Acute simvastatin increases endothelial nitric oxide synthase phosphorylation via AMP-activated protein kinase and reduces contractility of isolated rat mesenteric resistance arteries

Clinical Science

Volumn 121, Issue 10, 2011, Pages 449-458

  Rossoni, Luciana V ^a,b   Wareing, Mark ^b   Wenceslau, Camilla F ^a   Al Abri, Mahmood ^b   Cobb, Chris ^b   Austin, Clare ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Acetylcholine; AMP activated protein kinase; Nitric oxide; Resistance artery; Simvastatin; Statin

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MEVALONIC ACID; PHENYLEPHRINE; PROTEIN KINASE B; SIMVASTATIN;

ANIMAL TISSUE; ARTICLE; BLOOD VESSEL CONTRACTILITY; CARDIOVASCULAR PARAMETERS; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MALE; MESENTERIC ARTERY; NONHUMAN; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MALE; MESENTERIC ARTERIES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SIMVASTATIN; TISSUE CULTURE TECHNIQUES; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS;

EID: 80052363447     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20110259     Document Type: Article

References (44)

1. Scandinavian SimvastatinSurvivalStudyInvestigators (1994) Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the scandinavian simvastatin survival study (4S). Lancet 344, 1383-1389
2. Heart Protection Study Collaborative Group (2002) MRC/BHF heart protection study of cholesterol lowering with simvastatin in 20,536 high-risk individuals: a randomised placebo-controlled trial. Lancet 360, 7-22
3. Tziomalos, K., Athyros, V. G., Karagiannis, A. and Mikhailidis, D. P. (2009) JUPITER: major implications for vascular risk assessment. Curr. Med. Res. Opin. 25, 133-137
4. Mora, S. and Ridker, P. M. (2006) Justification for the use of statins in primary prevention: an intervention trial evaluating rosuvastatin (JUPITER): can C-reactive protein be used to target statin therapy in primary prevention? Am. J. Cardiol. 97, 33A-41A
5. Anderson, T. J., Meredith, I. T., Yeung, A. C., Frei, B., Selwyn, A. P. and Ganz, P. (1995) The effect of cholesterol-lowering and antioxidant therapy on endothelium-dependent coronary vasomotion. N. Engl. J. Med. 332, 488-493
6. O'Driscoll, G., Green, D. and Taylor, R. R. (1997) Simvastatin, an HMG-coenzyme A reductase inhibitor, improves endothelial function within 1 month. Circulation 95, 1126-1131
7. Omori, H., Nagashima, H., Tsurumi, Y., Takagi, A., Ishizuka, N., Hagiwara, N., Kawana, M. and Kasanuki, H. (2002) Direct in vivo evidence of a vascular statin: a single does of cerivastatin rapidly increases vascular endothelial responsiveness in healthy normocholesterolaemic subjects. Br. J. Clin. Pharmacol. 54, 395-399
8. Chen, H., Ren, J. Y., Xing, Y., Zhang, W. L., Liu, X., Wu, P.,Wang, R. J. and Luo, Y. (2009) Short-term withdrawal of simvastatin induces endothelial dysfunction in patients with coronary artery disease: a dose-response effect dependent on endothelial nitric oxide synthase. Int. J. Cardiol. 131, 313-320
9. Sessa, W. C. (2004) eNOS at a glance. J. Cell Sci. 117, 2427-2429
10. Fulton, D., Gratton, J-P., McCabe, T. J., Fontana, J., Fujio, Y., Walsh, K., Franke, T. F., Papapetropoulos, A. and Sessa, W. C. (2000) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399, 597-601
11. Sugawara, T., Ayer, R., Jadhav, V., Chen, W., Tsubokawa, T. and Zhang, J. H. (2008) Simvastatin attenuation of cerebral vasospasm after subarachnoid hemorrhage in rats via increased phosphorylation of Akt and endothelial nitric oxide synthase. J. Neurosci. Res. 86, 3635-3643
12. Harris, M. B., Blackstone, M. A., Sood, S. G., Li, C., Goolsby, J. M., Venema, V. J., Kemp, B. E. and Venema, R. C. (2004) Acute activation and phosphorylation of endothelial nitric oxide synthase by HMG-CoA reductase inhibitors. Am. J. Physiol. Heart Circ. Physiol. 287, H560-H566
13. Wang, J., Xu, Z., Kitajima, I. andWang, Z. (2008) Effects of different statins on endothelial nitric oxide synthase and Akt phosphorylation in endothelial cells. Int. J. Cardiol. 127, 33-39
14. Wong, A. K.F., Howie, J., Petrie, J. R. and Lang, C. C. (2009) AMP-activated protein kinase pathway: a potential therapeutic target in cardiometabolic disease. Clin. Sci. 116, 607-620
15. Chen, Z. P., Mitchelhill, K. I., Michell, B. J., Stapleton, D., Rodriguez-Crespo, I., Witters, L. A., Power, D. A., Ortiz de Montellano, P. R. and Kemp, B. E. (1999) AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1443, 285-289
16. Chen, H., Montagnani, M., Funshashi, T., Shimomura, I. and Quon, M. J. (2003) Adiponection stimulates production of nitric oxide in vascular endothelial cells. J. Biol. Chem. 278, 45021-45026
17. Morrow, V. A., Foufelle, F., Connell, J. M., Petrie, J. R., Gould, G.W. and Salt, I. P. (2003) Direct activation of AMP-activated protein kinase stimulates nitric oxide synthesis in human aortic endothelial cells. J. Biol. Chem. 278, 31629-31639
18. Bradley, E. A., Eringa, E. C., Stehouwer, C. D., Korstjens, I., van Nieuw Amerongen, G. P., Musters, R., Sipkema, P., Clark, M. G. and Rattigan, S. (2010) Activation of AMP-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-β-d-ribofuranoside in the muscle microcirculation increases nitric oxide synthesis and microvascular perfusion. Arterioscler. Thromb. Vasc. Biol. 30, 1137-1142
19. Sun, W., Lee, T.-S., Zhu, M., Gu, C., Wang, Y., Zhu, Y. and Shyy, J. Y. (2006) Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation 114, 2655-2662
20. Izumi, Y., Shiota, M., Kusakabe, H., Hikita, Y., Nakao, T. and Nakamura, Y. (2009) Pravastatin accelerates ischemia-induced angiogenesis through AMP-activated protein kinase. Hypertens. Res. 32, 675-678
21. Mulvany, M. and Halpern,W. (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ. Res. 41, 19-26
22. Lilja, J. J., Kivisto, K. T. and Neuvoven, P. J. (1998) Grapefruit juice-simvastatin interaction: effect of serum concentrations of simvastatin, simvastatin acid and HMG-CoA reductase inhibitors. Clin. Pharmacol. Ther. 64, 477-483
23. Kantola, T., Kivisto, K. T. and Neuvoven, P. J. (1998) Erythromicin and verapamil considerably increase serum simvastatin and simvastatin acid concentrations. Clin. Pharmacol. Ther. 64, 177-182
24. Shaw, L., Taggart, M. J. and Austin, C. (2000) Mechanisms of 17β-oestradiol induced vasodilatation in isolated pressurised rat small arteries. Br. J. Pharmacol. 129, 555-565
25. Xavier, F. E., Davel, A. P., Fukuda, L. E. and Rossoni, L. V. (2009) Chronic ouabain treatment exacerbates blood pressure elevation in spontaneously hypertensive rats: the role of vascular mechanisms. J. Hypertens. 27, 1233-1242
26. Laufs, U. and Liao, J. K. (1998) Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J. Biol. Chem. 272, 24266-24271
27. Laufs, U., La Fata, V., Plutzky, J. and Liao, J. K. (1998) Upregulation of endothelial nitric oxide synthase by HMG-CoA reductase inhibitors. Circulation 97, 1129-1135
28. Kalinowski, L., Dobrucki, I. T. and Malinski, T. (2002) Cerivastatin potentiates nitric oxide release and eNOS expression through inhibition of isoprenoids synthesis. J. Physiol. Pharmacol. 53, 585-595
29. Suzumura, K., Yashuhara, M., Tanaka, K., Odawara, A., Narita, H. and Suzuki, T. (1999) An in vitro study of the hydroxyl radical scavenging property of fluvastatin, and HMG-CoA reductase inhibitor. Chem. Pharm. Bull. 47, 1010-1012
30. Lane, P. and Gros, S. S. (2002) Disabling a C-terminal autoinhibitory control element in endothelial nitric-oxide synthase by phosphorylation provides a molecular explanation for activation of vascular NO synthesis by diverse physiological stimuli. J. Biol. Chem. 277, 19087-19094
31. Wu, H., Lu, D., Jiang, H., Xiong, Y., Qu, C. and Li, B. (2008) Increase in phosphorylation of Akt and its downstream signalling targets and suppression of apoptosis by simvastatin after traumatic brain injury. J. Neurosci. 109, 691-698
32. Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C., Busse, R. and Zeiher, A. M. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605
33. Luo, Z., Fujio, Y., Kureishi, Y., Rudic, R. D., Daumerie, G., Fulton, D., Sessa, W. C. and Walsh, K. (2000) Acute modulation of endothelial Akt/PKB activity alters nitric oxide-dependent vasomotor activity in vivo. J. Clin. Invest. 106, 493-499
34. Mukai, Y., Shimokawa, H., Matoba, T., Hiroki, J., Kunihiro, I., Fujiki, T. and Takeshita, A. (2003) Acute vasodilator effects of HMG-CoA reductase inhibitors: involvement of PI3-kinase/Akt pathway and Kv channels. J. Cardiovasc. Pharmacol. 42, 118-124
35. Hardie, D. G. and Carling, D. (1997) The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur. J. Biochem. 246, 259-273
36. Hawley, S. A., Davison, M., Woods, A., Davies, S. P., Beri, R. K., Carling, D. and Hardie, D. G. (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271, 27879-27887
37. 633.. Circ. Res. 104, 496-505
38. Kuo, R., Sartoretto, J. and Michel, T. (2009) Regulation of Rac1 by simvastatin in endothelial cells: differential roles of AMP-activated protein kinase and calmodulin-dependent kinase kinase-β. J. Biol. Chem. 284, 14734-14743
39. Caey, P. J. (1995) Mechanisms of protein prenylation and role in G protein function. Biochem. Soc. Trans. 23, 161-166
40. Rikitake, Y. and Liao, J. K. (2005) Rho GTPases, statins and nitric oxide. Circ. Res. 97, 1232-1235
41. Viollet, B., Mounier, R., Leclerc, J., Yazigi, A., Foretz, M. and Andreelli, F. (2007) Targeting AMP-activated protein kinase as a novel therapeutic approach for the treatment of metabolic disorders. Diabetes Metab. 33, 395-402
42. Towler, M. C. and Hardie, D. G. (2007) AMP-activated protein kinase in metabolic control and insulin signalling. Circ. Res. 100, 328-341
43. Haffner, S. M., Lehto, S., Rönnemaa, T., Pyörälä, K. and Laakso, M. (1998) Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N. Engl. J. Med. 339, 229-234
44. Cool, B., Zinker, B., Chiou, W., Kifle, L., Cao, N., Perham, M., Dickinson, R., Adler, A., Gagne, G., Iyengar, R. et al. (2006) Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab. 3, 403-416