Cholesterol: From heart attacks to Alzheimer's disease

Journal of Lipid Research

Volumn 44, Issue 8, 2003, Pages 1423-1430

  Raffaï, Robert L ^a   Weisgraber, Karl H ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

24 hydroxycholesterol; 24S cholesterol hydroxylase; Alzheimer's disease; Amyloid precursor protein; Amyloid peptide; Apolipoprotein E

Indexed keywords

AMYLOID BETA PROTEIN; CELL PROTEIN; CHOLESTEROL; PROTEINASE;

ALZHEIMER DISEASE; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; HEART INFARCTION; HOMEOSTASIS; HUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; REVIEW;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; APOLIPOPROTEINS E; CHOLESTEROL; MYOCARDIAL INFARCTION; STEROID HYDROXYLASES;

EID: 0142105914     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.R300007-JLR200     Document Type: Review

References (74)

1. Hardy, J., and D.J. Selkoe. 2002. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science. 297: 353-356.
2. Golde, T. E. 2003. Alzheimer disease therapy: Can the amyloid cascade be halted? J. Clin. Invest. 111: 11-18.
3. Selkoe, D.J. 2001. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid β-protein. J. Alzheimers Dis. 3: 75-80.
4. Kojro, E., G. Gimpl, S. Lammich, W. März, and F. Fahrenholz. 2001. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM 10. Proc. Natl. Acad. Sci. USA. 98: 5815-5820.
5. Bodovitz, S., and W. L. Klein. 1996. Cholesterol modulates α-secretase cleavage of amyloid precursor protein. J. Biol. Chem. 271: 4436-4440.
6. Vassar, R., B. D. Bennett, S. Babu-Khan, S. Kahn, E. A. Mendiaz, P. Denis, D. B. Teplow, S. Ross, P. Amarante, R. Loeloff, Y. Luo, S. Fisher, J. Fuller, S. Edenson, J. Lile, M. A. Jarosinski, A. L. Biere, E. Curran, T. Burgess, J-C. Louis, F. Collins, J. Treanor, G. Rogers, and M. Citron. 1999. β-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 286: 735-741.
7. Li, Y.-M., M.-T Lai, M. Xu, Q. Huang, J. DiMuzio-Mower, M. K. Sardana, X.-P. Shi, K.-C. Yin, J. A. shafer, and S. J. Gardell. 2000. Presenilin 1 is linked with γ-secretase activity in the detergent solubilized state. Proc. Natl. Acad. Sci. USA. 97: 6138-6143.
8. Greenfield, J. P., J. Tsai, G. K. Gouras, B. Hai, G. Thinakaran, F. Checler, S. S. Sisodia, P. Greengard, and H. Xu. 1999. Endoplasmic reticulum and trans-Golgi network generate distinct populations of Alzheimer β-amyloid peptides. Proc. Natl. Acad. Sci. USA. 96:742-747.
9. Jarrett, J. T., E. P. Berger, and P. T. Lansbury, Jr. 1993. The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: Implications for the pathogenesis of Alzheimer's disease. Biochemistry. 32: 4693-4697.
10. Savage, M. J., S. P. Trusko, D. S. Howland, L. R. Pinsker, S. Mistretta, A. G. Reaume, B. D. Greenberg, R. Siman, and R. W. Scott. 1998. Turnover of amyloid β-protein in mouse brain and acute reduction of its level by phorbol ester. J. Neurosci. 18: 1743-1752.
11. Selkoe, D. J. 2001. Clearing the brain's amyloid cobwebs. Neuron. 32:177-180.
12. 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA. 95: 6448-6453.
13. Walsh, D. M., D. M. Hartley, Y. Kusumoto, Y. Fezoui, M. M. Condron, A. Lomakin, G. B. Benedek, D. J. Selkoe, and D. B. Teplow. 1999. Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274: 25945-25952.
14. Hsia, A. Y., E. Masliah, L. McConlogue, G-Q. Yu, G. Tatsuno, K. Hu, D. Kholodenko, R. C. Malenka, R. A. Nicoll, and L. Mucke. 1999. Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc. Natl. Acad. Sci. USA. 96: 3228-3233.
15. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J. Neurosci. 20: 4050-4058.
16. Buttini, M., G-Q. Yu, K. Shockley, Y. Huang, B. Jones, E. Masliah, M. Mallory, T. Yeo, F. M. Longo, and L. Mucke. 2002. Modulation of Alzheimer-like synaptic and cholinergic deficits in transgenic mice by human apolipoprotein E depends on isoform, aging, and overexpression of amyloid β peptides but not on plaque formation. J. Neurosci. 22: 10539-10548.
17. Walsh, D. M., I. Klyubin, J. V. Fadeeva, W. K. Cullen, R. Anwyl, M. S. Wolfe, M.J. Rowan, and D.J. Selkoe. 2002. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 416: 535-539.
18. Jarvik, G. P., E. M. Wijsman, W. A. Kukull, G. D. Schellenberg, C. Yu, and E. B. Larson. 1995. Interactions of apolipoprotein E genotype, total cholesterol level, age, and sex in prediction of Alzheimer's disease: A case-control study. Neurology. 45: 1092-1096.
19. Kuo, Y-M., M. R. Emmerling, C. L. Bisgaier, A. D. Essenburg, H. C. Lampert, D. Drumm, and A. E. Roher. 1998. Elevated low-density lipoprotein in Alzheimer's disease correlates with brain Aβ1-42 levels. Biochem. Biophys. Res. Commun. 252: 711-715.
20. Wolozin, B., W. Kellman, P. Ruosseau, G. G. Celesia, and G. Siegel. 2000. Decreased prevalence of Alzheimer disease associated with 3- hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57: 1439-1443.
21. Jick, H., G. L. Zornberg, S. S. Jick, S. Seshadri, and D. A. Drachman. 2000. Statins and the risk of dementia. Lancet. 356: 1627-1631.
22. Sparks, D. L., S. W. Scheff, J. C. Hunsaker, H. Liu, T. Landers, and D. R. Gross. 1994. Induction of Alzheimer-like β-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol. Exp. Neurol. 126: 88-94.
23. Refolo, L. M., M. A. Pappolla, B. Malester, J. LaFrancois, T. Bryant-Thomas, R. Wang, G. S. Tint, K. Sambamurti, and K. Duff. 2000. Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol. Dis. 7: 321-331.
24. Shie, F-S., L-W. Jin, D. G. Cook, J. B. Leverenz, and R. C. LeBoeuf. 2002. Diet-induced hypercholesterolemia enhances brain Aβ accumulation in transgenic mice. Neroreport. 13: 455-459.
25. Fullerton, S. M., G. A. Shirman, W. J. Strittmatter, and W. D. Matthew. 2001. Impairment of the blood-nerve and blood-brain barriers in apolipoprotein E knockout mice. Exp. Neurol. 169: 13-22.
26. Fassbender, K., M. Simons, C. Bergmann, M. Stroick, D. Lütjohann, P. Keller, H. Runz, S. Kühl, T. Bertsch, K. von Bergmann, M. Hennerici, K. Beyreuther, and T. Hartmann. 2001. Simvastatin strongly reduces levels of Alzheimer's disease β-amyloid peptides Aβ42 and Aβ40 in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 98: 5856-5861.
27. Lee, S-J., U. Liyanage, P. E. Bickel, W. Xia, P. T. Lansbury, Jr., and K. S. Kosik. 1998. A detergent-insoluble membrane compartment contains Aβ in vivo. Nat. Med. 4: 730-734.
28. Wahrle, S., P. Das, A. C. Nyborg, C. McLendon, M. Shoji, T. Kawarabayashi, L. H. Younkin, S. G. Younkin, and T. E. Golde. 2002. Cholesterol-dependent ψ-secretase activity in buoyant cholesterol-rich membrane microdomains. Nerobiol. Dis. 9: 11-23.
29. Yanagisawa, K., and K. Matsuzaki. 2002. Cholesterol-dependent aggregation of amyloid β-protein. Ann. N. Y. Acad. Sci. 977: 384-386.
30. Puglielli, L., G. Konopka, E. Pack-Chung, L. A. M. Ingano, O. Berezovska, B. T. Hyman, T. Y. Chang, R. E. Tanzi, and D. Kovacs. 2001. Acyl-coenzyme A:cholesterol acyltransferase modulates the generation of the amyloid β-peptide. Nat. Cell Biol. 3: 905-912.
31. Dietschy, J. M., and S. D. Turley. 2001. Cholesterol metabolism in the brain. Curr. Opin. Lipidol. 12: 105-112.
32. Russell, D. W. 2003. The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72: 137-174.
33. 2 techniques in vivo and in vitro. J. Biol. Chem. 272: 30178-30184.
34. Lütjohann, D., O. Breuer, G. Ahlborg, I. Nennesmo, Å. Sidén, U. Diczfalusy, and I. Björkhem. 1996. Cholesterol homeostasis in human brain: Evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation. Proc. Natl. Acad. Sci. USA. 93: 9799-9804.
35. Lund, E. G., J. M. Guileyardo, and D. W. Russell. 1999. cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain. Proc. Natl. Acad. Sci. USA. 96: 7238-7243.
36. Papassotiropoulos, A., D. Lfitjohann, M. Bagli, S. Locatelli, F. Jessen, R. Buschfort, U. Ptok, I. Björkhem, K. von Bergmann, and R. Heun. 2002. 24S-hydroxycholesterol in cerebrospinal fluid is elevated in early stages of dementia. J. Psychiatr. Res. 36: 27-32.
37. Lund, E. G., C. Xie, T. Kotti, S. D. Turley, J. M. Dietschy, and D. W. Russell. Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover. J. Biol. Chem. In press.
38. Pitas, R. E., J. K. Boyles, S. H. Lee, D. Hui, and K. H. Weisgraber. 1987. Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B,E(LDL) receptors in the brain. J. Biol. Chem. 262: 14352-14360.
39. Lütjohann, D., A. Papassotiropoulos, I. Björkhem, S. Locatelli, M. Bagli, R. D. Oehring, U. Schlegel, F. Jessen, M. L. Rao, K. von Bergmann, and R. Heun. 2000. Plasma 24S-hydroxycholesterol (cerebrosterol) is increased in Alzheimer and vascular demented patients. J. Lipid Res. 41: 195-198.
40. Schönknecht, P., D. Lütjohann, J. Pantel, H. Bardenheuer, T. Hartmann, K. von Bergmann, K. Beyreuther, and J. Schröder. 2002. Cerebrospinal fluid 24S-hydroxycholesterol is increased in patients with Alzheimer's disease compared to healthy controls. Neurosci. Lett. 324: 83-85.
41. Kölsch, H., M. Ludwig, D. Lütjohann, and M. L. Rao. 2001. Neurotoxicity of 24-hydroxycholesterol, an important cholesterol elimination product of the brain, may be prevented by vitamin E and estradiol-17β.J. Neural Transm. 108: 475-488.
42. Bretillon, L., D. Lütjohann, L. Ståhle, T. Widhe, L. Bindl, G. Eggertsen, U. Diczfalusy, and I. Björkhem. 2000. Plasma levels of 24S-hydroxycholesterol reflect the balance between cerebral production and hepatic metabolism and are inversely related to body surface. J. Lipid Res. 41: 840-845.
43. Vega, G. L., M. F. Weiner, A. M. Lipton, K. von Bergmann, D. Lütjohann, C. Moore, and D. Svetlik. 2003. Reduction in levels of 24S-hydroxycholesterol by statin treatment in patients with Alzheimer disease. Arch. Neurol. 60: 510-515.
44. Bogdanovic, N., L. Bretillon, E. G. Lund, U. Diczfalusy, L. Lannfelt, B. Winblad, D. W. Russell, and I. Björkhem. 2001. On the turnover of brain cholesterol in patients with Alzheimer's disease. Abnormal induction of the cholesterol-catabolic enzyme CYP46 in glial cells. Neurosci. Lett. 314: 45-48.
45. Janowski, B. A., P. J. Willy, T. R. Devi, J. R. Falck, and D. J. Mangelsdorf. 1996. An oxysterol signalling pathway mediated by the nuclear receptor LXRα. Nature. 383: 728-731.
46. Lehmann, J. M., S. A. Kliewer, L. B. Moore, T. A. Smith-Oliver, B. B. Oliver, J-L. Su, S. S. Sundseth, D. A. Winegar, D. E. Blanchard, T. A. Spencer, and T. M. Willson. 1997. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J. Biol. Chem. 272: 3137-3140.
47. Papassotiropoulos, A.,J. R. Streffer, M. Tsolaki, S. Schmid, D. Thal, F. Nicosia, V. Iakovidou, A. Maddalena, D. Lütjohann, E. Ghebremedhin, T. Hegi, T. Pasch, M. Träxler, A. Brühl, L. Benussi, G. Binetti, H. Braak, R. M. Nitsch, and C. Hock. 2003. Increased brain β-amyloid load, phosphorylated tau, and risk of Alzheimer disease associated with an intronic CYP46 polymorphism. Arch. NeuroL 60: 29-35.
48. Desai, P., S. T. DeKosky, and M. I. Kamboh. 2002. Genetic variation in the cholesterol 24-hydroxylase (CYP46) gene and the risk of Alzheimer's disease. Neurosci. Lett. 328: 9-12.
49. Fagan, A. M., D. M. Holtzman, G. Munson, T. Mathur, D. Schneider, L. K. Chang, G. S. Getz, C. A. Reardon, J. Lukens, J. A. Shah, and M.J. LaDu. 1999. Unique lipoproteins secreted by primary astrocytes from wild type, apoE (-/-), and human apoE transgenic mice. J. Biol. Chem. 274: 30001-30007.
50. Fujii, H., K. Saito, H. Hamakawa, N. Maekawa, S. Fujigaki, H. Wada, K. Shimodawa, M. Seishima, and T. Takami. 2002. Immunohistochemical localization and mRNA expression of apolipoprotein A-I in rat spinal cord. J. Atheroscler. Thromb. 9: 93-98.
51. Boyles, J. K., R. E. Pitas, E. Wilson, R. W. Mahley, and J. M. Taylor. 1985. Apolipoprotein E associated with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76: 1501-1513.
52. Linton, M. F., R. Gish, S. T. Hubl, E. Bütler, C. Esquivel, W. I. Bry, J. K. Boyles, M. R. Wardell, and S. G. Young. 1991. Phenotypes of apolipoprotein B and apolipoprotein E after liver transplantation. J. Clin. Invest. 88: 270-281.
53. Boschert, U., E. Merlo-Pich, G. Higgins, A. D. Roses, and S. Catsicas. 1999. Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol. Dis. 6: 508-514.
54. Dekroon, R. M., and P.J. Armati. 2001. Synthesis and processing of apolipoprotein E in human brain cultures. Glia. 33: 298-305.
55. Pfrieger, F. W. 2002. Outsourcing in the brain: Do neurons depend on cholesterol delivery by astrocytes? Bioessays. 25: 72-78.
56. Mauch, D. H., K. Nägler, S. Schumacher, C. Göritz, E-C. Müller, A. Otto, and F. W. Pfrieger. 2001. CNS synaptogenesis promoted by glia-derived cholesterol. Science. 294: 1354-1357.
57. Roses, A. D., and A. M. Saunders. 1997. ApoE, Alzheimer's disease, and recovery from brain stress. Ann. N. Y. Acad. Sci. 826: 200-212.
58. Saunders, A. M., W. J. Strittmatter, D. Schmechel, P. H. St George-Hyslop, M. A. Pericak-Vance, S. H. Joo, B. L. Rosi, J. F. Gusella, D. R. Crapper-MacLachlan, M. J. Alberts, C. Hulette, B. Crain, D. Goldgaber, and A. D. Roses. 1993. Association of apolipoprotein E allele ε4 with late-onset familial and sporadic Alzheimer's disease. Neurology. 43: 1467-1472.
59. Corder, E. H., A. M. Saunders, W. J. Strittmatter, D. E. Schmechel, P. C. Gaskell, G. W. Small, A. D. Roses, J. L. Haines, and M. A. Pericak-Vance. 1993. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 261: 921-923.
60. Teasdale, G. M.,J. A. R. Nicoll, G. Murray, and M. Fiddes. 1997. Association of apolipoprotein E polymorphism with outcome after head injury. Lancet. 350: 1069-1071.
61. Roses, A. D. 1998. Apolipoprotein E and Alzheimer's disease. The tip of the susceptibility iceberg. Ann. N. Y. Acad. Sci. 855: 738-743.
62. Weisgraber, K. H., and R. W. Mahley. 1996. Human apolipoprotein E: The Alzheimer's disease connection. FASEB J. 10: 1485-1494.
63. Chapman, S., T. Sabo, A. D. Roses, and D. M. Michaelson. 2000. Reversal of presynaptic deficits of apolipoprotein E-deficient mice in human apolipoprotein E transgenic mice. Neuroscience. 97: 419-424.
64. Chen, Y., L. Lomnitski, D. M. Michaelson, and E. Shohami. 1997. Motor and cognitive deficits in apolipoprotein E-deficient mice after closed head injury. Neuroscience. 80: 1255-1262.
65. Mahley, R. W., and Y. Huang. 1999. Apolipoprotein E: From atherosclerosis to Alzheimer's disease and beyond. Curr. Opin. Lipidol. 10:207-217.
66. Huang, Y., X. Q. Liu, T. Wyss-Coray, W.J. Brecht, D. A. Sanan, and R. W. Mahley. 2001. Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc. Natl. Acad. Sci. USA. 98: 8838-8843.
67. Ji, Z-S., R. D. Miranda, Y. M. Newhouse, K. H. Weisgraber, Y. Huang, and R. W. Mahley. 2002. Apolipoprotein E4 potentiates amyloid β peptide-induced lysosomal leakage and apoptosis in neuronal cells. J. Biol. Chem. 277: 21821-21828.
68. Dong, L-M., and K. H. Weisgraber. 1996. Human apolipoprotein E4 domain interaction. Arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins. J. Biol. Chem. 271:19053-19057.
69. Gong, J-S., M. Kobayashi, H. Hayashi, K. Zou, N. Sawamura, S. C. Fujita, K. Yanagisawa, and M. Michikawa. 2002. Apolipoprotein E (apoE) isoform-dependent lipid release from astrocytes prepared from human apoE3 and apoE4 knock-in mice. J. Biol. Chem. 277: 29919-29926.
70. Sun, Y., S. Wu, G. Bu, M. K. Onifade, S. N. Patel, M.J. LaDu, A. M. Fagan, and D. M. Holtzman. 1998. Glial fibrillary acidic protein-apolipoprotein E (apoE) transgenic mice: Astrocyte-specific expression and differing biological effects of astrocyte-secreted apoE3 and apoE4 lipoproteins. J. Neurosci. 18: 3261-3272.
71. Michikawa, M., Q-W. Fan, I. Isobe, and K. Yanagisawa. 2000. Apolipoprotein E exhibits isoform-specific promotion of lipid efflux from astrocytes and neurons in culture. J. Neurochem. 74: 1008-1016.
72. Wollmer, M. A., J. R. Streffer, D. Lütjohann, M. Tsolaki, V. Iakovidou, T. Hegi, T. Pasch, H. H. Jung, K. von Bergmann, R. M. Nitsch, C. Hock, and A. Papassotiropoulos. 2003. ABCA1 modulates CSF cholesterol levels and influences the age at onset of Alzheimer's disease. Neurobiol. Aging. 24: 421-426.
73. Fukumoto, H., A. Deng, M. C. Irizarry, M. L. Fitzgerald, and G. W. Rebeck. 2002. Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Aβ levels. J. Biol. Chem. 277: 48508-48513.
74. Koldamova, R. P., I. M. Lefterov, M. D. Ikonomovic, J. Skoko, P. I. Lefterov, B. A. Isanski, S. T. DeKosky, and J. S. Lazo. 2003. 22R-Hydroxycholesterol and 9-cis-retinoic acid induce ATP-binding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid β secretion. J. Biol. Chem. 278: 13244-13256.