Regulation of hippocampal cholesterol metabolism by apoE and environmental stimulation

Journal of Neurochemistry

Volumn 95, Issue 4, 2005, Pages 987-997

  Levi, Ofir ^a   Lütjohann, Dieter ^b   Devir, Aliza ^a   Von Bergmann, Klaus ^b   Hartmann, Tobias ^c   Michaelson, Daniel M ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF BONN   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Alzheimer's disease; ApoE; Astrocytes; Cholesterol; Enriched environment; Synaptic plasticity

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; CHOLESTEROL; CHOLESTEROL DERIVATIVE; DESMOSTEROL; LATHOSTEROL;

ALLELE; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CHOLESTEROL METABOLISM; CONTROLLED STUDY; EDUCATION; ENVIRONMENTAL FACTOR; HIPPOCAMPUS; HISTOLOGY; HOMEOSTASIS; HYPERLIPOPROTEINEMIA TYPE 3; IMMUNOHISTOCHEMISTRY; METABOLIC REGULATION; METABOLITE; MOUSE; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; RISK FACTOR; STIMULATION; SYNAPTOGENESIS; TRANSGENIC MOUSE;

ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; ASTROCYTES; BLOTTING, WESTERN; CHOLESTEROL; ENVIRONMENT; HIPPOCAMPUS; HISTOCYTOCHEMISTRY; HUMANS; IMMUNOHISTOCHEMISTRY; ISOMERISM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL;

ANIMALIA; MUS MUSCULUS;

EID: 28244461327     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03441.x     Document Type: Article

References (50)

1. Bellosta S., Nathan B. P., Orth M., Dong L. M., Mahley R. W. and Pitas R. E. (1995) Stable expression and secretion of apolipoproteins E3 and E4 in mouse neuroblastoma cells produces differential effects on neurite outgrowth. J. Biol. Chem. 270, 27 063-27 071.
2. Bjorkhem I. and Meaney S. (2004) Brain cholesterol: long secret life behind a barrier. Arterioscler. Thromb. Vasc. Biol. 24, 806-815.
3. Chen Y., Constantini S., Trembovler V., Weinstock M. and Shohami E. (1996) An experimental model of closed head injury in mice: pathophysiology, histopathology, and cognitive deficits. J. Neurotrauma 13, 557-568.
4. Chen Y., Lomnitski L., Michaelson D. M. and Shohami E. (1997) Motor and cognitive deficits in apolipoprotein E-deficient mice after closed head injury. Neuroscience 80, 1255-1262.
5. Corder E. H., Saunders A. M., Strittmatter W. J., Schmechel D. E., Gaskell P. C., Small G. W., Roses A. D., Haines J. L. and Pericak-Vance M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923.
6. DeMattos R. B., Curtiss L. K. and Williams D. L. (1998) A minimally lipidated form of cell-derived apolipoprotein E exhibits isoform-specific stimulation of neurite outgrowth in the absence of exogenous lipids or lipoproteins. J. Biol. Chem. 273, 4206-4212.
7. DeMattos R. B., Brendza R. P., Heuser J. E., Kierson M., Cirrito J. R., Fryer J., Sullivan P. M., Fagan A. M., Han X. and Holtzman D. M. (2001) Purification and characterization of astrocyte-secreted apolipoprotein E- and J-containing lipoproteins from wild-type and human apoE transgenic mice. Neurochem. Int. 39, 415-425.
8. Dietschy J. M. and Turley S. D. (2004) Cholesterol metabolism in the central nervous system during early development and in the mature animal. J Lipid Res. 45, 1375-1397.
9. Emmerling M. R., Morganti-Kossmann M. C., Kossmann T. et al. (2000) Traumatic brain injury elevates the Alzheimer's amyloid peptide Aβ42 in human CSF. A possible role for nerve cell injury. Ann. NY Acad. Sci. 903, 118-122.
10. Fagan A. M., Holtzman D. M., Munson G. et al. (1999) Unique lipoproteins secreted by primary astrocytes from wild type, apoE(-/-), and human apoE transgenic mice. J. Biol. Chem. 274, 30 001-30 007.
11. Gong J. S., Kobayashi M., Hayashi H., Zou K., Sawamura N., Fujita S. C., Yanagisawa K. and Michikawa M. (2002) Apolipoprotein E (ApoE) isoform-dependent lipid release from astrocytes prepared from human ApoE3 and ApoE4 knock-in mice. J. Biol. Chem. 277, 29 919-29 926.
12. Han S. H. and Chung S. Y. (2000) Marked hippocampal neuronal damage without motor deficits after mild concussive-like brain injury in apolipoprotein E-deficient mice. Ann. NY Acad. Sci. 903, 357-365.
13. Handelmann G. E., Boyles J. K., Weisgraber K. H., Mahley R. W. and Pitas R. E. (1992) Effects of apolipoprotein Eβ, very low-density lipoproteins, and cholesterol on the extension of neurites by rabbit dorsal root ganglion neurons in vitro. J. Lipid Res. 33, 1677-1688.
14. Haydon P. G. (2001) GLIA: listening and talking to the synapse. Nat. Rev. Neurosci. 2, 185-193.
15. Herz J. and Bock H. H. (2002) Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71, 405-434.
16. Heverin M., Bogdanovic N., Lutjohann D., Bayer T., Pikuleva I., Bretillon L., Diczfalusy U., Winblad B. and Bjorkhem I. (2004) Changes in the levels of cerebral and extracerebral sterols in the brain of patients with Alzheimer's disease. J. Lipid Res. 45, 186-193.
17. Hirsch-Reinshagen V., Zhou S., Burgess B. L., Bernier L., McIsaac S. A., Chan J. Y., Tansley G. H., Cohn J. S., Hayden M. R. and Wellington C. L. (2004) Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J. Biol. Chem. 279, 41 197-41 207.
18. Holtzman D. M., Pitas R. E., Kilbridge J., Nathan B., Mahley R. W., Bu G. and Schwartz A. L. (1995) Low density lipoprotein receptor-related protein mediates apolipoprotein E-dependent neurite outgrowth in a central nervous system-derived neuronal cell line. Proc. Natl Acad. Sci. USA 92, 9480-9484.
19. Katzman R. (1993) Education and the prevalence of dementia and Alzheimer's disease. Neurology 43, 13-20.
20. Kawas C. H., Clark C. M., Farlow M. R., Knopman D. S., Marson D., Morris J. C., Thal L. J. and Whitehouse P. J. (1999) Clinical trials in Alzheimer disease: debate on the use of placebo controls. Alzheimer Dis. Assoc. Disord. 13, 124-129.
21. Lazarov O., Robinson J., Tang Y. P., Hairston I. S., Korade-Mirnics Z., Lee V. M., Hersh L. B., Sapolsky R. M., Mimics K. and Sisodia S. S. (2005) Environmental enrichment reduces Aβ levels and amyloid deposition in transgenic mice. Cell 120, 701-713.
22. Levi O., Jongen-Relo A. L., Feldon J., Roses A. D. and Michaelson D. M. (2003) ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol. Dis. 13, 273-282.
23. Levi O., Jongen-Relo A. L., Feldon J., Roses A. D. and Michaelson D. M. (2005) Brain area- and isoform-specific inhibition of synaptic plasticity by apoE4. J. Neurol. Sci. 15, 241-248.
24. Lund E. G., Guileyardo J. M. and Russell D. W. (1999) cDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain. Proc. Natl. Acad. Sci. USA 96, 7238-7243.
25. Lutjohann D. and von Bergmann K. (2003) 24S-hydroxycholesterol: a marker of brain cholestrol metabolism. Pharmacopsychiatry 36, 102-106.
26. Lutjohann D., Brzezinka A., Barth E., Abramowski D., Staufenbiel M., von Bergmann K., Beyreuther K., Multhaup G. and Bayer T. A. (2002) Profile of cholesterol-related sterols in aged amyloid precursor protein transgenic mouse brain. J. Lipid Res. 43, 1078-1085.
27. Masliah E., Mallory M., Ge N., Alford M., Veinbergs I. and Roses A. D. (1995) Neurodegeneration in the central nervous system of apoE-deficient mice. Exp. Neurol. 136, 107-122.
28. Masliah E., Mallory M., Veinbergs I., Miller A. and Samuel W. (1996) Alterations in apolipoprotein E expression during aging and neurodegeneration. Prog. Neurobiol. 50, 493-503.
29. Mauch D. H., Nagler K., Schumacher S., Goritz C., Muller E. C., Otto A. and Pfrieger F. W. (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294, 1354-1357.
30. Michikawa M. and Yanagisawa K. (1998) Apolipoprotein E4 induces neuronal cell death under conditions of suppressed de novo cholesterol synthesis. J. Neurosci. Res. 54, 58-67.
31. Michikawa M. and Yanagisawa K. (1999) Apolipoprotein E4 isoform-specific actions on neuronal cells in culture. Mech. Ageing Dev. 107, 233-243.
32. Michikawa M., Fan Q. W., Isobe I. and Yanagisawa K. (2000) Apolipoprotein E exhibits isoform-specific promotion of lipid efflux from astrocytes and neurons in culture. J. Neurochem. 74, 1008-1016.
33. Moceri V. M., Kukull W. A., Emanuel I., van Belle G. and Larson E. B. (2000) Early-life risk factors and the development of Alzheimer's disease. Neurology 54, 415-420.
34. Nathan B. P., Bellosta S., Sanan D. A., Weisgraber K. H., Mahley R. W. and Pitas R. E. (1994) Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264, 850-852.
35. Nathan B. P., Chang K. C., Bellosta S., Brisch E., Ge N., Mahley R. W. and Pitas R. E. (1995) The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerizarion. J. Biol. Chem. 270, 19 791-19 799.
36. Ophir G. and Levi O. (2004) The phenotypic effects of the apoE genotype in transgenic mice. Brain Aging 4, 22-26.
37. Ophir G., Meilin S., Efrati M., Chapman J., Karussis D., Roses A. and Michaelson D. M. (2003) Human apoE3 but not apoE4 rescues impaired astrocyte activation in apoE null mice. Neurobiol. Dis. 12, 56-64.
38. Pfrieger F. W. (2003) Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? Bioessays 25, 72-78.
39. Pitas R. E., Ji Z. S., Weisgraber K. H. and Mahley R. W. (1998) Role of apolipoprotein E in modulating neurite outgrowth: potential effect of intracellular apolipoprotein E. Biochem. Soc. Trans. 26, 257-262.
40. van Praag H., Kempermann G. and Gage F. H. (2000) Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1, 191-198.
41. Roses A. D. (1996) Apolipoprotein E alleles as risk factors in Alzheimer's disease. Annu. Rev. Med. 47, 387-400.
42. San Jose I., Garcia-Atares N., Pelaez B., Cabo R., Esteban I., Vega J. A. and Represa J. (2001) Reduction of glial fibrillary acidic protein- immunoreactive astrocytes in some brain areas of old hairless rhino-j mice (hr-rh-j). Neurosci. Lett. 309, 81-84.
43. Saunders A. M., Strittmatter W. J., Schmechel D. et al. (1993) Association of apolipoprotein E allele ε4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43, 1467-1472.
44. Seitz A., Kragol M., Aglow E., Showe L. and Heber-Katz E. (2003) Apolipoprotein E expression after spinal cord injury in the mouse. J. Neurosci. Res. 71, 417-426.
45. Sloop C. H., Dory L. and Roheim P. S. (1987) Interstitial fluid lipoproteins. J. Lipid Res. 28, 225-237.
46. Soffie M., Hahn K., Terao E. and Eclancher F. (1999) Behavioural and glial changes in old rats following environmental enrichment. Behav. Brain Res. 101, 37-49.
47. Williamson R., Lee D., Hagaman J. and Maeda N. (1992) Marked reduction of high density lipoprotein cholesterol in mice genetically modified to lack apolipoprotein A-I. Proc. Natl Acad. Sci. USA 89, 7134-7138.
48. Xu P. T., Schmechel D., Rothrock-Christian T. et al. (1996) Human apolipoprotein E2, E3, and E4 isoform-specific transgenic mice: human-like pattern of glial and neuronal immunoreactivity in central nervous system not observed in wild-type mice. Neurobiol. Dis. 3, 229-245.
49. Yamada A., Saji M., Ukita Y., Shinoda Y., Taniguchi M., Higaki K., Ninomiya H. and Ohno K. (2001) Progressive neuronal loss in the ventral posterior lateral and medial nuclei of thalamus in Niemann_Pick disease type C mouse brain. Brain Dev. 23, 288-297.
50. Zhang M. Y., Katzman R., Salmon D. et al. (1990) The prevalence of dementia and Alzheimer's disease in Shanghai, China: impact of age, gender, and education. Ann. Neurol. 27, 428-437.