Simvastatin enhances hippocampal long-term potentiation in C57BL/6 mice

Neuroscience

Volumn 166, Issue 2, 2010, Pages 435-444

  Mans, R A ^a,b   Chowdhury, N ^b   Cao, D ^b   Mcmahon, L L ^a,c   Li, L ^a,b  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Alzheimer's disease; Cognitive function; Learning and memory; Protein phosphorylation; Statins; Synaptic plasticity

Indexed keywords

PROTEIN KINASE B; SIMVASTATIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; COGNITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; IN VITRO STUDY; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOLECULAR DYNAMICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; TREATMENT RESPONSE; ANIMAL; C57BL MOUSE; DRUG EFFECT; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; METABOLISM; NONPARAMETRIC TEST; PHOSPHORYLATION; TIME; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIMVASTATIN; STATISTICS, NONPARAMETRIC; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 77951887071     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.12.062     Document Type: Article

References (48)

1. Balduini W, Mazzoni E, Carloni S, De Simoni MG, Perego C, Sironi L, Cimino M (2003) Prophylactic but not delayed administration of simvastatin protects against long-lasting cognitive and morphological consequences of neonatal hypoxic-ischemic brain injury, reduces interleukin-1beta and tumor necrosis factor-alpha mRNA induction, and does not affect endothelial nitric oxide synthase expression. Stroke 34:2007-2012.
2. Bosel J, Gandor F, Harms C, Synowitz M, Harms U, Djoufack PC, Megow D, Dirnagl U, Hortnagl H, Fink KB, Endres M (2005) Neuroprotective effects of atorvastatin against glutamate-induced excitotoxicity in primary cortical neurones. J Neurochem 92:1386- 1398.
3. Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232:34-47.
4. Buxbaum JD, Cullen EI, Friedhoff LT (2002) Pharmacological concentrations of the HMG-CoA reductase inhibitor lovastatin decrease the formation of the Alzheimer beta-amyloid peptide in vitro and in patients. Front Biosci 7:a50-a59.
5. Chen J, Zhang ZG, Li Y, Wang Y, Wang L, Jiang H, Zhang C, Lu M, Katakowski M, Feldkamp CS, Chopp M (2003) Statins induce angiogenesis, neurogenesis, and synaptogenesis after stroke. Ann Neurol 53:743-751.
6. Clarke RM, Lyons A, O'Connell F, Deighan BF, Barry CE, Anyakoha NG, Nicolaou A, Lynch MA (2008) A pivotal role for interleukin-4 in atorvastatin-associated neuroprotection in rat brain. J Biol Chem 283:1808-1817.
7. Clarke RM, O'Connell F, Lyons A, Lynch MA (2007) The HMG-CoA reductase inhibitor, atorvastatin, attenuates the effects of acute administration of amyloid-beta1-42 in the rat hippocampus in vivo. Neuropharmacology 52:136-145.
8. Collins R, Armitage J, Parish S, Sleight P, Peto R (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.
9. Cordle A, Landreth G (2005) 3-Hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors attenuate beta-amyloid-induced microglial inflammatory responses. J Neurosci 25:299-307.
10. Costa AC, Grybko MJ (2005) Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci Lett 382:317-322.
11. Endo A (2004) The discovery and development of HMG-CoA reductase inhibitors 1992. Atherosclerosis Suppl 5:67-80.
12. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143.
13. Fassbender K, Stroick M, Bertsch T, Ragoschke A, Kuehl S, Walter S, Walter J, Brechtel K, Muehlhauser F, Von Bergmann K, Lutjohann D (2002) Effects of statins on human cerebral cholesterol metabolism and secretion of Alzheimer amyloid peptide. Neurology 59: 1257-1258.
14. Hoffman DA, Sprengel R, Sakmann B (2002) Molecular dissection of hippocampal theta-burst pairing potentiation. Proc Natl Acad Sci U S A 99:7740-7745.
15. Hoglund K, Syversen S, Lewczuk P, Wallin A, Wiltfang J, Blennow K (2005) Statin treatment and a disease-specific pattern of betaamyloid peptides in Alzheimer's disease. Exp Brain Res 164:205- 214.
16. Hoglund K, Wiklund O, Vanderstichele H, Eikenberg O, Vanmechelen E, Blennow K (2004) Plasma levels of beta-amyloid(1-40), betaamyloid(1-42), and total beta-amyloid remain unaffected in adult patients with hypercholesterolemia after treatment with statins. Arch Neurol 61:333-337.
17. Jick H, Zornberg GL, Jick SS, Seshadri S, Drachman DA (2000) Statins and the risk of dementia. Lancet 356:1627-1631.
18. Jones PH (2003) Comparing HMG-CoA reductase inhibitors. Clin Cardiol 26:I15-I20.
19. Kotti T, Head DD, McKenna CE, Russell DW (2008) Biphasic requirement for geranylgeraniol in hippocampal long-term potentiation. Proc Natl Acad Sci U S A 105:11394-11399.
20. Kotti TJ, Ramirez DM, Pfeiffer BE, Huber KM, Russell DW (2006) Brain cholesterol turnover required for geranylgeraniol production and learning in mice. Proc Natl Acad Sci U S A 103:3869-3874.
21. Kuenzi FM, Fitzjohn SM, Morton RA, Collingridge GL, Seabrook GR (2000) Reduced long-term potentiation in hippocampal slices prepared using sucrose-based artificial cerebrospinal fluid. J Neurosci Methods 100:117-122.
22. 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.
23. Li L, Cao D, Kim H, Lester R, Fukuchi K (2006) Simvastatin enhances learning and memory independent of amyloid load in mice. Ann Neurol 60:729-739.
24. Liao JK (2002) Isoprenoids as mediators of the biological effects of statins. J Clin Invest 110:285-288.
25. Lisman J (2003) Long-term potentiation: outstanding questions and attempted synthesis. Philos Trans R Soc Lond B Biol Sci 358: 829-842.
26. Lu C, Mattson MP (2001) Dimethyl sulfoxide suppresses NMDA- and AMPA-induced ion currents and calcium influx and protects against excitotoxic death in hippocampal neurons. Exp Neurol 170:180-185.
27. Lu D, Qu C, Goussev A, Jiang H, Lu C, Schallert T, Mahmood A, Chen J, Li Y, Chopp M (2007a) Statins increase neurogenesis in the dentate gyrus, reduce delayed neuronal death in the hippocampal CA3 region, and improve spatial learning in rat after traumatic brain injury. J Neurotrauma 24:1132-1146.
28. Lu Y, Allen M, Halt AR, Weisenhaus M, Dallapiazza RF, Hall DD, Usachev YM, McKnight GS, Hell JW (2007b) Age-dependent requirement of AKAP150-anchored PKA and GluR2-lacking AMPA receptors in LTP. EMBO J 26:4879-4890.
29. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21.
30. Nakao T, Shiota M, Tatemoto Y, Izumi Y, Iwao H (2007) Pravastatin induces rat aortic endothelial cell proliferation and migration via activation of PI3K/Akt/mTOR/p70 S6 kinase signaling. J Pharmacol Sci 105:334-341.
31. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23:3679-3688.
32. Pooler AM, Xi SC, Wurtman RJ (2006) The 3-hydroxy-3-methylglutaryl co-enzyme A reductase inhibitor pravastatin enhances neurite outgrowth in hippocampal neurons. J Neurochem 97:716-723.
33. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22:3359-3365.
34. Sawada M, Sato M (1975) The effect of dimethyl sulfoxide on the neuronal excitability and cholinergic transmission in Aplysia ganglion cells. Ann N Y Acad Sci 243:337-357.
35. Shepherd J, Blauw GJ, Murphy MB, Bollen EL, Buckley BM, Cobbe SM, Ford I, Gaw A, Hyland M, Jukema JW, Kamper AM, Macfarlane PW, Meinders AE, Norrie J, Packard CJ, Perry IJ, Stott DJ, Sweeney BJ, Twomey C, Westendorp RG (2002) Pravastatin in elderly individuals at risk of vascular disease (PROSPER): a randomised controlled trial. Lancet 360:1623-1630.
36. Simons M, Schwarzler F, Lutjohann D, von Bergmann K, Beyreuther K, Dichgans J, Wormstall H, Hartmann T, Schulz JB (2002) Treatment with simvastatin in normocholesterolemic patients with Alzheimer's disease: a 26-week randomized, placebo-controlled, double-blind trial. Ann Neurol 52:346-350.
37. Sjogren M, Gustafsson K, Syversen S, Olsson A, Edman A, Davidsson P, Wallin A, Blennow K (2003) Treatment with simvastatin in patients with Alzheimer's disease lowers both alpha- and betacleaved amyloid precursor protein. Dement Geriatr Cogn Disord 16:25-30.
38. Skaletz-Rorowski A, Lutchman M, Kureishi Y, Lefer DJ, Faust JR, Walsh K (2003) HMG-CoA reductase inhibitors promote cholesterol-dependent Akt/PKB translocation to membrane domains in endothelial cells. Cardiovasc Res 57:253-264.
39. Smith CC, McMahon LL (2005) Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J Neurosci 25:7780-7791.
40. Smith CC, McMahon LL (2006) Estradiol-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26:8517-8522.
41. Sparks DL, Sabbagh MN, Connor DJ, Lopez J, Launer LJ, Browne P, Wasser D, Johnson-Traver S, Lochhead J, Ziolwolski C (2005) Atorvastatin for the treatment of mild to moderate Alzheimer disease: preliminary results. Arch Neurol 62:753-757.
42. Tsvyetlynska NA, Hill RH, Grillner S (2005) Role of AMPA receptor desensitization and the side effects of a DMSO vehicle on reticulospinal EPSPs and locomotor activity. J Neurophysiol 94:3951- 3960.
43. Vaughan CJ (2003) Prevention of stroke and dementia with statins: effects beyond lipid lowering. Am J Cardiol 91:23B-29B.
44. Wolozin B, Kellman W, Ruosseau P, Celesia GG, Siegel G (2000) Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch Neurol 57:1439-1443.
45. Wolozin B, Wang SW, Li NC, Lee A, Lee TA, Kazis LE (2007) Simvastatin is associated with a reduced incidence of dementia and Parkinson's disease. BMC Med 5:20.
46. Wu H, Lu D, Jiang H, Xiong Y, Qu C, Li B, Mahmood A, Zhou D, Chopp M (2008) Simvastatin-mediated upregulation of VEGF and BDNF, activation of the PI3K/Akt pathway, and increase of neurogenesis are associated with therapeutic improvement after traumatic brain injury. J Neurotrauma 25:130-139.
47. Yasuda H, Barth AL, Stellwagen D, Malenka RC (2003) A developmental switch in the signaling cascades for LTP induction. Nat Neurosci 6:15-16.
48. Zacco A, Togo J, Spence K, Ellis A, Lloyd D, Furlong S, Piser T (2003) 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors protect cortical neurons from excitotoxicity. J Neurosci 23:11104- 11111.