural and functional adaptation of rat resistance arteries to chronic changes in blood flow. Cardiovasc Res 81: 788-796.
45. Leo CH, Hart JL, Woodman OL, (2011) 3′,4′-Dihydroxyflavonol reduces superoxide and improves nitric oxide function in diabetic rat mesenteric arteries. PLoS One 6: e20813.
46. Sena CM, Matafome P, Louro T, Nunes E, Fernandes R, et al. (2011) Metformin restores endothelial function in aorta of diabetic rats. Br J Pharmacol 163: 424-437.
47. Laight DW, Carrier MJ, Anggard EE, (2000) Antioxidants, diabetes and endothelial dysfunction. Cardiovasc Res 47: 457-464.
48. Hile C, Veves A, (2003) Diabetic neuropathy and microcirculation. Curr Diab Rep 3: 446-451.
49. Huang A, Yang YM, Feher A, Bagi Z, Kaley G, et al. (2012) Exacerbation of endothelial dysfunction during the progression of diabetes: role of oxidative stress. Am J Physiol Regul Integr Comp Physiol 302: R674-681.
50. El-Remessy AB, Tawfik HE, Matragoon S, Pillai B, Caldwell RB, et al. (2010) Peroxynitrite mediates diabetes-induced endothelial dysfunction: possible role of Rho kinase activation. Exp Diabetes Res 2010: 247861.
51. Georgescu A, Popov D, Constantin A, Nemecz M, Alexandru N, et al. (2011) Dysfunction of human subcutaneous fat arterioles in obesity alone or obesity associated with Type 2 diabetes. Clin Sci (Lond) 120: 463-472.
52. Forstermann U, Munzel T, (2006) Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714.
53. Leo CH, Hart JL, Woodman OL, (2011) Impairment of both nitric oxide-mediated and EDHF-type relaxation in small mesenteric arteries from rats with streptozotocin-induced diabetes. Br J Pharmacol 162: 365-377.
54. Oniki H, Goto K, Fujii K, Kansui Y, Murakami N, et al. (2012) Effects of the Superoxide Dismutase Mimetic Tempol on Impaired Endothelium-Dependent and Endothelium-Independent Relaxations in Type II Diabetic Rats. Clin Exp Hypertens.
55. Munzel T, Gori T, Bruno RM, Taddei S, (2010) Is oxidative stress a therapeutic target in cardiovascular disease? Eur Heart J 31: 2741-2748.
56. Vessieres E, Belin de Chantemele EJ, Guihot AL, Jardel A, Toutain B, et al. (2013) Cyclooxygenase-2-derived prostanoids reduce inward arterial remodeling induced by blood flow reduction in old obese Zucker rat mesenteric arteries. Vascul Pharmacol 58: 356-362.
57. Belin de Chantemele EJ, Vessieres E, Dumont O, Guihot AL, Toutain B, et al. (2009) Reactive oxygen species are necessary for high flow (shear stress)-induced diameter enlargement of rat resistance arteries. Microcirculation 16: 391-402.
58. Tian XY, Wong WT, Xu A, Lu Y, Zhang Y, et al. (2012) Uncoupling protein-2 protects endothelial function in diet-induced obese mice. Circ Res 110: 1211-1216.
59. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF, (1997) High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 96: 25-28.
60. Gendron ME, Thorin-Trescases N, Villeneuve L, Thorin E, (2007) Aging associated with mild dyslipidemia reveals that COX-2 preserves dilation despite endothelial dysfunction. Am J Physiol Heart Circ Physiol 292: H451-458.
61. Belin de Chantemele EJ, Vessieres E, Guihot AL, Toutain B, Loufrani L, et al. (2010) Cyclooxygenase-2 preserves flow-mediated remodelling in old obese Zucker rat mesenteric arteries. Cardiovasc Res 86: 516-525.
62. Wong SL, Leung FP, Lau CW, Au CL, Yung LM, et al. (2009) Cyclooxygenase-2-derived prostaglandin F2alpha mediates endothelium-dependent contractions in the aortae of hamsters with increased impact during aging. Circ Res 104: 228-235.
63. Tian XY, Wong WT, Leung FP, Zhang Y, Wang YX, et al. (2012) Oxidative stress-dependent cyclooxygenase-2-derived prostaglandin f(2alpha) impairs endothelial function in renovascular hypertensive rats. Antioxid Redox Signal 16: 363-373.
64. Garcia Rodriguez LA, Gonzalez-Perez A, Bueno H, Hwa J, (2011) NSAID use selectively increases the risk of non-fatal myocardial infarction: a systematic review of randomised trials and observational studies. PLoS One 6: e16780.
65. Dumont O, Loufrani L, Henrion D, (2007) Key role of the NO-pathway and matrix metalloprotease-9 in high blood flow-induced remodeling of rat resistance arteries. Arterioscler Thromb Vasc Biol 27: 317-324.
66. Prevost G, Bulckaen H, Gaxatte C, Boulanger E, Beraud G, et al. (2011) Structural modifications in the arterial wall during physiological aging and as a result of diabetes mellitus in a mouse model: are the changes comparable? Diabetes Metab 37: 106-111.