Statin effects on cholesterol micro-domains in brain plasma membranes

Biochemical Pharmacology

Volumn 65, Issue 5, 2003, Pages 843-856

  Kirsch, Christopher ^a   Eckert, Gunter P ^a   Mueller, Walter E ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Alzheimer's disease; Brain; Cholesterol; Lipids; Membrane; Statins

Indexed keywords

CHOLESTEROL; FLOTILLIN; MEMBRANE LIPID; MEVINOLIN; PRAVASTATIN; SIMVASTATIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN MEMBRANE; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SYNAPTOSOME; TISSUE DISTRIBUTION;

EID: 0037333737     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(02)01654-4     Document Type: Article

References (92)

1. Roher A.E., Kuo Y.M., Kokjohn K.M., Emmerling M.R., Gracon S. Amyloid and lipids in the pathology of Alzheimer disease. Amyloid. 6:1999;136-145.
2. Frears E.R., Stephens D.J., Walters C.E., Davies H., Austen B.M. The role of cholesterol in the biosynthesis of beta-amyloid. Neuroreport. 10:1999;1699-1705.
3. Bodovitz S., Klein W.L. Cholesterol modulates alpha-secretase cleavage of amyloid precursor protein. J. Biol. Chem. 271:1996;4436-4440.
4. Fassbender K., Simons M., Bergmann C., Stroick M., Lutjohann D., Keller P., Runz H., Kuhl S., Bertsch T., von Bergmann K., Hennerici M., Beyreuther K., Hartmann T. Simvastatin strongly reduces levels of Alzheimer's disease beta-amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5856-5861.
5. Wood W.G., Schroeder F., Avdulov N.A., Chochina S.V., Igbavboa U. Recent advances in brain cholesterol dynamics: transport, domains, and Alzheimer's disease. Lipids. 34:1999;225-234.
6. Simons M., Keller P., De Strooper B., Beyreuther K., Dotti C.G., Simons K. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 95:1998;6460-6464.
7. Czech C., Forstl H., Hentschel F., Monning U., Besthorn C., Geiger-Kabisch C., Sattel H., Masters C., Beyreuther K. Apolipoprotein E-4 gene dose in clinically diagnosed Alzheimer's disease: prevalence, plasma cholesterol levels and cerebrovascular change. Eur. Arch. Psychiatr. Clin. Neurosci. 243:1994;291-292.
8. Svennerholm L., Gottfries C.G. Membrane lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early-onset form (type I) and demyelination in late-onset form (type II). J. Neurochem. 62:1994;1039-1047.
9. Mason R.P., Shoemaker W.J., Shajenko L., Chambers T.E., Herbette L.G. Evidence for changes in the Alzheimer's disease brain cortical membrane structure mediated by cholesterol. Neurobiol. Aging. 13:1992;413-419.
10. Kakio A., Nishimoto S.S., Yanagisawa K., Kozutsumi Y., Matsuzaki K. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J. Biol. Chem. 276:2001;24985-24990.
11. Selkoe D.J. Alzheimer's disease: a central role for amyloid. J. Neuropathol. Exp. Neurol. 53:1994;438-447.
12. Bayer T.A., Wirths O., Majtenyi K., Hartmann T., Multhaup G., Beyreuther K., Czech C. Key factors in Alzheimer's disease: beta-amyloid precursor protein processing, metabolism and intraneuronal transport. Brain Pathol. 11:2001;1-11.
13. Hartmann H., Eckert A., Muller W.E. beta-Amyloid protein amplifies calcium signalling in central neurons from the adult mouse. Biochem. Biophys. Res. Commun. 194:1993;1216-1220.
14. Kawahara M., Kuroda Y. Molecular mechanism of neurodegeneration induced by Alzheimer's beta-amyloid protein: channel formation and disruption of calcium homeostasis. Brain Res. Bull. 53:2000;389-397.
15. Müller W.E., Kirsch C., Eckert G.P. Membrane-disordering effects of beta-amyloid peptides. Biochem. Soc. Trans. 29:2001;617-623.
16. Lousberg T.R., Denham A.M., Rasmussen J.R. A comparison of clinical outcome studies among cholesterol-lowering agents. Ann. Pharmacother. 35:2001;1599-1607.
17. Wolozin B., Kellman W., Rousseau P., Celesia G.G., Siegel G. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57:2000;1439-1443.
18. Jick H., Zornberg G.L., Jick S.S., Seshadri S., Drachman D.A. Statins and the risk of dementia. Lancet. 356:2000;1627-1631.
19. Hamelin B.A., Turgeon J. Hydrophilicity/lipophilicity: relevance for the pharmacology and clinical effects of HMG-CoA reductase inhibitors. Trends Pharmacol. Sci. 19:1998;26-37.
20. Guillot F., Misslin P., Lemaire M. Comparison of fluvastatin and lovastatin blood-brain barrier transfer using in vitro and in vivo methods. J. Cardiovasc. Pharmacol. 21:1993;339-346.
21. Saheki A., Terasaki T., Tamai I., Tsuji A. In vivo and in vitro blood-brain barrier transport of 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase inhibitors. Pharm. Res. 11:1994;305-311.
22. Botti R.E., Triscari J., Pan H.Y., Zayat J. Concentrations of pravastatin and lovastatin in cerebrospinal fluid in healthy subjects. Clin. Neuropharmacol. 14:1991;256-261.
23. Komai T., Shigehara E., Tokui T., Koga T., Ishigami M., Kuroiwa C., Horiuchi S. Carrier-mediated uptake of pravastatin by rat hepatocytes in primary culture. Biochem. Pharmacol. 43:1992;667-670.
24. Dietschy J.M., Turley S.D. Cholesterol metabolism in the brain. Curr. Opin. Lipidol. 12:2001;105-112.
25. Hartmann T. Cholesterol, A beta and Alzheimer's disease. Trends Neurosci. 24:2001;S45-S48.
26. Kojro E., Gimpl G., Lammich S., Marz W., Fahrenholz F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5815-5820.
27. Marx J. Alzheimer's disease: bad for the heart, bad for the mind? Science. 294:2001;508-509.
28. Golde T.E., Eckman C.B. Cholesterol modulation as an emerging strategy for the treatment of Alzheimer's disease. Drug Discov. Today. 6:2001;1049-1055.
29. Wolozin B. A fluid connection: cholesterol and A beta. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5371-5373.
30. Refolo L.M., Pappolla M.A., LaFrancois J., Malester B., Schmidt S.D., Thomas-Bryant T., Tint G.S., Wang R., Mercken M., Petanceska S.S., Duff K.E. A Cholesterol-lowering drug reduces beta-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 8:2001;890-899.
31. Shie F.S., Jin L.W., Cook D.G., Leverenz J.B., LeBoeuf R.C. Diet-induced hypercholesterolemia enhances brain Abeta accumulation in transgenic mice. Neuroreport. 13:2002;455-459.
32. Doggrell S.A. Statins in the 21st century: end of the simple story? Expert Opin. Invest. Drugs. 10:2001;1755-1766.
33. Desager J.P., Horsmans Y. Clinical pharmacocinetics of 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors. Clin. Pharmacokinet. 31:1996;348-371.
34. Bellosta S., Ferri N., Bernini F., Paoletti R., Corsini A. Non-lipid-related effects of statins. Ann. Med. 32:2000;164-176.
35. Takemoto M., Liao J.K. Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitors. Arterioscler. Thromb. Vasc. Biol. 21:2001;1712-1719.
36. Corsini A., Bernini F., Quarato P., Donetti E., Bellosta S., Fumagalli R., Paoletti R., Soma V.M. Non-lipid-related effects of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Cardiology. 87:1996;458-468.
37. Cucchiara B., Kasner S.E. Use of statins in CNS disorders. J. Neurol. Sci. 187:2001;81-89.
38. Bonetta L. Potential neurological value of statins increases. Nat. Med. 8:2002;541.
39. Liscum L., Dahl N.K. Intracellular cholesterol transport. J. Lipid Res. 33:1992;1239-1254.
40. Simons K., Ikonen E. How cells handle cholesterol. Science. 290:2000;1721-1726.
41. Schroeder F., Woodford J.K., Kavecansky J., Wood W.G., Joiner C. Cholesterol domains in biological membranes. Mol. Membr. Biol. 12:1995;113-119.
42. Runz H., Rietdorf J., Tomic I., de Bernard M., Beyreuther K., Pepperkok R., Hartmann T. Inhibition of intracellular cholesterol transport alters presenilin localization and amyloid precursor protein processing in neuronal cells. J. Neurosci. 22:2002;1679-1689.
43. Liu Y., Peterson D.A., Schubert D. Amyloid beta peptide alters intracellular vesicle trafficking and cholesterol homeostasis. Proc. Natl. Acad. Sci. U.S.A. 95:1998;13266-13271.
44. Puglielli L., Konopka G., Pack-Chung E., Ingano L.A., Berezovska O., Hyman B.T., Chang T.Y., Tanzi R.E., Kovacs D.M. Acyl-coenzyme A: cholesterol acyltransferase modulates the generation of the amyloid beta-peptide. Nat. Cell Biol. 3:2001;905-912.
45. Eckert G.P., Kirsch C., Mueller W.E. Differential effects of lovastatin treatment on brain cholesterol levels in normal and apoE-deficient mice. Neuroreport. 12:2001;883-887.
46. Locatelli S., Lutjohann D., Schmidt H.H., Otto C., Beisiegel U., von Bergmann K. Reduction of plasma 24S-hydroxycholesterol (cerebrosterol) levels using high-dosage simvastatin in patients with hypercholesterolemia: evidence that simvastatin affects cholesterol metabolism in the human brain. Arch. Neurol. 59:2002;213-216.
47. Bjorkhem I., Lutjohann D., Diczfalusy U., Stahle L., Ahlborg G., Wahren J. Cholesterol homeostasis in human brain: turnover of 24S-hydroxycholesterol and evidence for a cerebral origin of most of this oxysterol in the circulation. J. Lipid Res. 39:1998;1594-1600.
48. Hayashi H., Igbavboa U., Hamanaka H., Kobayashi M., Fujita S.C., Wood W.G., Yanagisawa K. Cholesterol is increased in the exofacial leaflet of synaptic plasma membranes of human apolipoprotein E4 knock-in mice. Neuroreport. 13:2002;383-386.
49. Cardenas-Vazquez J.C.R., Martinez F.M.A. Comparative toxicity of high doses of vastatins currently used by clinicians, in CD-1 male mice fed with a hypercholesterolemic diet. Life Sci. 65:1999;947-956.
50. Eckert G.P., Wood W.G., Muller W.E. Effects of aging and beta-amyloid on the properties of brain synaptic and mitochondrial membranes. J. Neural. Transm. 108:2001;1051-1064.
51. Igbavboa U., Avdulov N.A., Schroeder F., Wood W.G. Increasing age alters transbilayer fluidity and cholesterol asymmetry in synaptic plasma membranes of mice. J. Neurochem. 66:1996;1717-1725.
52. Schroeder F., Nemecz G., Wood W.G., Joiner C., Morrot G., Ayraut-Jarrier M., Devaux P.F. Transmembrane distribution of sterol in the human erythrocyte. Biochim. Biophys. Acta. 1066:1991;183-192.
53. Schmalzing G., Kutschera P. Modulation of ATPase activities of human erythrocyte membranes by free fatty acids or phospholipase A2. J. Membr. Biol. 69:1982;65-76.
54. Schroeder F., Frolov A.A., Murphy E.J., Atshaves B.P., Jefferson J.R., Pu L., Wood W.G., Foxworth W.B., Kier A.B. Recent advances in membrane cholesterol domain dynamics and intracellular cholesterol trafficking. Proc. Soc. Exp. Biol. Med. 213:1996;150-177.
55. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:1951;265-275.
56. Schroeder F., Morrison W.J., Gorka C., Wood W.G. Transbilayer effects of ethanol on fluidity of brain membrane leaflets. Biochim. Biophys. Acta. 946:1988;85-94.
57. Kaiser R.D., London E. Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth. Biochemistry. 37:1998;8180-8190.
58. Lentz B.R. Use of fluorescent probes to monitor molecular order and motions within liposome bilayers. Chem. Phys. Lipids. 64:1993;99-116.
59. Weber G. Resolution of heterogeneous fluorescence from proteins and aromatic amino acids by phase-sensitive detection of fluorescence. Biochem. J. 51:1952;145-167.
60. Sweet W.D., Schroeder F. Plasma membrane lipid composition modulates action of anesthetics. Biochim. Biophys. Acta. 861:1986;53-61.
61. Sweet W.D., Schroeder F. Charged anaesthetics alter LM-fibroblast plasma-membrane enzymes by selective fluidization of inner or outer membrane leaflets. Biochem. J. 239:1986;301-310.
62. Mulders F., van Langen H., van Ginkel G., Levine Y.K. Effects of steroid molecules on the dynamical structure of dioleoylphosphatidylcholine and digalactosyldiacylglycerol bilayers. Biochim. Biophys. Acta. 859:1986;209-218.
63. Macdonald A.G., Wahle K.W., Cossins A.R., Behan M.K. Temperature, pressure and cholesterol effects on bilayer fluidity a comparison of pyrene excimer/monomer ratios with the steady-state fluorescence polarization of diphenylhexatriene in liposomes and microsomes. Biochim. Biophys. Acta. 938:1988;231-242.
64. Eckert GP, Igbavboa U, Müller WE, Wood WG. Lipid rafts of purified mouse brain synaptosomes prepared with or without detergent reveal different lipid and protein domains. Brain Res 2002; in press.
65. Kirsch C., Eckert G.P., Müller W.E. Cholesterol attenuates the membrane perturbing properties of β-amyloid peptides. Amyloid. 9:2002;149-159.
66. Auerbach B.J., Parks J.S., Applebaum-Bowden D. A rapid and sensitive micro-assay for the enzymatic determination of plasma and lipoprotein cholesterol. J. Lipid Res. 31:1990;738-742.
67. Chalvardjian A., Rudnicki E. Determination of lipid phosphorus in the nanomolar range. Anal. Biochem. 36:1970;225-226.
68. Krause B.R., Princen H.M. Lack of predictability of classical animal models for hypolipidemic activity: a good time for mice? Atherosclerosis. 140:1998;15-24.
69. Schroeder F., Gallegos A.M., Atshaves B.P., Storey S.M., McIntosh A.L., Petrescu A.D., Huang H., Starodub O., Chao H., Yang H., Frolov A., Kier A.B. Recent advances in membrane microdomains: rafts, caveolae, and intracellular cholesterol trafficking. Exp. Biol. Med. (Maywood). 226:2001;873-890.
70. Simons K., Toomre D. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:2000;31-39.
71. Riddell D.R., Christie G., Hussain I., Dingwall C. Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr. Biol. 11:2001;1288-1293.
72. Bernini F., Didoni G., Bonfadini G., Bellosta S., Fumagalli R. Requirement for mevalonate in acetylated LDL induction of cholesterol esterification in macrophages. Atherosclerosis. 104:1993;19-26.
73. Yamazaki T., Chang T.Y., Haass C., Ihara Y. Accumulation and aggregation of amyloid beta-protein in late endosomes of Niemann-pick type C cells. J. Biol. Chem. 276:2001;4454-4460.
74. Wood WG, Eckert GP, Igbavboa U, Müller WE. Amyloid beta-peptide interactions with membranes and cholesterol: causes and causalities of Alzheimer's disease. Biochim Biophys Acta 2002; in press.
75. Eckert G.P., Cairns N.J., Maras A., Gattaz W.F., Muller W.E. Cholesterol modulates the membrane-disordering effects of beta-amyloid peptides in the hippocampus: specific changes in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 11:2000;181-186.
76. Igbavboa U., Avdulov N.A., Chochina S.V., Wood W.G. Transbilayer distribution of cholesterol is modified in brain synaptic plasma membranes of knockout mice deficient in the low-density lipoprotein receptor, apolipoprotein E, or both proteins. J. Neurochem. 69:1997;1661-1667.
77. Skoog I. Vascular aspects in Alzheimer's disease. J. Neural. Transm. Suppl. 59:2000;37-43.
78. Endres M., Laufs U., Huang Z., Nakamura T., Huang P., Moskowitz M.A., Liao J.K. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 95:1998;8880-8885.
79. Kivipelto M., Helkala E.L., Laakso M.P., Hanninen T., Hallikainen M., Alhainen K., Soininen H., Tuomilehto J., Nissinen A. Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. Br. Med. J. 322:2001;1447-1451.
80. Kalaria R.N., Ballard C. Overlap between pathology of Alzheimer disease and vascular dementia. Alzheimer Dis. Assoc. Disord. 13(Suppl. 3):1999;S115-S123.
81. Das U.N. Essential fatty acids as possible mediators of the actions of statins. Prostaglandins Leukot. Essent. Fatty Acids. 65:2001;37-40.
82. Colton C.A., Brown C.M., Czapiga M., Vitek M.P. Apolipoprotein-E allele-specific regulation of nitric oxide production. Ann. NY Acad. Sci. 962:2002;212-225.
83. Meresse S., Delbart C., Fruchart J.C., Cecchelli R. Low-density lipoprotein receptor on endothelium of brain capillaries. J. Neurochem. 53:1989;340-345.
84. Wolozin B. Cholesterol and Alzheimer's disease. Biochem. Soc. Trans. 30:2002;525-529.
85. Igbavboa U., Hamilton J., Kim H.Y., Sun G.Y., Wood W.G. A new role for apolipoprotein E: modulating transport of polyunsaturated phospholipid molecular species in synaptic plasma membranes. J. Neurochem. 80:2002;255-261.
86. Kabouridis P.S., Janzen J., Magee A.L., Ley S.C. Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur. J. Immunol. 30:2000;954-963.
87. Hao M., Mukherjee S., Maxfield F.R. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc. Natl. Acad. Sci. U.S.A. 98:2001;13072-13077.
88. Wahrle S., Das P., Nyborg A.C., McLendon C., Shoji M., Kawarabayashi T., Younkin L.H., Younkin S.G., Golde T.E. Cholesterol-dependent gamma-secretase activity in buoyant cholesterol-rich membrane microdomains. Neurobiol. Dis. 9:2002;11-23.
89. Sidera C, Frimpong-Manso J, Liu C, Austen BM. The role of cholesterol in the processing of beta-secretase Asp-2. In: Korczyn AD, editor. Proceedings of the 2nd International Congress on Vascular Dementia, Salzburg, Austria. Monduzzi Editore, International Proceedings Division; 2002. p. 147-53.
90. Slotte J.P. Cholesterol-sphingomyelin interactions in cells - effects on lipid metabolism. Subcell. Biochem. 28:1997;277-293.
91. Feron O., Dessy C., Desager J.P., Balligand J.L. Hydroxy-methylglutaryl-coenzyme A reductase inhibition promotes endothelial nitric oxide synthase activation through a decrease in caveolin abundance. Circulation. 103:2001;113-118.
92. Accad M., Smith S.J., Newland D.L., Sanan D.A., King L.E. Jr., Linton M.F., Fazio S. Massive xanthomatosis and altered composition of atherosclerotic lesions in hyperlipidemic mice lacking acyl CoA:cholesterol acyltransferase 1. J. Clin. Invest. 105:2000;711-719.