Modification of endothelial nitric oxide synthase through AMPK after experimental subarachnoid hemorrhage

Journal of Neurotrauma

Volumn 26, Issue 7, 2009, Pages 1157-1165

  Osuka, Koji ^a   Watanabe, Yasuo ^b   Usuda, Nobuteru ^c   Atsuzawa, Kimie ^c   Yoshida, Jun ^d   Takayasu, Masakazu ^a  

^a AICHI MEDICAL UNIVERSITY   (Japan)

^b SHOWA PHARMACEUTICAL UNIVERSITY   (Japan)

^c FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

AMP activated protein kinase; Endothelial nitric oxide synthase; Subarachnoid hemorrhage

Indexed keywords

ADENYLATE KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; SERINE; THREONINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASILAR ARTERY; BRAIN BLOOD FLOW; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; MALE; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; UPREGULATION; WESTERN BLOTTING; ANALYSIS OF VARIANCE; ANIMAL; METABOLISM; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; TIME; VASCULAR ENDOTHELIUM;

ADENYLATE KINASE; ANALYSIS OF VARIANCE; ANIMALS; BASILAR ARTERY; BLOTTING, WESTERN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; IMMUNOHISTOCHEMISTRY; MALE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; TIME FACTORS;

EID: 69249098863     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0836     Document Type: Article

References (39)

1. Akiyama, M., Eguchi, D., Weiler, D., O'Brien, T., Kovesdi, I., Scotland, R.S., Sessa, W.C., and Katusic, Z.S. (2002). Expression and function of recombinant S1179D endothelial nitric oxide synthase in canine cerebral arteries. Stroke 33, 1071-1076. (Pubitemid 34293594)
2. Atochin, D.N., Wang, A., Liu, V.W., Critchlow, J.D., Dantas, A.P., Looft-Wilson, R., Murata, T., Salomone, S., Shin, H.K., Ayata, C., Moskowitz, M.A., Michel, T., Sessa, W.C., and Huang, P.L. (2007). The phosphorylation state of eNOS modulates vascular reactivity and outcome of cerebral ischemia in vivo. J. Clin. Invest. 117, 1961-1967.
3. Boo, Y.C., and Jo, H. (2003). Flow-dependent regulation of endothelial nitric oxide synthase: role of protein kinases. Am. J. Physiol. Cell Physiol. 285, C499-508.
4. Boo, Y.C., Sorescu, G., Boyd, N., Shiojima, I., Walsh, K., Du, J., and Jo, H. (2002). Shear stress stimulates phosphorylation of endothelial nitric-oxide synthase at Ser1179 by Akt-independent mechanisms: role of protein kinase A. J. Biol. Chem. 277, 3388-3396.
5. Calvert, J.W., Gundewar, S., Jha, S., Greer, J.J., Bestermann, W.H., Tian, R., and Lefer, D.J. (2008). Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 57, 696-705.
6. Chen, J., Zacharek, A., Zhang, C., Jiang, H., Li, Y., Roberts, C., Lu, M., Kapke, A., and Chopp, M. (2005). Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J. Neurosci. 25, 2366-2375. (Pubitemid 40322278)
7. 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. 443, 285-289. (Pubitemid 29080812)
8. 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. (Pubitemid 29279182)
9. Fisslthaler, B., Dimmeler, S., Hermann, C., Busse, R., and Fleming, I. (2000). Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol. Scand. 168, 81-88.
10. 2+/ calmodulin-dependent endothelial nitric oxide synthase activity. Circ. Res. 88, E68-75.
11. Fulton, D., Gratton, J.P., McCabe, T.J., Fontana, J., Fujio, Y., Walsh, K., Franke, T.F., Papapetropoulos, A., and Sessa, W.C. (1999). Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399, 597-601. (Pubitemid 29279181)
12. Gules, I., Satoh, M., Clower, B.R., Nanda, A., and Zhang, J.H. (2002). Comparison of three rat models of cerebral vasospasm. Am. J. Physiol. Heart Circ. Physiol. 283, H2551-2559.
13. Hardie, D.G. (2004). The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 117, 5479-5487.
14. Hashiguchi, A., Yano, S., Morioka, M., Hamada, J., Ushio, Y., Takeuchi, Y., and Fukunaga, K. (2004). Up-regulation of endothelial nitric oxide synthase via phosphatidylinositol 3-kinase pathway contributes to ischemic tolerance in the CA1 subfield of gerbil hippocampus. J. Cereb. Blood Flow Metab. 24, 271-279.
15. Hino, A., Tokuyama, Y., Weir, B., Takeda, J., Yano, H., Bell, G.I., and Macdonald, R.L. (1996). Changes in endothelial nitric oxide synthase mRNA during vasospasm after subarachnoid hemorrhage in monkeys. Neurosurgery 39, 562-567. (Pubitemid 26292030)
16. Huang, Z., Huang, P.L., Panahian, N., Dalkara, T., Fishman, M.C., and Moskowitz, M.A. (1994). Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885. (Pubitemid 24324247)
17. Ibrahim, J., Miyashiro, J.K., and Berk, B.C. (2003). Shear stress is differentially regulated among inbred rat strains. Circ. Res. 92, 1001-1009.
18. Jung, C.S., Oldfield, E.H., Harvey-White, J., Espey, M.G., Zimmermann, M., Seifert, V., and Pluta, R.M. (2007). Association of an endogenous inhibitor of nitric oxide synthase with cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage. J. Neurosurg. 107, 945-950. (Pubitemid 350255207)
19. Kasuya, H., Weir, B.K., Nakane, M., Pollock, J.S., Johns, L., Marton, L.S., and Stefansson, K. (1995). Nitric oxide synthase and guanylate cyclase levels in canine basilar artery after subarachnoid hemorrhage. J. Neurosurg. 82, 250-255.
20. Lynch, J.R., Wang, H., McGirt, M.J., Floyd, J., Friedman, A.H., Coon, A.L., Blessing, R., Alexander, M.J., Graffagnino, C., Warner, D.S., and Laskowitz, D.T. (2005). Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial. Stroke 36, 2024-2026. (Pubitemid 41266547)
21. McCullough, L.D., Zeng, Z., Li, H., Landree, L.E., McFadden, J., and Ronnett, G.V. (2005). Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J. Biol. Chem. 280, 20493-20502.
22. McGirt, M.J., Blessing, R., Alexander, M.J., Nimjee, S.M., Woodworth, G.F., Friedman, A.H., Graffagnino, C., Laskowitz, D.T., and Lynch, J.R. (2006). Risk of cerebral vasopasm after subarachnoid hemorrhage reduced by statin therapy: a multivariate analysis of an institutional experience. J. Neurosurg. 105, 671-674. (Pubitemid 44703927)
23. McGirt, M.J., Lynch, J.R., Parra, A., Sheng, H., Pearlstein, R.D., Laskowitz, D.T., Pelligrino, D.A., and Warner, D.S. (2002). Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 33, 2950-2956. (Pubitemid 35462871)
24. Michell, B.J., Chen, Z., Tiganis, T., Stapleton, D., Katsis, F., Power, D.A., Sim, A.T., and Kemp, B.E. (2001). Coordinated control of endothelial nitric-oxide synthase phosphorylation by protein kinase C and the cAMP-dependent protein kinase. J. Biol. Chem. 276, 17625-17628.
25. 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.
26. Mount, P.F., Hill, R.E., Fraser, S.A., Levidiotis, V., Katsis, F., Kemp, B.E., and Power, D.A. (2005). Acute renal ischemia rapidly activates the energy sensor AMPK but does not increase phosphorylation of eNOS-Ser1177. Am. J. Physiol. Renal Physiol. 289, F1103-1115.
27. Murata, H., Ihara, Y., Nakamura, H., Yodoi, J., Sumikawa, K., and Kondo, T. (2003). Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J. Biol. Chem. 278, 50226-50233.
28. Pluta, R.M. (2006). Dysfunction of nitric oxide synthases as a cause and therapeutic target in delayed cerebral vasospasm after SAH. Neurol. Res. 28, 730-737.
29. Pluta, R.M., Jung, C.S., Harvey-White, J., Whitehead, A., Shilad, S., Espey, M.G., and Oldfield, E.H. (2005). In vitro and in vivo effects of probucol on hydrolysis of asymmetric dimethyl L-arginine and vasospasm in primates. J. Neurosurg. 103, 731-738.
30. Pluta, R.M., Thompson, B.G., Dawson, T.M., Snyder, S.H., Boock, R.J., and Oldfield, E.H. (1996). Loss of nitric oxide synthase immunoreactivity in cerebral vasospasm. J. Neurosurg. 84, 648-654. (Pubitemid 26104234)
31. Richards, M.K., and Marletta, M.A. (1994). Characterization of neuronal nitric oxide synthase and a C415H mutant, purified from a baculovirus overexpression system. Biochemistry 33, 14723-14732.
32. Santhanam, A.V., Smith, L.A., Akiyama, M., Rosales, A.G., Bailey, K.R., and Katusic, Z.S. (2005). Role of endothelial NO synthase phosphorylation in cerebrovascular protective effect of recombinant erythropoietin during subarachnoid hemorrhage-induced cerebral vasospasm. Stroke 36, 2731-2737.
33. Sayama, T., Suzuki, S., and Fukui, M. (1999). Role of inducible nitric oxide synthase in the cerebral vasospasm after subarachnoid hemorrhage in rats. Neurol. Res. 21, 293-298.
34. 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.
35. Tseng, M.Y., Hutchinson, P.J., Czosnyka, M., Richards, H., Pickard, J.D., and Kirkpatrick, P.J. (2007). Effects of acute pravastatin treatment on intensity of rescue therapy, length of inpatient stay, and 6-month outcome in patients after aneurysmal subarachnoid hemorrhage. Stroke 38, 1545-1550. (Pubitemid 46684172)
36. Vallance, P., Leone, A., Calver, A., Collier, J., and Moncada, S. (1992). Endogenous dimethylarginine as an inhibitor of nitric oxide synthesis. J. Cardiovasc. Pharmacol. 20 Suppl 12, S60-62.
37. Widenka, D.C., Medele, R.J., Stummer, W., Bise, K., and Steiger, H.J. (1999). Inducible nitric oxide synthase: a possible key factor in the pathogenesis of chronic vasospasm after experimental subarachnoid hemorrhage. J. Neurosurg. 90, 1098-1104. (Pubitemid 29241179)
38. Yasukawa, T., Tokunaga, E., Ota, H., Sugita, H., Martyn, J.A., and Kaneki, M. (2005). S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance. J. Biol. Chem. 280, 7511-7518.
39. Zou, M.H., Hou, X.Y., Shi, C.M., Nagata, D., Walsh, K., and Cohen, R.A. (2002). Modulation by peroxynitrite of Akt- and AMP-activated kinase-dependent Ser1179 phosphorylation of endothelial nitric oxide synthase. J. Biol. Chem. 277, 32552-32557.