Apolipoprotein-E forms dimers in human frontal cortex and hippocampus

BMC Neuroscience

Volumn 11, Issue , 2010, Pages

  Elliott, David A ^a   Halliday, Glenda M ^a,b   Garner, Brett ^a,c  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; DIMER; DISULFIDE; IODOACETAMIDE; THIOL; THIOL DERIVATIVE; THROMBIN;

ADULT; AGED; ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; BRAIN HOMOGENATE; CELL LYSATE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; HETEROZYGOTE; HIPPOCAMPUS; HOMOZYGOTE; HUMAN; HUMAN TISSUE; MALE; NEUROBLASTOMA CELL; NONHUMAN; PROTEIN ANALYSIS; RABBIT; WESTERN BLOTTING; ANIMAL; CHEMISTRY; FRONTAL LOBE; METABOLISM; METHODOLOGY; MIDDLE AGED; PROTEIN MULTIMERIZATION; TUMOR CELL LINE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; BLOTTING, WESTERN; CELL LINE, TUMOR; DISULFIDES; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; PROTEIN MULTIMERIZATION; RABBITS; SULFHYDRYL COMPOUNDS; THROMBIN;

EID: 77649298679     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-11-23     Document Type: Article

References (52)

1. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240:622-630. 10.1126/science.3283935, 3283935.
2. Ladu MJ, Reardon C, Van Eldik L, Fagan AM, Bu G, Holtzman D, Getz GS. Lipoproteins in the central nervous system. Ann N Y Acad Sci 2000, 903:167-175. 10.1111/j.1749-6632.2000.tb06365.x, 10818504.
3. Rall SC, Weisgraber KH, Innerarity TL, Mahley RW. Structural basis for receptor binding heterogeneity of apolipoprotein E from type III hyperlipoproteinemic subjects. Proc Natl Acad Sci USA 1982, 79:4696-4700. 10.1073/pnas.79.15.4696, 346743, 6289314.
4. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 1993, 261:921-923. 10.1126/science.8346443, 8346443.
5. Strittmatter WJ, Saunders AM, Schmechel D, Pericak-Vance M, Enghild J, Salvesen GS, Roses AD. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc Natl Acad Sci USA 1993, 90:1977-1981. 10.1073/pnas.90.5.1977, 46003, 8446617.
6. LaDu MJ, Gilligan SM, Lukens JR, Cabana VG, Reardon CA, Van Eldik LJ, Holtzman DM. Nascent astrocyte particles differ from lipoproteins in CSF. J Neurochem 1998, 70:2070-2081.
7. Xu Q, Li Y, Cyras C, Sanan DA, Cordell B. Isolation and characterization of apolipoproteins from murine microglia. Identification of a low density lipoprotein-like apolipoprotein J-rich but E-poor spherical particle. J Biol Chem 2000, 275:31770-31777. 10.1074/jbc.M002796200, 10918055.
8. Xu PT, Gilbert JR, Qiu HL, Ervin J, Rothrock-Christian TR, Hulette C, Schmechel DE. Specific regional transcription of apolipoprotein E in human brain neurons. Am J Pathol 1999, 154:601-611. 1850012, 10027417.
9. Boschert U, Merlo-Pich E, Higgins G, Roses AD, Catsicas S. Apolipoprotein E expression by neurons surviving excitotoxic stress. Neurobiol Dis 1999, 6:508-514. 10.1006/nbdi.1999.0251, 10600406.
10. Metzger RE, LaDu MJ, Pan JB, Getz GS, Frail DE, Falduto MT. Neurons of the human frontal cortex display apolipoprotein E immunoreactivity: implications for Alzheimer's disease. J Neuropathol Exp Neurol 1996, 55:372-380. 10.1097/00005072-199603000-00013, 8786396.
11. Elliott DA, Kim WS, Jans DA, Garner B. Apoptosis induces neuronal apolipoprotein-E synthesis and localization in apoptotic bodies. Neurosci Lett 2007, 416:206-210. 10.1016/j.neulet.2007.02.014, 17320289.
12. Mahley RW, Nathan BP, Pitas RE. Apolipoprotein E. Structure, function, and possible roles in Alzheimer's disease. Ann N Y Acad Sci 1996, 777:139-145. 10.1111/j.1749-6632.1996.tb34412.x, 8624076.
13. Miyata M, Smith JD. Apolipoprotein E allele-specific antioxidant activity and effects on cytotoxicity by oxidative insults and beta-amyloid peptides. Nat Genet 1996, 14:55-61. 10.1038/ng0996-55, 8782820.
14. Strittmatter WJ, Weisgraber KH, Goedert M, Saunders AM, Huang D, Corder EH, Dong LM, Jakes R, Alberts MJ, Gilbert JR, et al. Hypothesis: microtubule instability and paired helical filament formation in the Alzheimer disease brain are related to apolipoprotein E genotype. Exp Neurol 1994, 125:163-171. discussion 172-164, 10.1006/exnr.1994.1019, 8313935.
15. Mahley RW, Rall SC. Apolipoprotein E: far more than a lipid transport protein. Annu Rev Genomics Hum Genet 2000, 1:507-537. 10.1146/annurev.genom.1.1.507, 11701639.
16. Arai H, Kashiwagi S, Nagasaka Y, Uchida K, Hoshii Y, Nakamura K. Oxidative modification of apolipoprotein E in human very-low-density lipoprotein and its inhibition by glycosaminoglycans. Arch Biochem Biophys 1999, 367:1-8. 10.1006/abbi.1999.1222, 10375392.
17. Jordan J, Galindo MF, Miller RJ, Reardon CA, Getz GS, LaDu MJ. Isoform-specific effect of apolipoprotein E on cell survival and beta-amyloid-induced toxicity in rat hippocampal pyramidal neuronal cultures. J Neurosci 1998, 18:195-204.
18. Beffert U, Aumont N, Dea D, Lussier-Cacan S, Davignon J, Poirier J. Apolipoprotein E isoform-specific reduction of extracellular amyloid in neuronal cultures. Brain Res Mol Brain Res 1999, 68:181-185. 10.1016/S0169-328X(99)00073-X, 10320795.
19. Bell RD, Sagare AP, Friedman AE, Bedi GS, Holtzman DM, Deane R, Zlokovic BV. Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system. J Cereb Blood Flow Metab 2007, 27:909-918.
20. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, et al. ApoE promotes the proteolytic degradation of Abeta. Neuron 2008, 58:681-693. 10.1016/j.neuron.2008.04.010, 2493297, 18549781.
21. Xu Q, Brecht WJ, Weisgraber KH, Mahley RW, Huang Y. Apolipoprotein E4 domain interaction occurs in living neuronal cells as determined by fluorescence resonance energy transfer. J Biol Chem 2004, 279:25511-25516. 10.1074/jbc.M311256200, 15054100.
22. LaDu MJ, Falduto MT, Manelli AM, Reardon CA, Getz GS, Frail DE. Isoform-specific binding of apolipoprotein E to beta-amyloid. J Biol Chem 1994, 269:23403-23406.
23. Tokuda T, Calero M, Matsubara E, Vidal R, Kumar A, Permanne B, Zlokovic B, Smith JD, Ladu MJ, Rostagno A, et al. Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid beta peptides. Biochem J 2000, 348(Pt 2):359-365. 10.1042/0264-6021:3480359, 1221074, 10816430.
24. Morrow JA, Segall ML, Lund-Katz S, Phillips MC, Knapp M, Rupp B, Weisgraber KH. Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain. Biochemistry 2000, 39:11657-11666. 10.1021/bi000099m, 10995233.
25. Clement-Collin V, Barbier A, Dergunov AD, Visvikis A, Siest G, Desmadril M, Takahashi M, Aggerbeck LP. The structure of human apolipoprotein E2, E3 and E4 in solution. 2. Multidomain organization correlates with the stability of apoE structure. Biophys Chem 2006, 119:170-185. 10.1016/j.bpc.2005.07.009, 16125836.
26. Marques MA, Tolar M, Harmony JA, Crutcher KA. A thrombin cleavage fragment of apolipoprotein E exhibits isoform-specific neurotoxicity. Neuroreport 1996, 7:2529-2532. 10.1097/00001756-199611040-00025, 8981417.
27. Tolar M, Marques MA, Harmony JA, Crutcher KA. Neurotoxicity of the 22 kDa thrombin-cleavage fragment of apolipoprotein E and related synthetic peptides is receptor-mediated. J Neurosci 1997, 17:5678-5686.
28. Huang Y, Liu XQ, Wyss-Coray T, Brecht WJ, Sanan DA, Mahley RW. Apolipoprotein E fragments present in Alzheimer's disease brains induce neurofibrillary tangle-like intracellular inclusions in neurons. Proc Natl Acad Sci USA 2001, 98:8838-8843. 10.1073/pnas.151254698, 37522, 11447277.
29. Elliott DA, Tsoi K, Holinkova S, Chan SL, Kim WS, Halliday GM, Rye KA, Garner B. Isoform-specific proteolysis of apolipoprotein-E in the brain. Neurobiol Aging 2010,
30. Weisgraber KH, Shinto LH. Identification of the disulfide-linked homodimer of apolipoprotein E3 in plasma. Impact on receptor binding activity. J Biol Chem 1991, 266:12029-12034.
31. LaDu MJ, Lukens JR, Reardon CA, Getz GS. Association of human, rat, and rabbit apolipoprotein E with beta-amyloid. J Neurosci Res 1997, 49:9-18. 10.1002/(SICI)1097-4547(19970701)49:1<9::AID-JNR2>3.0.CO;2-H, 9211985.
32. Montine KS, Bassett CN, Ou JJ, Markesbery WR, Swift LL, Montine TJ. Apolipoprotein E allelic influence on human cerebrospinal fluid apolipoproteins. J Lipid Res 1998, 39:2443-2451.
33. Rebeck GW, Alonzo NC, Berezovska O, Harr SD, Knowles RB, Growdon JH, Hyman BT, Mendez AJ. Structure and functions of human cerebrospinal fluid lipoproteins from individuals of different APOE genotypes. Exp Neurol 1998, 149:175-182. 10.1006/exnr.1997.6710, 9454626.
34. Sun Y, Wu S, Bu G, Onifade MK, Patel SN, LaDu MJ, Fagan AM, Holtzman DM. 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 1998, 18:3261-3272.
35. Innerarity TL, Mahley RW, Weisgraber KH, Bersot TP. Apoprotein (E-A-II) complex of human plasma lipoproteins. II. Receptor binding activity of a high density lipoprotein subfraction modulated by the apo(E--A-II) complex. J Biol Chem 1978, 253:6289-6295.
36. Yamauchi K, Tozuka M, Hidaka H, Nakabayashi T, Sugano M, Kondo Y, Nakagawara A, Katsuyama T. Effect of apolipoprotein AII on the interaction of apolipoprotein E with beta-amyloid: some apo(E-AII) complexes inhibit the internalization of beta-amyloid in cultures of neuroblastoma cells. J Neurosci Res 2000, 62:608-614. 10.1002/1097-4547(20001115)62:4<608::AID-JNR16>3.0.CO;2-4, 11070505.
37. Yamauchi K, Tozuka M, Nakabayashi T, Sugano M, Hidaka H, Kondo Y, Katsuyama T. Higher avidity binding of apolipoprotein (E-AII) complex than of apolipoprotein E monomer to beta-amyloid. J Neurosci Res 1999, 58:301-307. 10.1002/(SICI)1097-4547(19991015)58:2<301::AID-JNR10>3.0.CO;2-9, 10502286.
38. Minagawa H, Gong JS, Jung CG, Watanabe A, Lund-Katz S, Phillips MC, Saito H, Michikawa M. Mechanism underlying apolipoprotein E (ApoE) isoform-dependent lipid efflux from neural cells in culture. J Neurosci Res 2009, 87:2498-2508. 10.1002/jnr.22073, 19326444.
39. Bradley WA, Gilliam EB, Gotto AM, Gianturco SH. Apolipoprotein-E degradation in human very low density lipoproteins by plasma protease(s): chemical and biological consequences. Biochem Biophys Res Commun 1982, 109:1360-1367. 10.1016/0006-291X(82)91927-1, 6301435.
40. Bode W. Structure and interaction modes of thrombin. Blood Cells Mol Dis 2006, 36:122-130. 10.1016/j.bcmd.2005.12.027, 16480903.
41. Huntington JA. Molecular recognition mechanisms of thrombin. J Thromb Haemost 2005, 3:1861-1872. 10.1111/j.1538-7836.2005.01363.x, 16102053.
42. Caillet-Boudin ML, Dupont-Wallois L, Soulie C, Delacourte A. Apolipoprotein E and Tau phosphorylation in human neuroblastoma cells. Neurosci Lett 1998, 250:83-86. 10.1016/S0304-3940(98)00448-0, 9697924.
43. Dupont-Wallois L, Soulie C, Sergeant N, Wavrant-de Wrieze N, Chartier-Harlin MC, Delacourte A, Caillet-Boudin ML. ApoE synthesis in human neuroblastoma cells. Neurobiol Dis 1997, 4:356-364. 10.1006/nbdi.1997.0155, 9440124.
44. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc Natl Acad Sci USA 1998, 95:6460-6464. 10.1073/pnas.95.11.6460, 27798, 9600988.
45. 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 2002, 22:1679-1689.
46. Kim WS, Suryo Rahmanto A, Kamili A, Rye KA, Guillemin GJ, Gelissen IC, Jessup W, Hill AF, Garner B. Role of ABCG1 and ABCA1 in regulation of neuronal cholesterol efflux to apolipoprotein-E discs and suppression of amyloid-beta peptide generation. J Biol Chem 2007, 282:2851-2861. 10.1074/jbc.M607831200, 17121837.
47. Kim WS, Weickert CS, Garner B. Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. J Neurochem 2008, 104:1145-1166. 10.1111/j.1471-4159.2007.05099.x, 17973979.
48. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 1991, 41:479-486.
49. NIA Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Aging 1997, 18:S1-2. 10.1016/S0197-4580(97)00057-2, 9330978, NIA.
50. West MJ, Coleman PD, Flood DG, Troncoso JC. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772. 10.1016/S0140-6736(94)92338-8, 7916070.
51. Furukawa Y, Fu R, Deng HX, Siddique T, O'Halloran TV. Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu, Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc Natl Acad Sci USA 2006, 103:7148-7153. 10.1073/pnas.0602048103, 1447524,1447524, 16636274.
52. Ellman GL. Tissue sulfhydryl groups. Arch Biochem Biophys 1959, 82:70-77. 10.1016/0003-9861(59)90090-6, 13650640.