No effects of atorvastatin (10 mg/d or 80 mg/d) on nitric oxide, prostacyclin, thromboxane and oxidative stress in type 2 diabetes mellitus patients of the DALI study

Pharmacological Research

Volumn 94, Issue , 2015, Pages 1-8

  Tsikas, Dimitrios ^a   Pham, Vu Vi ^a   Suchy, Maria Theresia ^a   Van De Ree, Marcel A ^b   Huisman, Menno V ^b   Frölich, Jürgen C ^a   Princen, Hans M G ^c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c TNO   (Netherlands)

Author keywords

8 iso Prostaglandin F2 ; Carbonic anhydrase; Cardiovascular disease; Diabetes mellitus type 2; Nitric oxide; Oxidative stress; Prostacyclin; Statins; Thromboxane

Indexed keywords

2,3 DINOR 6 OXOPROSTAGLANDIN F1 ALPHA; 2,3 DINORTHROMBOXANE B2; 8 ISOPROSTAGLANDIN F2 ALPHA; ATORVASTATIN; CARBONATE DEHYDRATASE; CHOLESTEROL; NITRATE; NITRIC OXIDE; NITRITE; PLACEBO; PROSTACYCLIN; PROSTAGLANDIN SYNTHASE; THROMBOXANE; THROMBOXANE A2; 6 OXOPROSTAGLANDIN F1 ALPHA; 8-EPI-PROSTAGLANDIN F2ALPHA; CREATININE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PROSTACYCLIN DERIVATIVE; PROSTAGLANDIN F2 ALPHA;

ADULT; AGED; ANTIOXIDANT ACTIVITY; ARTICLE; BIOSYNTHESIS; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG EFFECT; DRUG TREATMENT FAILURE; DYSLIPIDEMIA; FEMALE; HEART PROTECTION; HUMAN; LIPID PEROXIDATION; LIPOLYSIS; MAJOR CLINICAL STUDY; MALE; MASS FRAGMENTOGRAPHY; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; TANDEM MASS SPECTROMETRY; TREATMENT DURATION; URINE LEVEL; ANALOGS AND DERIVATIVES; DRUG EFFECTS; METABOLISM; URINE;

6-KETOPROSTAGLANDIN F1 ALPHA; AGED; ATORVASTATIN CALCIUM; CREATININE; DIABETES MELLITUS, TYPE 2; DINOPROST; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; FEMALE; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MALE; MIDDLE AGED; NITRIC OXIDE; OXIDATIVE STRESS; PROSTAGLANDINS I; THROMBOXANES;

EID: 84923108972     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.01.004     Document Type: Article

References (87)

1. C.R. Sirtori The pharmacology of statins Pharmacol Res 88 2014 3 11
2. M. Bifulco, and A. Endo Statin: new life for an old drug Pharmacol Res 88 2014 1 2
3. N. Ferri, and A. Corsini Clinical evidence of statin therapy in non-dyslipidemic disorders Pharmacol Res 88 2014 20 30
4. S. Pisanti, P. Picardi, E. Ciaglia, A. D'Alessandro, and M. Bifulco Novel prospects of statins as therapeutic agents in cancer Pharmacol Res 88 2014 84 98
5. T.I. Kassimatis, and D.J. Goldsmith Statins in chronic kidney disease and kidney transplantation Pharmacol Res 88 2014 62 73
6. C. Ulivieri, and C.T. Baldari Statins: from cholesterol-lowering drugs to novel immunomodulators for the treatment of Th17-mediated autoimmune diseases Pharmacol Res 88 2014 41 52
7. G.D. Norata, G. Tibolla, and A.L. Catapano Statins and skeletal muscles toxicity: from clinical trials to everyday practice Pharmacol Res 88 2014 107 113
8. H.L. Lv, D.M. Jin, M. Liu, Y.M. Liu, J.F. Wang, and D.F. Geng Long-term efficacy and safety of statin treatment beyond six years: a meta-analysis of randomized controlled trials with extended follow-up Pharmacol Res 81 2014 64 73
9. I.C. Gelissen, and A.J. McLachlan The pharmacogenomics of statins Pharmacol Res 88 2014 99 106
10. M.J. Klag, D.E. Ford, L.A. Mead, J. He, P.K. Whelton, and K.Y. Linag Serum cholesterol in young men and subsequent cardiovascular disease N Engl J Med 328 1993 313 318
11. Scandinavian Simvastatin Survival Study Group Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: Scandinavian Simvastatin Survival Study (4S) Lancet 344 1994 1383 1389
12. M. Takemoto, and J.K. Liao Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors Arterioscler Thromb Vasc Biol 21 2001 1712 1719
13. U. Laufs, and J.K. Liao Post-transcriptional regulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors Circulation 97 1998 1129 1135
14. Y. Rikitake, S. Kawashima, S. Takeshita, T. Yamashita, H. Azumi, and M. Yasahura Anti-oxidative properties of fluvastatin, an HMG-CoA reductase inhibitor, contribute to prevention of atherosclerosis in cholesterol-fed rabbits Atherosclerosis 154 2001 87 96
15. U. Landmesser, B. Hornig, and H. Drexler Endothelial dysfunction in hypercholesterolemia: mechanisms, pathophysiological importance, and therapeutic interventions Semin Thromb Hemost 26 2000 529 537
16. S.H. Wilson, R.D. Simari, P.J.M. Best, T.E. Peterson, L.O. Lerman, and M. Aviram Simvastatin preserves coronary endothelial function in hypercholesterolemia in the absence of lipid lowering Arterioscler Thromb Vasc Biol 21 2001 122 128
17. S.M. Haffner Management of dyslipidemia in adults with diabetes Diabetes Care 21 1998 160 178
18. J.R. Sowers, M. Epstein, and E.D. Fröhlich Diabetes, hypertension, and cardiovascular disease: an update Hypertension 37 2001 1053 1059
19. S. Pennathur, and J.W. Heinecke Mechanisms of oxidative stress in diabetes: implications for the pathogenesis of vascular disease and antioxidant therapy Front Biosci 9 2004 565 574
20. 2-isoprostanes: markers and mediators in human disease Curr Pharm Anal 3 2007 39 51
21. D. Steinberg, and A. Lewis Conner Memorial Lecture. Oxidative modification of LDL and atherogenesis Circulation 95 1997 1062 1071
22. A. Oguogho, and H. Sinzinger Isoprostanes in atherosclerosis J Physiol Pharmacol 51 2000 673 682
23. 2-Isoprostanes) in smokers N Engl J Med 332 1995 1198 1203
24. 2α levels are elevated in individuals with non-insulin dependent diabetes mellitus FEBS Lett 368 1995 225 229
25. 2α and platelet activation in diabetes mellitus: effects of improved metabolic control and vitamin E supplementation Circulation 99 1999 224 229
26. 2α is increased in hypercholesterolemia Arterioscler Thromb Vasc Biol 11 1997 3230 3234
27. 2 isoprostanes in hypercholesterolemia Circulation 98 1998 2822 2828
28. J.P. Cooke, and X.X. Flow NO and atherogenesis Proc Natl Acad Sci USA 100 2003 768 770
29. U. Landmesser, D.G. Harrison, and H. Drexler Oxidant stress-a major cause of reduced endothelial nitric oxide availability in cardiovascular diseases Eur J Clin Pharmacol 62 2006 13 19
30. F.V. van Venrooij, M.A. van de Ree, M.L. Bots, R.P. Stolk, M.V. Huisman, J.D. Banga on behalf of the DALI study group Aggressive lipid lowering does not improve endothelial function in type 2 diabetes mellitus Diabetes Care 25 2002 1211 1216
31. 2-isoprostane formation in hypercholesterolemic subjects: no further effect of vitamin E Circulation 106 2002 2543 2549
32. R. Preston Mason, M.F. Walter, and R.F. Jacob Effects of HMG-CoA reductase inhibitors on endothelial function. Role of microdomains and oxidative stress Circulation Suppl. II 2004 109 II-34-II-41
33. The effect of aggressive versus standard lipid lowering by atorvastatin on diabetic dyslipidemia. The Diabetes Atorvastatin Lipid Intervention (DALI) Study Group Diabetes Care 24 2001 1335 1341
34. D. Tsikas Simultaneous derivatization and quantification of the nitric oxide metabolites nitrite and nitrate in biological fluids by gas chromatography/mass spectrometry Anal Chem 72 2000 4064 4072
35. D. Tsikas, E. Schwedhelm, J. Fauler, F.M. Gutzki, E. Mayatepek, and J.C. Frölich Specific and rapid quantification of 8-iso-prostaglandin via in urine of healthy humans and patients with Zellweger syndrome by gas chromatography-tandem mass spectrometry J Chromatogr B 716 1998 7 17
36. 2α in human urine J Chromatogr B 74 2000 99 112
37. 1α in human urine J Chromatogr A 885 2000 351 359
38. D. Tsikas, F.M. Gutzki, and D.O. Stichtenoth Circulating and excretory nitrite and nitrate as indicators of nitric oxide synthesis in humans: methods of analysis Eur J Clin Pharmacol 62 2006 51 59
39. V.V. Pham, D.O. Stichtenoth, and D. Tsikas Nitrite correlates with 3-nitrotyrosine but not with the F(2)-isoprostane 15(S)-8-iso-PGF(2alpha) in urine of rheumatic patients Nitric Oxide 21 2009 210 215
40. D. Tsikas, J. Niemann, M. Flentje, A. Schwarz, and P. Tossios N-Acetylcysteine (NAC) inhibits renal nitrite and nitrate reabsorption in healthy subjects and in patients undergoing cardiac surgery: risk of nitric oxide (NO) bioavailability loss by NAC? Int J Cardiol 177 2014 30 33
41. D. Tsikas Application of gas chromatography-mass spectrometry and gas chromatography-tandem mass spectrometry to assess in vivo synthesis of prostaglandins, thromboxane, leukotrienes, isoprostanes and related compounds in humans J Chromatogr B 717 1998 201 245
42. S. Parkkila, D. Vullo, A. Maresca, F. Carta, A. Scozzafava, and C.T. Supuran Serendipitous fragment-based drug discovery: ketogenic diet metabolites and statins effectively inhibit several carbonic anhydrases Chem Commun (Camb) 48 2012 3551 3553
43. D. Tsikas, E. Schwedhelm, M.T. Suchy, J. Niemann, F.M. Gutzki, and V.J. Erpenbeck Divergence in urinary 8-iso-PGF(2alpha) (IPF(2alpha)-III, 15-F(2t)-IsoP) levels from gas chromatography-tandem mass spectrometry quantification after thin-layer chromatography and immunoaffinity column chromatography reveals heterogeneity of 8-iso-PGF(2alpha), possible methodological, mechanistic and clinical implications J Chromatogr B 794 2003 237 255
44. 2α FEBS Lett 586 2012 3723 3730
45. G. Lupattelli, B. Palumbo, and H. Sinzinger Statin induced myopathy does not show up in MIBI scintigraphy Nuclear Med Commun 22 2001 575 578
46. H. Sinzinger, F. Chehne, and G. Lupattelli Oxidation injury in patients receiving HMG-CoA reductase inhibitors: occurrence in patients without enzyme elevation or myopathy Drug Saf 25 2002 877 883
47. H. Sinzinger, and A. Oguogho Variable influence of statins on isoprostanes in hyperlipidemia Adv Exp Med Biol 525 2003 209 212
48. M.S. Zhou, E.A. Jaimes, and L. Raij Atorvastatin prevents end-organ injury in salt-sensitive hypertension: role of eNOS and oxidant stress Hypertension 44 2004 186 190
49. M. Sugiyama, M. Ohashi, H. Takase, K. Sato, R. Ueda, and Y. Dohi Effects of atorvastatin on inflammation and oxidative stress Heart Vessels 20 2005 133 136
50. G.D. Kom, E. Schwedhelm, R. Maas, R. Schneider, R. Benndorf, and R.H. Böger Impact of atorvastatin treatment on platelet-activating factor acetylhydrolase and 15-F(2trans)-isoprostane in hypercholesterolaemic patients Br J Clin Pharmacol 63 2007 672 679
51. R. Cangemi, L. Loffredo, R. Carnevale, L. Perri, M.P. Patrizi, and V. Sanguigni Early decrease of oxidative stress by atorvastatin in hypercholesterolaemic patients: effect on circulating vitamin E Eur Heart J 29 2008 54 62
52. B. Ky, A. Burke, S. Tsimikas, M.L. Wolfe, M.G. Tadesse, and P.O. Szapary The influence of pravastatin and atorvastatin on markers of oxidative stress in hypercholesterolemic humans J Am Coll Cardiol 51 2008 1653 1662
53. M.S. Zhou, I.H. Schuman, E.A. Jaimes, and L. Raij Renoprotection by statins is linked to a decrease in renal oxidative stress, TGF-beta, and fibronectin with concomitant increase in nitric oxide bioavailability Am J Physiol Renal Physiol 295 2008 F53 F59
54. U. Singh, S. Devaraj, I. Jialal, and D. Siegel Comparison effect of atorvastatin (10 versus 80 mg) on biomarkers of inflammation and oxidative stress in subjects with metabolic syndrome Am J Cardiol 102 2008 321 325
55. V. Noriega, C. Pennanen, M.P. Sánchez, M. Chiong, M. Llancaqueo, and S. Lavandero (TTA)n polymorphism in 3-hydroxy-3-methylglutaryl-coenzyme A and response to atorvastatin in coronary artery disease patients Basic Clin Pharmacol Toxicol 104 2009 211 215
56. P. Pignatelli, R. Carnevale, R. Cangemi, L. Loffredo, V. Sanguigni, and C. Stefanutti Atorvastatin inhibits gp91phox circulating levels in patients with hypercholesterolemia Arterioscler Thromb Vascul Biol 30 2010 360 367
57. M. Renke, N. Knap, L. Tylicki, P. Rutkowski, A. Neuwelt, and W. Larczynski Atorvastatin attenuates oxidative stress in patients with chronic kidney disease Med Sci Monitor 16 2010 LE3-3
58. R. Carnevale, P. Pignatelli, S. Di Santo, S. Bartimoccia, V. Sanguigni, and L. Napoleone Atorvastatin inhibits oxidative stress via adiponectin-mediated NADPH oxidase down-regulation in hypercholesterolemic patients Atherosclerosis 213 2010 225 234
59. S. Negi, I. Shukrullah, E. Veledar, H.L. Bloom, D.P. Jones, and S.C. Dudley Statin therapy for the prevention of atrial fibrillation trial (SToP AF trial) J Cardiovasc Electrophysiol 22 2011 414 419
60. P. Pignatelli, R. Carnevale, D. Pastori, R. Cangemi, L. Napoleone, and S. Bartimoccia Immediate antioxidant and antiplatelet effect of atorvastatin via inhibition of Nox2 Circulation 126 2012 92 103
61. P.G. Scheffer, R.K. Schindhelm, V.M. van Verschuer, M. Groenemeijer, S. Simsek, and Y.M. Smulders No effect of atorvastatin and simvastatin on oxidative stress in patients at high risk for cardiovascular disease Neth J Med 71 2013 359 365
62. A. Kei, C. Tellis, E. Liberopoulos, A. Tselepis, and M. Elisaf Effect of switch to the highest dose of rosuvastatin versus add-on-statin fenofibrate versus add-on-statin nicotinic acid/laropiprant on oxidative stress markers in patients with mixed dyslipidemia Cardiovasc Ther 32 2014 139 146
63. F. Violi, R. Carnevale, D. Pastori, and P. Pignatelli Antioxidant and antiplatelet effects of atorvastatin by Nox2 inhibition Trends Cardiovasc Med 24 2014 142 148
64. J.F. Berbée, M.C. Wong, Y. Wang, J.W. van der Hoorn, P.P. Khedoe, and J.B. van Klinken Resveratrol protects against atherosclerosis, but does not add to the antiatherogenic effect of atorvastatin, in APOE∗3-Leiden. CETP mice J Nutr Biochem 24 2014 1423 1430
65. F.H.A.F. de Man, I.J.A.M. Jonkers, E. Schwedhelm, A.H.M. Smelt, W. Onkenhout, and W. van Duyvenvoorde Normal oxidative stress and enhanced lipoprotein resistance to in vitro oxidation in hypertriglyceridemia. Effects of bezafibrate therapy Arterioscler Thromb Vasc Biol 20 2000 2434 2440
66. 2-isoprostanes) in plasma and low density lipoprotein exposed to oxidative stress in vitro J Clin Investig 93 1994 998 1004
67. N. Roglans, E. Sanguino, C. Peris, M. Alegret, M. Vazquez, and T. Adzet Atorvastatin treatment induced peroxisome proliferator-activated receptor α expression and decreased plasma nonesterified fatty acids and liver triglyceride in fructose-fed rats J Pharmacol Exp Ther 302 2002 232 239
68. P. Ferre The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity Diabetes 53 2004 43 50
69. G. Martin, H. Duez, C. Blanquart, V. Berezowski, P. Poulain, and J.C. Fruchart Statin-induced inhibition of the Rho-signaling pathway activates PPAR alpha and induces HDL apoA-I J Clin Investig 107 2001 1423 1431
70. 2α is frequently increased in patients with muscle pain and/or CK-elevation after HMG-Co-enzyme-A-reductase inhibitor therapy J Clin Pharm Ther 26 2001 303 310
71. S.J. O'Meara, and B.T. Kinsella Effect of the statin atorvastatin on intracellular signaling by the prostacyclin receptor in vitro and in vivo Br J Pharmacol 43 2004 292 302
72. K. Nakamura, H. Masuda, H. Kariyazono, J. Arima, Y. Iguro, and K. Yamada Effects of atorvastatin and aspirin combined therapy on inflammatory responses in patients undergoing coronary artery bypass grafting Cytokine 36 2006 201 210
73. M.T. Santos, M.P. Fuset, M. Ruano, A. Moscardó, and J. Valles Effect of atorvastatin on platelet thromboxane A(2) synthesis in aspirin-treated patients with acute myocardial infarction Am J Cardiol 104 2009 1618 1623
74. S. Alusik, Z. Paluch, M. Lejsková, and T. Adámek The inhibitory effect of statins on urinary 11-dehydrothromboxane levels Int Angiol 29 2010 255 259
75. L. Puccetti, F. Santilli, A.L. Pasqui, S. Lattanzio, R. Liani, and F. Ciani Effects of atorvastatin and rosuvastatin on thromboxane-dependent platelet activation and oxidative stress in hypercholesterolemia Atherosclerosis 214 2012 122 128
76. B. Luzak, M. Boncler, J. Rywaniak, R. Wilk, L. Stanczyk, and M. Czyz The effect of a platelet cholesterol modulation on the acetylsalicylic acid-mediated blood platelet inhibition in hypercholesterolemic patients Eur J Pharmacol 658 2011 91 97
77. P. Pignatelli, R. Carnevale, D. Pastori, R. Cangemi, L. Napoleone, and C. Bartimoccia Nocella Immediate antioxidant and antiplatelet effect of atorvastatin via inhibition of Nox2 Circulation 126 2012 92 103
78. A. Moscardó, J. Vallés, A. Latorre, I. Madrid, and M.T. Santos Reduction of platelet cytosolic phospholipase A2 activity by atorvastatin and simvastatin: biochemical regulatory mechanisms Thromb Res 131 2013 e154 e159
79. K.P. Bliden, A. Singla, M.G. Gesheff, P.P. Toth, A. Tabrizchi, and G. Ens Statin therapy and thromboxane generation in patients with coronary artery disease treated with high-dose aspirin Thromb Haemost 112 2014 323 331
80. R.J. Gryglewski, W. Uracz, J. Swies, S. Chlopicki, E. Marcinkiewicz, and M. Lomnicka Comparison of endothelial pleiotropic actions of angiotensin converting enzyme inhibitors and statins Ann N Y Acad Sci 947 2001 229 245
81. M. Bayes, X. Rabasseda, and J.R. Prous Gateways to clinical trials Methods Find Exp Clin Pharmacol 24 2002 159 184
82. Y. Birnbaum, Y. Ye, S. Rosanio, S. Tavackoli, Z.Y. Hu, and E.R. Schwarz Prostaglandins mediate the cardioprotective effects of atorvastatin against ischemia-reperfusion injury Cardiovasc Res 65 2005 345 355
83. A.M. Kuklinska, B. Mroczko, W.J. Musial, R. Sawicki, A. Kozieradzka, and M. Usowicz-Szarynska Influence of atorvastatin on blood pressure control in treated hypertensive, normolipemic patients - an open, pilot study Blood Press 19 2010 260 266
84. 2α, a potent agonist of the vascular thromboxane/endoperoxide receptor, is a platelet thromboxane/endoperoxide receptor antagonist Prostaglandins 44 1992 155 163
85. 2 receptor in vivo Circulation 101 2000 2833 2840
86. J. Bauer, A. Ripperger, S. Frantz, S. Ergün, E. Schwedhelm, and R.A. Benndorf Pathophysiology of isoprostanes in the cardiovascular system: implications of isoprostane-mediated thromboxane A2 receptor activation Br J Pharmacol 171 2014 3115 3131
87. D. Tousoulis, C. Simopoulou, N. Papageorgious, E. Oikonomou, G. Hatzis, and G. Siasos Endothelial dysfunction in conduit arteries and in microcirculation. Novel therapeutic approaches Pharmacol Ther 144 2014 253 267