Simvastatin attenuation of cerebral vasospasm after subarachnoid hemorrhage in rats via increased phosphorylation of Akt and endothelial nitric oxide synthase

Journal of Neuroscience Research

Volumn 86, Issue 16, 2008, Pages 3635-3643

  Sugawara, Takashi ^a,b   Ayer, Robert ^a   Jadhav, Vikram ^a   Chen, Wanqiu ^a   Tsubokawa, Tamiji ^a   Zhang, John H ^a,c  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c LOMA LINDA UNIVERSITY   (United States)

Author keywords

Cerebral vasospasm; eNOS; Experimental subarachnoid hemorrhage; PI3K Akt; Statin

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SIMVASTATIN; WORTMANNIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTERY DIAMETER; ARTICLE; BRAIN VASOSPASM; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HISTOPATHOLOGY; INTERNAL CAROTID ARTERY; LOW DRUG DOSE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SUBARACHNOID HEMORRHAGE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; CAROTID STENOSIS; CEREBRAL ARTERIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ENZYME INHIBITORS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MALE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIMVASTATIN; SUBARACHNOID HEMORRHAGE; UP-REGULATION; VASOSPASM, INTRACRANIAL;

EID: 59349103744     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21807     Document Type: Article

References (44)

1. Baki L, Neve RL, Shao Z, Shioi J, Georgakopoulos A, Robakis NK. 2008. Wild-type but not FAD mutant presenilin-1 prevents neuronal degeneration by promoting phosphatidylinositol 3-kinase neuroprotective signaling. J Neurosci 28:483-490.
2. Barry KJ, Scott RM. 1979. Effect of intravenous ethanol on cerebral vasospasm produced by subarachnoid blood. Stroke 10:535-537.
3. Bederson JB, Germano IM, Guarino L. 1995. Cortical blood flow and cerebral perfusion pressure in a new noncraniotomy model of subarachnoid hemorrhage in the rat. Stroke 26:1086-1091.
4. Cahill J, Calvert JW, Solaroglu I, Zhang JH. 2006. Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37:1868-1874.
5. Czuriga I, Edes I. 2006. [Lowering cholesterol: how low is low enough?]. Orv Hetil 147:1349-1356.
6. de Oliveira JG, Beck J, Ulrich C, Rathert J, Raabe A, Seifert V. 2007. Comparison between clipping and coiling on the incidence of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a systematic review and meta-analysis. Neurosurg Rev 30:22-30.
7. Endres M, Laufs U, Huang Z, Nakamura T, Huang P, Moskowitz MA, Liao JK. 1998. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 95:8880-8885.
8. Erdos B, Snipes JA, Tulbert CD, Katakam P, Miller AW, Busija DW. 2006. Rosuvastatin improves cerebrovascular function in Zucker obese rats by inhibiting NAD(P)H oxidase-dependent superoxide production. Am J Physiol Heart Circ Physiol 290:H1264-H1270.
9. Gao F, Gao E, Yue TL, Ohlstein EH, Lopez BL, Christopher TA, Ma XL. 2002. Nitric oxide mediates the antiapoptotic effect of insulin in myocardial ischemia-reperfusion: the roles of PI3-kinase, Akt, and endothelial nitric oxide synthase phosphorylation. Circulation 105:1497-1502.
10. Garcia JH, Wagner S, Liu KF, Hu XJ. 1995. Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation. Stroke 26:627-634.
11. Ho FM, Lin WW, Chen BC, Chao CM, Yang CR, Lin LY, Lai CC, Liu SH, Liau CS. 2006. High glucose-induced apoptosis in human vascular endothelial cells is mediated through NF-kappaB and c-Jun NH2-terminal kinase pathway and prevented by PI3K/Akt/eNOS pathway. Cell Signal 18:391-399.
12. Jin KL, Mao XO, Nagayama T, Goldsmith PC, Greenberg DA. 2000. Induction of vascular endothelial growth factor receptors and phosphatidylinositol 3′-kinase/Akt signaling by global cerebral ischemia in the rat. Neuroscience 100:713-717.
13. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, Lefer DJ, Sessa WC, Walsh K. 2000. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med 6:1004-1010.
14. Kusaka G, Ishikawa M, Nanda A, Granger DN, Zhang JH. 2004. Signaling pathways for early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 24:916-925.
15. Laufs U, Liao JK. 1998. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem 273:24266-24271.
16. Liao JK, Laufs U. 2005. Pleiotropic effects of statins. Annu Rev Pharmacol Toxicol 45:89-118.
17. Laufs U, Fata VL, Liao JK. 1997. Inhibition of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase blocks hypoxia-mediated down-regulation of endothelial nitric oxide synthase. J Biol Chem 272:31725-31729.
18. Lynch JR, Wang H, McGirt MJ, Floyd J, Friedman AH, Coon AL, Blessing R, Alexander MJ, Graffagnino C, Warner DS, Laskowitz DT. 2005. Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial. Stroke 36:2024-2026.
19. McGirt MJ, Lynch JR, Parra A, Sheng H, Pearlstein RD, Laskowitz DT, Pelligrino DA, Warner DS. 2002. Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 33:2950-2956.
20. McGirt MJ, Blessing R, Alexander MJ, Nimjee SM, Woodworth GF, Friedman AH, Graffagnino C, Laskowitz DT, Lynch JR. 2006a. Risk of cerebral vasopasm after subarachnoid hemorrhage reduced by statin therapy: a multivariate analysis of an institutional experience. J Neurosurg 105:671-674.
21. McGirt MJ, Pradilla G, Legnani FG, Thai QA, Recinos PF, Tamargo RJ, Clatterbuck RE. 2006b. Systemic administration of simvastatin after the onset of experimental subarachnoid hemorrhage attenuates cerebral vasospasm. Neurosurgery 58:945-951.
22. Ostrowski RP, Colohan AR, Zhang JH. 2006a. Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol Res 28:399-414.
23. Ostrowski RP, Tang J, Zhang JH. 2006b. Hyperbaric oxygen suppresses NADPH oxidase in a rat subarachnoid hemorrhage model. Stroke 37:1314-1318.
24. Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH. 2004. Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 35:2412-2417.
25. Parra A, McGirt MJ, Sheng H, Laskowitz DT, Pearlstein RD, Warner DS. 2002. Mouse model of subarachnoid hemorrhage associated cerebral vasospasm: methodological analysis. Neurol Res 24:510-516.
26. -/-mice in vivo. Circulation 107:2480-2486.
27. Prager R. 1989. [Treatment of hyperlipidemia with HMG-CoA reductase inhibitors]. Wien Med Wochenschr Suppl 105:17-20.
28. Santhanam AV, Smith LA, Akiyama M, Rosales AG, Bailey KR, Katusic ZS. 2005. Role of endothelial NO synthase phosphorylation in cerebrovascular protective effect of recombinant erythropoietin during subarachnoid hemorrhage-induced cerebral vasospasm. Stroke 36:2731-2737.
29. Scott PA, Tremblay A, Brochu M, St.Louis J. 2007. Vasorelaxant action of 17-estradiol in rat uterine arteries: role of nitric oxide synthases and estrogen receptors. Am J Physiol Heart Circ Physiol 293:H3713-H3719.
30. Sehba FA, Bederson JB. 2006. Mechanisms of acute brain injury after subarachnoid hemorrhage. Neurol Res 28:381-398.
31. Shioda N, Ishigami T, Han F, Moriguchi S, Shibuya M, Iwabuchi Y, Fukunaga K. 2007. Activation of phosphatidylinositol 3-kinase/protein kinase B pathway by a vanadyl compound mediates its neuroprotective effect in mouse brain ischemia. Neuroscience 148:221-229.
32. Sugawara T, Ayer R, Jadhav V, Zhang JH. 2007. A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J Neurosci Methods 167:327-334.
33. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, Sena-Esteves M, Hiltunen M, Yang SH, Zhong Z, Shen Y, Simpkins JW, Tanzi RE. 2007. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54:721-737.
34. Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ. 2005. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke 36:1627-1632.
35. Tsubokawa T, Solaroglu I, Yatsushige H, Cahill J, Yata K, Zhang JH. 2006. Cathepsin and calpain inhibitor E64d attenuates matrix metalloproteinase-9 activity after focal cerebral ischemia in rats. Stroke 37:1888-1894.
36. Urbich C, Dernbach E, Zeiher AM, Dimmeler S. 2002. Double-edged role of statins in angiogenesis signaling. Circ Res 90:737-744.
37. van Groen T, Puurunen K, Maki HM, Sivenius J, Jolkkonen J. 2005. Transformation of diffuse beta-amyloid precursor protein and beta-amyloid deposits to plaques in the thalamus after transient occlusion of the middle cerebral artery in rats. Stroke 36:1551-1556.
38. Vauzour D, Vafeiadou K, Rice-Evans C, Williams RJ, Spencer JP. 2007. Activation of pro-survival Akt and ERK1/2 signalling pathways underlie the anti-apoptotic effects of flavanones in cortical neurons. J Neurochem 103:1355-1367.
39. Wang H, Wu YB, Du XH. 2005. Effect of dexamethasone on nitric oxide synthase and caspase-3 gene expressions in endotoxemia in neonate rat brain. Biomed Environ Sci 18:181-186.
40. Wang J, Tokoro T, Matsui K, Higa S, Kitajima I. 2005. Pitavastatin at low dose activates endothelial nitric oxide synthase through PI3K-AKT pathway in endothelial cells. Life Sci 76:2257-2268.
41. Wassmann S, Laufs U, Baumer AT, Muller K, Ahlbory K, Linz W, Itter G, Rosen R, Bohm M, Nickenig G. 2001. HMG-CoA reductase inhibitors improve endothelial dysfunction in normocholesterolemic hypertension via reduced production of reactive oxygen species. Hypertension 37:1450-1457.
42. Wolfrum S, Dendorfer A, Schutt M, Weidtmann B, Heep A, Tempel K, Klein HH, Dominiak P, Richardt G. 2004. Simvastatin acutely reduces myocardial reperfusion injury in vivo by activating the phosphatidylinositide 3-kinase/Akt pathway. J Cardiovasc Pharmacol 44:348-355.
43. Xie Z, Dong Y, Maeda U, Moir R, Inouye SK, Culley DJ, Crosby G, Tanzi RE. 2006. Isoflurane-induced apoptosis: a potential pathogenic link between delirium and dementia. J Gerontol A Biol Sci Med Sci 61:1300-1306.
44. Xie Z, Dong Y, Maeda U, Moir RD, Xia W, Culley DJ, Crosby G, Tanzi RE. 2007. The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid beta-protein accumulation. J Neurosci 27:1247-1254.