Neuron-Specific Apolipoprotein E4 Proteolysis Is Associated with Increased Tau Phosphorylation in Brains of Transgenic Mice

Journal of Neuroscience

Volumn 24, Issue 10, 2004, Pages 2527-2534

  Brecht, Walter J ^a,b   Harris, Faith M ^a,b   Chang, Shengjun ^a,b   Tesseur, Ina ^a,e   Yu, Gui Qiu ^a   Xu, Qin ^a,b   Fish, Jo Dee ^b   Wyss Coray, Tony ^a,c,e   Buttini, Manuel ^a,c,f   Mucke, Lennart ^a,c   Mahley, Robert W ^a,b,c,d   Huang, Yadong ^a,b,d  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^f ELAN PHARMACEUTICALS   (United States)

Author keywords

Alzheimer's disease; Apolipoprotein E; Excitotoxin; Proteolysis; Tau phosphorylation; Transgenic mice

Indexed keywords

AMYLOID; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; EXCITOTOXIN; GLIAL FIBRILLARY ACIDIC PROTEIN; ISOPROTEIN; KAINIC ACID; NEURON SPECIFIC ENOLASE; TAU PROTEIN;

AGE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CEREBELLUM; CONTROLLED STUDY; FEMALE; FRAGMENTATION REACTION; HIPPOCAMPUS; MALE; MOUSE; NEOCORTEX; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

AGING; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; APOLIPOPROTEINS E; ASTROCYTES; BRAIN; BRAIN CHEMISTRY; FEMALE; GENE TARGETING; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; KAINIC ACID; MICE; MICE, TRANSGENIC; NEURONS; NEUROTOXINS; PEPTIDE FRAGMENTS; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); TAU PROTEINS;

EID: 12144290271     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4315-03.2004     Document Type: Article

References (69)

1. Aoki K, Uchihara T, Sanjo N, Nakamura A, Ikeda K, Tsuchiya K, Wakayama Y (2003) Increased expression of neuronal apolipoprotein E in human brain with cerebral infarction. Stroke 34:875-880.
2. V717F transgenic mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 96:15233-15238.
3. Bao F, Arai H, Matsushita S, Higuchi S, Sasaki H (1996) Expression of apolipoprotein E in normal and diverse neurodegenerative disease brain. NeuroReport 7:1733-1739.
4. Beffert U, Poirier J (1996) Apolipoprotein E, plaques, tangles and cholinergic dysfunction in Alzheimer's disease. Ann NY Acad Sci 777:166-174.
5. Boschert U, Merlo-Pich E, Higgins G, Roses AD, Catsicas S (1999) Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol Dis 6:508-514.
6. Boyles JK, Pitas RE, Wilson E, Mahley RW, Taylor JM (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.
7. -/- mice: isoform-specific effects on neurodegeneration. J Neurosci 19:4867-4880.
8. Buttini M, Akeefe H, Lin C, Mahley RW, Pitas RE, Wyss-Coray T, Mucke L (2000) Dominant negative effects of apolipoprotein E4 revealed in transgenic models of neurodegenerative disease. Neuroscience 97:207-210.
9. Buttini M, Yu G-Q, Shockley K, Huang Y, Jones B, Masliah E, Mallory M, Yeo T, Longo FM, Mucke L (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.
10. Cataldo AM, Barnett JL, Pieroni C, Nixon RA (1997) Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased β-amyloidogenesis. J Neurosci 17:6142-6151.
11. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, Nixon RA (2000) Endocytic pathway abnormalities precede amyloid β deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am J Pathol 157:277-286.
12. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261:921-923.
13. Crowther RA (1993) Tau protein and paired helical filaments of Alzheimer's disease. Curr Opin Struct Biol 3:202-206.
14. Dekroon RM, Armati PJ (2001) Synthesis and processing of apolipoprotein E in human brain cultures. Glia 33:298-305.
15. Diedrich JF, Minnigan H, Carp RI, Whitaker JN, Race R, Frey II W, Haase AT (1991) Neuropathological changes in scrapie and Alzheimer's disease are associated with increased expression of apolipoprotein E and cathepsin D in astrocytes. J Virol 65:4759-4768.
16. Dupont-Wallois L, Soulié C, Sergeant N, Wavrant-de Wrieze N, Chartier-Harlin M-C, Delacourte A, Caillet-Boudin M-L (1997) ApoE synthesis in human neuroblastoma cells. Neurobiol Dis 4:356-364.
17. Farrer LA, Cupples LA, Haines JL, Hyman B, Kukull WA, Mayeux R, Myers RH, Pericak-Vance MA, Risch N, Van Duijn CM (1997) Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease: a meta-analysis. JAMA 278:1349-1356.
18. Ferreira S, Dupire M-J, Delacourte A, Najib J, Caillet-Boudin M-L (2000) Synthesis and regulation of apolipoprotein E during the differentiation of human neuronal precursor NT2/D1 cells into postmitotic neurons. Exp Neurol 166:415-421.
19. Grbovic OM, Mathews PM, Jiang Y, Schmidt SD, Dinakar R, Summers-Terio NB, Ceresa BP, Nixon RA, Cataldo AM (2003) Rab5-stimulated upregulation of the endocytic pathway increases intracellular β-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Aβ production. J Biol Chem 278:31261-31268.
20. Han S-H, Einstein G, Weisgraber KH, Strittmatter WJ, Saunders AM, Pericak-Vance M, Roses AD, Schmechel DE (1994) Apolipoprotein E is localized to the cytoplasm of human cortical neurons: a light and electron microscopic study. J Neuropathol Exp Neurol 53:535-544.
21. Harris FM, Brecht WJ, Xu Q, Tesseur I, Kekonius L, Wyss-Coray T, Fish JD, Masliah E, Hopkins PC, Scearce-Levie K, Weisgraber KH, Mucke L, Mahley RW, Huang Y (2003) Carboxyl-terminal-truncated apolipoprotein E4 causes Alzheimer's disease-like neurodegeneration and behavioral deficits in transgenic mice. Proc Natl Acad Sci USA 100:10966-10971.
22. Harris FM, Tesseur I, Brecht WJ, Xu Q, Mullendorff K, Chang S, Wyss-Coray T, Mahley RW, Huang Y (2004) Astroglial regulation of apolipoprotein E expression in neuronal cells: implications for Alzheimer's disease. J Biol Chem 279:3862-3868.
23. Hartman RE, Wozniak DF, Nardi A, Olney JW, Sartorius L, Holtzman DM (2001) Behavioral phenotyping of GFAP-apoE3 and -apoE4 transgenic mice: apoE4 mice show profound working memory impairments in the absence of Alzheimer's-like neuropathology. Exp Neurol 170:326-344.
24. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol 60:1119-1122.
25. Herz J, Beffert U (2000) Apolipoprotein E receptors: linking brain development and Alzheimer's disease. Nat Rev Neurosci 1:51-58.
26. Holtzman DM, Bales KR, Tenkova T, Fagan AM, Parsadanian M, Sartorius LJ, Mackey B, Olney J, McKeel D, Wozniak D, Paul SM (2000) Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 97:2892-2897.
27. Huang Y, Mahley RW (1999). Apolipoprotein E and human disease. In: Plasma lipids and their role in disease (Barter PJ, Rye K-A, eds), pp 257-284. Amsterdam: Harwood.
28. Huang Y, Liu XQ, Rall Jr SC, Taylor JM, von Eckardstein A, Assmann G, Mahley RW (1998) Overexpression and accumulation of apolipoprotein E as a cause of hypertriglyceridemia. J. Biol Chem 273:26388-26393.
29. Huang Y, Liu XQ, Wyss-Coray T, Brecht WJ, Sanan DA, Mahley RW (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.
30. V717F transgenic mice. Acta Neuropathol (Berl) 100:451-458.
31. Ji Z-S, Miranda RD, Newhouse YM, Weisgraber KH, Huang Y, Mahley RW (2002) Apolipoprotein E4 potentiates amyloid β peptide-induced lysosomal leakage and apoptosis in neuronal cells. J Biol Chem 277:21821-21828.
32. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE (1994) Isoform-specific binding of apolipoprotein E to β-amyloid. J Biol Chem 269:23403-23406.
33. Lesuisse C, Xu G, Anderson J, Wong M, Jankowsky J, Holtz G, Gonzalez V, Wong PCY, Price DL, Tang F, Wagner S, Borchelt DR (2001) Hyperexpression of human apolipoprotein E4 in astroglia and neurons does not enhance amyloid deposition in transgenic mice. Hum Mol Genet 10:2525-2537.
34. Ljungberg MC, Dayanandan R, Asuni A, Rupniak TH, Anderton BH, Lovestone S (2002) Truncated apoE forms tangle-like structures in a neuronal cell line. NeuroReport 13:867-870.
35. 1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer β-protein into filaments. Nature 372:92-94.
36. Mahley R, Huang Y (1999) Apolipoprotein E: from atherosclerosis to Alzheimer's disease and beyond. Curr Opin Lipidol 10:207-217.
37. Mahley R, Huang Y (2000) Apolipoprotein E: structure and function in lipid metabolism and neurobiology. In: The molecular and genetic basis of neurologic and psychiatric disease, Ed 3 (Rosenberg RN, Prusiner SB, DiMauro S, Barchi RL, Nestler EJ, eds), pp 565-573. Philadelphia: Butterworth Heinemann.
38. Masliah E, Westland CE, Rockenstein EM, Abraham CR, Mallory M, Veinberg I, Sheldon E, Mucke L (1997) Amyloid precursor proteins protect neurons of transgenic mice against acute and chronic excitotoxic injuries in vivo. Neuroscience 78:135-146.
39. Metzger RE, LaDu MJ, Pan JB, Getz GS, Frail DE, Falduto MT (1996) Neurons of the human frontal cortex display apolipoprotein E immunoreactivity: implications for Alzheimer's disease. J Neuropathol Exp Neurol 55:372-380.
40. Miyata M, Smith JD (1996) Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and β-amyloid peptides. Nat Genet 14:55-61.
41. Morrison JH, Hof PR (2002) Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer's disease. Prog Brain Res 136:467-486.
42. Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K (1991) Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res 541:163-166.
43. Nathan BP, Bellosta S, Sanan DA, Weisgraber KH, Mahley RW, Pitas RE (1994) Differential effects of apolipoproteins E3 and E4 on neuronal growth in vitro. Science 264:850-852.
44. Nathan BP, Chang K-C, Bellosta S, Brisch E, Ge N, Mahley RW, Pitas RE (1995) The inhibitory effect of apolipoprotein E4 on neurite outgrowth is associated with microtubule depolymerization. J Biol Chem 270:19791-19799.
45. Poirier J, Hess M, May PC, Finch CE (1991) Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning. Mol Brain Res 11:97-106.
46. Raber J, Wong D, Buttini M, Orth M, Bellosta S, Pitas RE, Mahley RW, Mucke L (1998) Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci USA 95:10914-10919.
47. Raber J, Wong D, Yu G-Q, Buttini M, Mahley RW, Pitas RE, Mucke L (2000) Apolipoprotein E and cognitive performance. Nature 404:352-354.
48. Raber J, Bongers G, LeFevour A, Buttini M, Mucke L (2002) Androgens protect against apolipoprotein E4-induced cognitive deficits. J Neurosci 22:5204-5209.
49. Romas SN, Santana V, Williamson J, Ciappa A, Lee JH, Rondon HZ, Estevez P, Lantigua R, Medrano M, Torres M, Stern Y, Tycko B, Mayeux R (2002) Familial Alzheimer disease among Caribbean Hispanics: a reexamination of its association with APOE. Arch Neurol 59:87-91.
50. Roses AD (1994) The Alzheimer diseases. Curr Neurol 14:111-141.
51. Roses AD (1996) Apolipoprotein E alleles as risk factors in Alzheimer's disease. Annu Rev Med 47:387-400.
52. Saunders AM, Strittmatter WJ, Schmechel D, St George-Hyslop PH, Pericak-Vance MA, Joo SH, Rosi BL, Gusella JF, Crapper-MacLachlan DR, Alberts MJ, Hulette C, Crain B, Goldgaber D, Roses AD (1993) Association of apolipoprotein E allele e4 with late-onset familial and sporadic Alzheimer's disease. Neurology 43:1467-1472.
53. Schauwecker PE, Steward O (1997) Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc Natl Acad Sci USA 94:4103-4108.
54. Selkoe DJ (1991) The molecular pathology of Alzheimer's disease. Neuron 6:487-498.
55. Spinler SA, Cziraky MJ (1994) Lipoprotein(a): physiologic function, association with atherosclerosis, and effects of lipid-lowering drug therapy. Ann Pharmacother 28:343-351.
56. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD (1993a) Apolipoprotein E: high-avidity binding to β-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 90:1977-1981.
57. Strittmatter WJ, Weisgraber KH, Huang DY, Dong L-M, Salvesen GS, Pericak-Vance M, Schmechel D, Saunders AM, Goldgaber D, Roses AD (1993b) Binding of human apolipoprotein E to synthetic amyloid β peptide: isoform-specific effects and implications for late-onset Alzheimer disease. Proc Natl Acad Sci USA 90:8098-8102.
58. Strittmatter WJ, Saunders AM, Goedert M, Weisgraber KH, Dong L-M, Jakes R, Huang DY, Pericak-Vance M, Schmechel D, Roses AD (1994) Isoform-specific interactions of apolipoprotein E with microtubule-associated protein tau: implications for Alzheimer disease. Proc Natl Acad Sci USA 91:11183-11186.
59. Tang M-X, Stern Y, Marder K, Bell K, Gurland B, Lantigua R, Andrews H, Feng L, Tycko B, Mayeux R (1998) The APOE-e4 allele and the risk of Alzheimer disease among African Americans, whites, and Hispanics. JAMA 279:751-755.
60. Tanzi RE, Bertram L (2001) New frontiers in Alzheimer's disease genetics. Neuron 32:181-184.
61. Tesseur I, Van Dorpe J, Spittaels K, Van den Haute C, Moechars D, Van Leuven F (2000a) Expression of human apolipoprotein E4 in neurons causes hyperphosphorylation of protein tau in the brains of transgenic mice. Am J Pathol 156:951-964.
62. Tesseur I, Van Dorpe J, Bruynseels K, Bronfman F, Sciot R, Van Lommel A, Van Leuven F (2000b) Prominent axonopathy and disruption of axonal transport in transgenic mice expressing human apolipoprotein E4 in neurons of brain and spinal cord. Am J Pathol 157:1495-1510.
63. Tolar M, Marques MA, Harmony JAK, Crutcher KA (1997) Neurotoxicity of the 22 kDa thrombin-cleavage fragment of apolipoprotein E and related synthetic peptides is receptor-mediated. J Neurosci 17:5678-5686.
64. Tolar M, Keller JN, Chan S, Mattson MP, Marques MA, Crutcher KA (1999) Truncated apolipoprotein E (apoE) causes increased intracellular calcium and may mediate apoE neurotoxicity. J Neurosci 19:7100-7110.
65. Wisniewski T, Frangione B (1992) Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci Lett 135:235-238.
66. Wisniewski T, Castaño EM, Golabek A, Vogel T, Frangione B (1994) Acceleration of Alzheimer's fibril formation by apolipoprotein E in vitro. Am J Pathol 145:1030-1035.
67. Xu P-T, Schmechel D, Rothrock-Christian T, Burkhart DS, Qiu H-L, Popko B, Sullivan P, Maeda N, Saunders AM, Roses AD, Gilbert JR (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.
68. Xu P-T, Gilbert JR, Qiu H-L, Ervin J, Rothrock-Christian TR, Hulette C, Schmechel DE (1999a) Specific regional transcription of apolipoprotein E in human brain neurons. Am J Pathol 154:601-611.
69. s) is preferentially associated with neuron-enriched cultures from APOE transgenic mice. Neurobiol Dis 6:63-75.