Secretion of apolipoprotein E by brain glia requires protein prenylation and is suppressed by statins

Brain Research

Volumn 958, Issue 1, 2002, Pages 100-111

  Naidu, Asha ^a   Xu, Qiang ^a,b   Catalano, Rosanne ^a   Cordell, Barbara ^a  

^a SCIOS INC   (United States)

^b Osel Inc   (United States)

Author keywords

Alzheimer; ApoE; Glia; Prenylation

Indexed keywords

APOLIPOPROTEIN E; COMPACTIN; MEVALONIC ACID; MEVINOLIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; COGNITION; CONTROLLED STUDY; DEMENTIA; GLIA; HIPPOCAMPUS; MICROGLIA; NONHUMAN; PARENCHYMA; PRENYLATION; PRIORITY JOURNAL; PROTEIN SECRETION; SYNTHESIS; TISSUE CULTURE;

ALKYL AND ARYL TRANSFERASES; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; ANIMALS, NEWBORN; APOLIPOPROTEINS E; ASTROCYTES; BRAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FARNESYLTRANSTRANSFERASE; HIPPOCAMPUS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LOVASTATIN; MEVALONIC ACID; MICE; MICE, TRANSGENIC; MICROGLIA; NEUROGLIA; POLYISOPRENYL PHOSPHATES; PROTEIN ISOPRENYLATION;

EID: 0037146884     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03480-7     Document Type: Article

References (53)

1. Bales K.R., Verina T., Dodel R.C., Du Y., Alstiel L., Bender M., Hyslop P., Johnstone E.M., Little S.P., Cummins D.J., Piccardo P., Ghetti B., Paul S.M. Lack of apolipoprotein E dramatically reduces amyloid. Nature Genet. 17:1997;263-264.
2. 717F transgenic mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 96:1999;15233-15238.
3. Bales K.R., Du Y., Holtzman D., Cordell B., Paul S.M. Neuroinflammation and Alzheimer's disease: critical roles for cytokine/Aβ-induced glial activation, NF-κB, and apolipoprotein E. Neurobiol. Aging. 21:2000;427-432.
4. Basu S.K., Goldstein J.L., Brown M.S. Independent pathways for secretion of cholesterol and apolipoprotein E by macrophage. Science. 219:1983;871-873.
5. Beffert U., Danik M., Krzywkowski P., Ramassamy C., Berrada F., Poirier J. The neurobiology of apolipoproteins and their receptors in the CNS and Alzheimer's disease. Brain Res. Rev. 27:1998;119-142.
6. Boyles J.K., Pitas R.E., Wilson E., Mahley R.W., Taylor J.M. Apolipoprotein E associates with astrocytic glia of the central nervous system and with nonmyelinating glia of the peripheral nervous system. J. Clin. Invest. 76:1985;1501-1513.
7. Corder E.H., Saunders A.M., Strittmatter W.J., Schmechel D.E., Gaskell P.C., Small G.W., Roses A.D., Haines J.L., Pericak-Vance M.A. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science. 261:1993;921-923.
8. Davignon J., Gregg R.E., Sing C.F. Apolipoprotein E polymorphism and atherosclerosis. Atherosclerosis. 8:1988;1-12.
9. 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. USA. 95:1998;8880-8885.
10. 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 Abeta42 and Abeta40 in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 98:2001;5856-5861.
11. Fisher J.E., Rogers M.J., Halasy J.M., Luckman S.P., Hughes D.E., Masarachia P.J., Wesolowski G., Russell R.G.G., Rodan G.A., Reszka A.A. Alendronate mechanism of action: geranylgeraniol, an intermediate in the mevalonate pathway, prevents inhibition of osteoclast formation, bone resorption, and kinase activation in vitro. Proc. Natl. Acad. Sci. USA. 96:1999;133-138.
12. Garcia A.M., Rowell C., Ackermann K., Kowalczyk J.J., Lewis M.D. Peptidomimetic inhibitors of Ras farnesylation and function in whole cells. J. Biol. Chem. 268:1995;18415-18418.
13. Gearing M., Mori H., Mirra S.S. Abeta-peptide length and apolipoprotein E genotype in Alzheimer disease. Ann. Neurol. 39:1996;395-399.
14. Griffin W.S.T., Sheng J.G., Royston M.C., Gentleman S.M., McKenzie J.E., Graham D.I., Roberts G.W., Mrak R.E. Glial-neuronal interactions in Alzheimer's disease: the potential role of a 'cytokine cycle' in disease progression. Brain Pathol. 8:1998;65-72.
15. Herz J. The LDL receptor gene family: (un)expected signal transducers in the brain. Neuron. 29:2001;571-581.
16. Holtzman D.M., Bales K.R., Tenkova T., Fagan A.M., Parsadanian M., Sartorius L.J., Mackey B., Olney J., McKeel D., Wozniak D., Paul S.M. Apolipoprotein E isoform-dependent amyloid deposition and neurite degeneration in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 97:2000;2892-2897.
17. Jarvik G.P., Wijsman E.M., Kukull W.A., Schellenberg G.D., Yu C., Larson E.B. Interactions of apolipoprotein E genotype, total cholesterol level, age and sex in prediction of Alzheimer disease: a case-control study. Neurology. 45:1995;1092-1096.
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. Kwak B., Mulhaupt F., Myit S., Mach F. Statins as a newly recognized type of immunomodulator. Nature Med. 6:2000;1399-1402.
20. LaDu M.J., Falduto M.T., Manelli A.M., Reardon C.A., Getz G.S., Frail D.E. Isoform-specific binding of apolipoprotein E to beta-amyloid. J. Biol. Chem. 269:1994;23403-23406.
21. LaDu M.J., Reardon C.A., Van Eldik L.J., Fagan A.M., Bu G., Holtzman D.M., Getz G.S. Lipoproteins in the central nervous system. Ann. NY Acad. Sci. 903:2000;167-175.
22. Lerner E.C., Qian Y., Blaskovich M.A., Fossum R.D., Vogt A., Sun J., Cox A.D., Der C.J., Hamilton A.D., Sebti S.M. Ras CAAX peptidomimetic FTI-277 selectively blocks oncogenic Ras signaling by inducing cytoplasmic accumulation of inactive Ras-Raf complexes. J. Biol. Chem. 270:1995;26802-26806.
23. Ma J., Wee A., Brewer H.B., Das S., Potter H. Amyloid-associated proteins alpha-1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer beta-protein into filaments. Nature. 372:1994;92-94.
24. Manne V., Ricca C.S., Brown J.G., Tuomari A., Yan N., Patel D.V., Schmidt R., Lynch M.J., Ciosek J., Carboni J.M., Robinson S., Gordon E.M., Barbacid M., Seizinger B.R., Biller S.A. Ras farnesylation as a target for novel antitumor agents: potent and selective farnesyl diphosphate analog inhibitors of farnesyltransferase. Drug Dev. Res. 34:1995;121-137.
25. Naidu A., Catalano R., Bales K., Wu S., Paul S.M., Cordell S.M.B. Conversion of brain apolipoprotein E to an insoluble form in a mouse model of Alzheimer disease. NeuroReport. 12:2001;1265-1270.
26. Nakai M., Kawamata T., Maeda K., Tanaka C. Expression of apolipoprotein E mRNA in rat microglia. Neurosci. Lett. 211:1996;41-44.
27. Naslund J., Thyberg J., Tjernberg L.O., Wernstedt C., Karlstrom A.R., Bogdanovic N., Gandy S.E., Lannfelt L., Terenius L., Nordstedt C. Characterization of stable complexes involving apolipoprotein E and the amyloid beta peptide in Alzheimer's disease brain. Neuron. 15:1995;219-228.
28. Notkola I.L., Sulkava R., Pekkanen J., Erkinjuntti T., Ehnholm C., Kivinen P., Tuomilehto J., Nissinen A. Serum total cholesterol, apolipoprotein E epsilon 4 allele, and Alzheimer's disease. Neuroepidemiology. 17:1998;14-20.
29. Pahan K., Sheikh F.G., Namboodiri A.M.S., Singh I. Lovastatin and phenylacetate inhibit the induction of nitric oxide synthase and cytokines in rat primary astrocytes, microglia, and macrophages. J. Clin. Invest. 100:1997;2671-2679.
30. Park H.-J., Galper J.B. 3-Hydroxy-3-methylglutaryl CoA reductase inhibitors up-regulate transforming growth factor-beta signaling in cultured heart cells via inhibition of geranylgeranylation of RhoA GTPase. Proc. Natl. Acad. Sci. USA. 96:1999;11525-11530.
31. Permanne B., Perez C., Soto C., Frangione B., Wisniewski T. Detection of apolipoprotein E/dimeric soluble amyloid beta complexes in Alzheimer's disease brain supernatants. Biochem. Biophys. Res. Commun. 240:1997;715-720.
32. Pitas R.E., Boyles J.K., Lee S.H., Foss D., Mahley R.W. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim. Biophys. Acta. 917:1987;148-161.
33. Poirier J. Apolipoprotein E and Alzheimer's disease: a role in amyloid catabolism. Ann. NY Acad. Sci. 924:2000;81-90.
34. Quon D., Wang Y., Catalano R., Marian Scardina J., Murakami K., Cordell B. Formation of β-amyloid protein deposits in brains of transgenic mice. Nature. 352:1991;239-241.
35. Refolo L.M., Malester B., LaFrancois J., Thomas-Bryant T., Wang R., Tint G.S., Sambamurti K., Duff K.E., Pappolla M.A. Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model. Neurobiol. Dis. 7:2000;321-331.
36. Refolo L.M., Pappolla M.A., LaFrancois J., Malester J., 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 disease. Neurobiol. Dis. 8:2001;890-899.
37. Russo C., Angelini D., Dapino D., Piccini A., Piombo G., Schettini G., Chen S., Teller J.K., Zaccheo D., Gambetti P., Tabaton M. Opposite roles of apolipoprotein E in normal brains and in Alzheimer's disease. Proc. Natl. Acad. Sci. USA. 95:1998;15598-15602.
38. Saunders A.M. Apolipoprotein E and Alzheimer's disease: an update on genetic and functional analyses. J. Neuropathol. Exp. Neurol. 59:2000;751-758.
39. Sheng J.G., Mrak R.E., Griffin W.T.S. Apolipoprotein E distribution among different plaque types in Alzheimer disease: implications for its role in plaque progression. Neuropathol. Appl. Neurol. 22:1996;334-341.
40. 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. USA. 95:1998;6460-6464.
41. Sinensky M. Functional aspects of polyisoprenoid protein substituents: roles in protein-protein interaction and trafficking. Biochim. Biophys. Acta. 1529:2000;203-209.
42. Slooter A.J.C., Tang M.-X., van Duijn C.M., Stern Y., Ott A., Bell K., Breteler M.M.B., van Broeckhoven C., Tatemichi T.K., Tycko B., Hofman A., Mayeux A.R. Apolipoprotein E epsilon-4 and the risk of dementia with stroke. A population-based investigation. J. Am. Med. Assoc. 277:1997;818-821.
43. Snowdon D.A., Greiner L.H., Mortimer J.A., Riley K.P., Greiner P.A., Markesbery W.R. Brain infarction and the clinical expression of Alzheimers disease. The nun study. J. Am. Med. Assoc. 277:1997;813-817.
44. Sparks D.L., Scheff S.W., Hunsaker J.C., Liu H., Landers T., Gross D.R. Induction of Alzheimer-like beta-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol. Exp. Neurol. 126:1994;88-94.
45. Sparks D.L. Coronary artery disease, hypertension, ApoE, and cholesterol: a link to Alzheimer's disease? Ann. NY Acad. Sci. 826:1997;128-146.
46. Stoppini L., Buchs P.A., Muller D. A simple method for organotypic culture of nervous tissue. J. Neurosci. Methods. 37:1991;173-182.
47. Styren S.D., Kamboh M.I., Dekosky J. Expression of differential immune factors in temporal cortex and cerebellum: the role of alpha-1-antichymotrypsin, apolipoprotein E, and reactive glia in the progression of Alzheimer disease. Comp. Neurol. 396:1998;511-520.
48. Sun J., Qian Y., Hamilton A.D., Sebti S.M. Ras CAAX peptidomimetic FTI-276 selectively blocks tumor growth in nude mice of a human lung carcinoma with k-Ras mutation and p53 deletion. Cancer Res. 55:1995;4243-4247.
49. Sun J., Qian Y., Hamilton A.D., Sebti S.M. Both farnesyltransferase and geranylgeranyltransferase I inhibitors are required for inhibition of oncogenic k-Ras prenylation but each alone is sufficient to suppress human growth in nude mouse xenografts. Oncogene. 16:1998;1467-1473.
50. Wisniewski T., Castano E.M., Goldbek A., Vogel T., Frangione B. Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. Am. J. Pathol. 145:1994;1030-1035.
51. Weitz-Schmidt G., Welzenbach K., Brinkmann V., Kamata T., Kallen J., Bruns C., Cottens S., Takada Y., Hommel U. Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site. Nature Med. 7:2001;687-692.
52. Wolozin B., Kellman W., Ruosseau P., Celesia G.G., Siegel G. Decreased prevalence of Alzheimer disease with 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57:2000;1439-1443.
53. Xu Q., Cyras C., Sanan D.A., Cordell B. Isolation and characterization of apolipoproteins from murine microglia. J. Biol. Chem. 275:2000;31770-31777.