Increased ATP-binding cassette transporter A1 expression in Alzheimer's disease hippocampal neurons

Journal of Alzheimer's Disease

Volumn 21, Issue 1, 2010, Pages 193-205

  Kim, Woojin Scott ^a,b   Bhatia, Surabhi ^a   Elliott, David A ^a   Agholme, Lotta ^a   Kgedal, Katarina ^a   McCann, Heather ^a   Halliday, Glenda M ^a,b   Barnham, Kevin J ^c   Garner, Brett ^a,d  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

ABCA1; Alzheimer's disease; amyloid peptide; ATP binding cassette transporter A1; hippocampus; neurodegeneration

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN E; MESSENGER RNA; PUMA PROTEIN; ABC TRANSPORTER; ABCA1 PROTEIN, HUMAN; APOPTOSIS REGULATORY PROTEIN; BBC3 PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BINDING;

AGED; ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE; UPREGULATION; AGE; ANIMAL; CEREBELLUM; CHO CELL LINE; CRICETULUS; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HAMSTER; METABOLISM; NEUROBLASTOMA; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TIME; TUMOR CELL LINE; VERY ELDERLY;

AGE FACTORS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEINS E; APOPTOSIS REGULATORY PROTEINS; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; CEREBELLUM; CHO CELLS; CRICETINAE; CRICETULUS; FEMALE; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; MALE; MICE; NEUROBLASTOMA; NEURONS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RNA, MESSENGER; TIME FACTORS; TRANSFECTION;

EID: 77953285846     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100324     Document Type: Article

References (83)

1. Hung LW, Wang IX, Nikaido K, Liu PQ, Ames GF, Kim SH (1998) Crystal structure of the ATP-binding subunit of an ABC transporter. Nature 396, 703-707.
2. Klein I, Sarkadi B, Varadi A (1999) An inventory of the human ABC proteins. Biochim BiophysActa 1461, 237-262.
3. Higgins CF, Linton KJ (2004) The ATP switch model for ABC transporters. Nat Struct Mol Biol 11, 918-926.
4. Oram JF, Lawn RM (2001) ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J Lipid Res 42, 1173-1179.
5. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO, Loubser O, Ouelette BF, Fichter K, Ashbourne-Excoffon KJ, Sensen CW, Scherer S, Mott S, Denis M, Martindale D, Frohlich J, Morgan K, Koop B, Pimstone S, Kastelein JJ, Gen-est J, Jr., Hayden MR (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22, 336-345. (Pubitemid 29369523)
6. Bodzioch M, Orso E, Klucken J, Langmann T, Bottcher A, Diederich W, Drobnik W, Barlage S, Buchler C, Porsch-Ozcurumez M, Kaminski WE, Hahmann HW, Oette K, Rothe G, Aslanidis C, Lackner KJ, Schmitz G (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. NatGenet 22, 347-351.
7. Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, Deleuze JF, Brewer HB, Duverger N, Denefle P, Assmann G (1999) Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat Genet 22, 352-355.
8. Luciani MF, Denizot F, Savary S, Mattei MG, Chimini G (1994) Cloning of two novel ABC transporters mapping on human chromosome 9. Genomics 21, 150-159.
9. Langmann T., Klucken J, Reil M, Liebisch G, Luciani MF, Chimini G, Kaminski WE, Schmitz G (1999) Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem Biophys Res Commun 257, 29-33.
10. Vance JE, Hayashi H, Karten B (2005) Cholesterol homeostasis in neurons and glial cells. Semin CellDevBiol 16, 193-212.
11. Hirsch-Reinshagen V, Wellington CL (2007) Cholesterol metabolism, apolipoprotein E, adenosine triphosphate-binding cassette transporters, and Alzheimer's disease. Curr Opin Lipidol 18, 325-332.
12. Koldamova R, Leffterov I (2007) Role of LXR and ABCA1 in the pathogenesis of Alzheimer's disease-implications for a new therapeutic approach. Curr Alzheimer Res 4, 171-178.
13. Kim WS, Suryo Rahmanto A, Kamili A, Rye KA, Guillemin GJ, Gelissen IC, Jessup W, Hill AF, Garner B (2007) 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 282, 2851-2861.
14. Kim WS, Weickert CS, Garner B (2008) Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. JNeurochem 104, 1145-1166.
15. Wellington CL, Walker EK, Suarez A, Kwok A, Bissada N, Singaraja R, Yang YZ, Zhang LH, James E, Wilson JE, Fran-cone O, McManus BM, Hayden MR (2002) ABCA1 mR-NA and protein distribution patterns predict multiple different roles and levels of regulation. Lab Invest 82, 273-283.
16. Koldamova RP, Leffterov IM, Ikonomovic MD, Skoko J, Lefterov PI, Isanski BA, DeKosky ST, Lazo JS (2003) 22R-hydroxycholesterol and 9-cis-retinoic acid induce ATP-binding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid beta secretion. J Biol Chem 278, 13244-13256.
17. Hirsch-Reinshagen V, Zhou S, Burgess BL, Bernier L, McIsaac SA, Chan JY, Tansley GH, Cohn JS, Hayden MR, Wellington CL (2004) Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain. J Biol Chem 279, 41197-41207.
18. Tachikawa M, Watanabe M, Hori S, Fukaya M, Ohtsuki S, Asashima T, Terasaki T (2005) Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain. J Neurochem 95, 294-304.
19. Kim WS, Guillemin GJ, Glaros EN, Lim CK, Garner B (2006) Quantitation of ATP-binding cassette subfamily-A transporter gene expression in primary human brain cells. Neuroreport 17, 891-896.
20. Wahrle SE, Jiang H, Parsadanian M, Legleiter J, Han X, Fryer JD, Kowalewski T, Holtzman DM (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipi-dation of astrocyte-secreted apoE. J Biol Chem 279, 4098740993.
21. Karten B, Campenot RB, Vance DE, Vance JE (2006) Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J Biol Chem 281, 4049-4057.
22. Abildayeva K, Jansen PJ, Hirsch-Reinshagen V, Bloks VW, Bakker AH, Ramaekers FC, de Vente J, Groen AK, Wellington CL, Kuipers F, Mulder M (2006) 24(S)-hydroxycholesterol participates in a liver X receptor-controlled pathway in as-trocytes that regulates apolipoprotein E-mediated cholesterol efflux. J Biol Chem 281, 12799-12808.
23. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58, 681-693.
24. Sun Y, Yao J, Kim TW, Tall AR (2003) Expression of liver X receptor target genes decreases cellular amyloid beta peptide secretion. J Biol Chem 278, 27688-27694.
25. Brown J, 3rd, Theisler C, Silberman S, Magnuson D, Gottardi-Littell N, Lee JM, Yager D, Crowley J, Sambamurti K, Rahman MM, Reiss AB, Eckman CB, Wolozin B (2004) Differential expression of cholesterol hydroxylases in Alzheimer's disease. J Biol Chem 279, 34674-34681. (Pubitemid 39318097)
26. Burns MP, Vardanian L, Pajoohesh-Ganji A, Wang L, Cooper M, Harris DC, Duff K, Rebeck GW (2006) The effects of ABCA1 on cholesterol efflux and Abeta levels in vitro and in vivo. J Neurochem 98, 792-800.
27. Kim WS, Chan SL, Hill AF, Guillemin GJ, Garner B (2009) Impact of 27-hydroxycholesterol on amyloid-beta peptide production and ATP-binding cassette transporter expression in primary human neurons. JAlzheimers Dis 16, 121-131.
28. West MJ, Coleman PD, Flood DG, Troncoso JC (1994) Differences in the pattern ofhippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344, 769-772.
29. Fukumoto H, Deng A, Irizarry MC, Fitzgerald ML, Rebeck GW (2002) Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Abeta levels. J Biol Chem 277, 48508-48513.
30. NIA (1997) 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 18, S1-2.
31. Gregory GC, Macdonald V, Schofield PR, Kril JJ, Halliday GM (2006) Differences in regional brain atrophy in genetic forms of Alzheimer's disease. Neurobiol Aging 27, 387-393.
32. Mexal S, Berger R, Adams CE, Ross RG, Freedman R, Leonard S (2006) Brain pH has a significant impact on human postmortem hippocampal gene expression profiles. Brain Res 1106, 1-11.
33. Monoranu CM, Apfelbacher M, Grunblatt E, Puppe B, Ala-fuzoff I, Ferrer I, Al-Saraj S, Keyvani K, Schmitt A, Falkai P, Schittenhelm J, Halliday G, Kril J, Harper C, McLean C, Riederer P, Roggendorf W (2009) pH measurement as quality control on human post mortem brain tissue: a study of the BrainNet Europe consortium. Neuropathol Appl Neurobiol 35, 329-337.
34. Jankowsky JL, Fadale DJ, Anderson J, Xu GM, Gonzales V, Jenkins NA, Copeland NG, Lee MK, Younkin LH, Wagner SL, Younkin SG, Borchelt DR (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. HumMol Genet 13, 159-170.
35. Reiserer RS, Harrison FE, Syverud DC, McDonald MP (2007) Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav 6, 54-65.
36. Elliott DA, Tsoi K, Holinkova S, Chan SL, Kim WS, Halliday GM, Rye KA, Garner B (2010) Isoform-specific proteolysis of apolipoprotein-E in the brain. Neurobiol Aging. in press
37. Broe M, Shepherd CE, Mann DM, Milward EA, Gai WP, Thiel E, Halliday GM (2005) Insoluble alpha-synuclein in Alzheimer's disease without Lewy body formation. Neurotox Res 7, 69-76.
38. White AR, Du T, Laughton KM, Volitakis I, Sharples RA, Xilinas ME, Hoke DE, Holsinger RM, Evin G, Cherny RA, Hill AF, Barnham KJ, Li QX, Bush AI, Masters CL (2006) Degradation of the Alzheimer disease amyloid beta-peptide by metal-dependent up-regulation ofmetalloprotease activity. J Biol Chem 281, 17670-17680.
39. Koldamova R, Staufenbiel M, Lefterov I (2005) Lack of AB-CA1 considerably decreases brain Apoe level and increases amyloid deposition in APP23 mice. J Biol Chem 280, 4322443235.
40. Wahrle SE, Jiang H, Parsadanian M, Kim J, Li A, Knoten A, Jain S, Hirsch-Reinshagen V, Wellington CL, Bales KR, Paul SM, Holtzman DM (2008) Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease. J Clin Invest 118, 671-682.
41. Quinn CM, Kagedal K, Terman A, Stroikin U, Brunk UT, Jes-sup W, Garner B (2004) Induction of fibroblast apolipopro-tein E expression during apoptosis, starvation-induced growth arrest and mitosis. BiochemJ 378, 753-761.
42. Mahley RW (1988) Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622630.
43. Elliott DA, Kim WS, Jans DA, Garner B (2007) Apoptosis induces neuronal apolipoprotein-E synthesis and localization in apoptotic bodies. Neurosci Lett 416, 206-210.
44. Steckley D, Karajgikar M, Dale LB, Fuerth B, Swan P, Drummond-Main C, Poulter MO, Ferguson SS, Strasser A, Cregan SP (2007) Puma is a dominant regulator of oxida-tive stress induced Bax activation and neuronal apoptosis. J Neurosci 27, 12989-12999.
45. Cregan SP, Arbour NA, Maclaurin JG, Callaghan SM, Fortin A, Cheung EC, Guberman DS, Park DS, Slack RS (2004) p53 activation domain 1 is essential for PUMA upregulation and p53-mediated neuronal cell death. J Neurosci 24, 1000310012.
46. Reimertz C, Kogel D, Rami A, Chittenden T, Prehn JH (2003) Gene expression during ER stress-induced apoptosis in neurons: induction of the BH3-only protein Bbc3/PUMA and activation of the mitochondrial apoptosis pathway. J Cell Biol 162, 587-597.
47. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocam-pal long-term potentiation in vivo. Nature 416, 535-539.
48. Hung LW, Ciccotosto GD, Giannakis E, Tew DJ, Perez K, Masters CL, Cappai R, Wade JD, Barnham KJ (2008) Amyloid-beta peptide (Abeta) neurotoxicity is modulated by the rate of peptide aggregation: Abeta dimers and trimers correlate with neurotoxicity. J Neurosci 28, 11950-11958.
49. Ono K, Condron MM, Teplow DB (2009) Structure-neurotoxicity relationships ofamyloid beta-protein oligomers. Proc Natl Acad Sci USA 106, 14745-14750.
50. Wollmer MA, Streffer JR, Lutjohann D, Tsolaki M, Iakovi-dou V, Hegi T, Pasch T, Jung HH, Bergmann K, Nitsch RM, Hock C, Papassotiropoulos A (2003) ABCA1 modulates CSF cholesterol levels and influences the age at onset of Alzheimer's disease. Neurobiol Aging. 24, 421-426.
51. Katzov H, Chalmers K, Palmgren J, Andreasen N, Johansson Cairns NJ, Gatz M, Wilcock GK, Love S, Pedersen NL, Brookes AJ, Blennow K, Kehoe PG, Prince JA (2004) Genetic variants of ABCA1 modify Alzheimer disease risk and quantitative traits related to beta-amyloid metabolism. Hum Mutat 23, 358-367.
52. Sundar PD, Feingold E, Minster RL, DeKosky ST, Kamboh MI (2007) Gender-specific association of ATP-binding cassette transporter 1 (ABCA1) polymorphisms with the risk of late-onset Alzheimer's disease. Neurobiol Aging 28, 856-862.
53. Wang F, Jia J (2007) Polymorphisms of cholesterol metabolism genes CYP46 and ABCA1 and the risk of sporadic Alzheimer's disease in Chinese. Brain Res 1147, 34-38.
54. Wavrant-De Vrieze F, Compton D, Womick M, Arepalli S, Adighibe O, Li L, Perez-Tur J, Hardy J (2007) ABCA1 polymorphisms and Alzheimer's disease. Neurosci Lett 416, 180183.
55. Chu LW, Li Y, Li Z, Tang AY, Cheung BM, Leung RY, Yik PY, Jin DY, Song YQ (2007) A novel intronic polymorphism of ABCA1 gene reveals risk for sporadic Alzheimer's disease in Chinese. Am J Med Genet B Neuropsychiatr Genet 144B, 1007-1013.
56. Rodriguez-Rodriguez E, Mateo I, Llorca J, Sanchez-Quintana I, Infante J, Garcia-Gorostiaga I, Sanchez-Juan P, Berciano J, Combarros O (2007) Association of genetic variants of AB-CA1 with Alzheimer's disease risk. Am J Med Genet B Neu-ropsychiatr Genet 144B, 964-968.
57. Reynolds CA, Hong MG, Eriksson UK, Blennow K, Bennet AM, Johansson B, Malmberg B, Berg S, Wiklund F, Gatz M, Pedersen NL, Prince JA (2009) A survey of ABCA1 sequence variation confirms association with dementia. Hum Mutat 30, 1348-1354.
58. Wahrle SE, Jiang H, Parsadanian M, Hartman RE, Bales KR, Paul SM, Holtzman DM (2005) Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer's disease. J Biol Chem 280, 43236-43242.
59. Hirsch-Reinshagen V, Maia LF, Burgess BL, Blain JF, Naus KE, McIsaac SA, Parkinson PF, Chan JY, Tansley GH, Hayden MR, Poirier J, Van Nostrand W, Wellington CL (2005) The absence of ABCA1 decreases soluble apoE levels but does not diminish amyloid deposition in two murine models of Alzheimer's disease. J Biol Chem 280, 43243-43256.
60. Hirsch-Reinshagen V, Chan JY, Wilkinson A, Tanaka T, Fan J, Ou G, Maia LF, Singaraja RR, Hayden MR, Wellington CL (2007) Physiologically regulated transgenic ABCA1 does not reduce amyloid burden or amyloid-beta peptide levels in vivo. J Lipid Res 48, 914-923.
61. Karasinska JM, Rinninger F, Lutjohann D, Ruddle P, Franciosi S, Kruit JK, Singaraja RR, Hirsch-Reinshagen V, Fan J, Brun-ham LR, Bissada N, Ramakrishnan R, Wellington CL, Parks JS, Hayden MR (2009) Specific loss of brain ABCA1 increases brain cholesterol uptake and influences neuronal structure and function. J Neurosci 29, 3579-3589.
62. Koldamova RP, Lefterov IM, Staufenbiel M, Wolfe D, Huang S, Glorioso JC, Walter M, Roth MG, Lazo JS (2005) The liver X receptor ligand T0901317 decreases amyloid beta production in vitro and in a mouse model of Alzheimer's disease. J Biol Chem 280, 4079-4088.
63. Zelcer N, Khanlou N, Clare R, Jiang Q, Reed-Geaghan EG, Landreth GE, Vinters HV, Tontonoz P (2007) Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors. Proc Natl Acad Sci USA 104, 10601-10606.
64. Riddell DR, Zhou H, Comery TA, Kouranova E, Lo CF, Warwick HK, Ring RH, Kirksey Y, Aschmies S, Xu J, Kubek K, Hirst WD, Gonzales C, Chen Y, Murphy E, Leonard S, Va-sylyev D, Oganesian A, Martone RL, Pangalos MN, Reinhart PH, Jacobsen JS (2007) The LXR agonist TO901317 selectively lowers hippocampal Abeta42 and improves memory in the Tg2576 mouse model of Alzheimer's disease. Mol Cell Neurosci 34, 621-628.
65. Niizuma K, Endo H, Nito C, Myer DJ, Chan PH (2009) Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia. Stroke 40, 618-625.
66. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW (2004) Incipient Alzheimer's disease: micro array correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci U S A 101, 2173-2178.
67. Akram A, Schmeidler J, Katsel P, Hof PR, Haroutunian V (2010) Increased expression of cholesterol transporter AB-CA1 is highly correlated with severity of dementia in AD hippocampus. Brain Res 1318, 167-177.
68. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30, 207-210.
69. Heverin M, Bogdanovic N, Lutjohann D, Bayer T, Pikuleva I, Bretillon L, Diczfalusy U, Winblad B, Bjorkhem I (2004) Changes in the levels of cerebral and extracerebral sterols in the brain ofpatients with Alzheimer's disease. J Lipid Res 45, 186-193.
70. Heverin M, Meaney S, Lutjohann D, Diczfalusy U, Wahren J, Bjorkhem I (2005) Crossing the barrier: net flux of 27-hydroxycholesterol into the human brain. J Lipid Res 46, 10471052.
71. Fu X, Menke JG, Chen Y, Zhou G, MacNaul KL, Wright SD, Sparrow CP, Lund EG (2001) 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J Biol Chem 276, 38378-38387.
72. Gylys KH, Fein JA, Yang F, Miller CA, Cole GM (2007) Increased cholesterol in Abeta-positive nerve terminals from Alzheimer's disease cortex. Neurobiol Aging 28, 8-17.
73. Smith JD, Waelde C, Horwitz A, Zheng P (2002) Evaluation of the role of phosphatidylserine translocase activity in ABCA1-mediated lipid efflux. J Biol Chem 277, 17797-17803.
74. Buechler C, Bared SM, Aslanidis C, Ritter M, Drobnik W, Schmitz G (2002) Molecular and functional interaction of the ATP-binding cassette transporter A1 with Fas-associated death domain protein. J Biol Chem 277, 41307-41310.
75. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, Ratovit-sky T, Regard J, Copeland NG, Jenkins NA, Sisodia SS, Price DL (1996) A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet Anal 13, 159-163. (Pubitemid 27063321)
76. Simons M, Keller P, De Strooper B, Beyreuther K, Dotti CG, Simons K (1998) Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc Natl Acad Sci USA 95,6460-6464.
77. Ehehalt R, Keller P, Haass C, Thiele C, Simons K (2003) Amy-loidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160, 113-123.
78. Kalvodova L, Kahya N, Schwille P, Ehehalt R, Verkade P, Drechsel D, Simons K (2005) Lipids as modulators of prote-olytic activity ofBACE: involvement ofcholesterol, glycosph-ingolipids, and anionic phospholipids in vitro. J Biol Chem 280, 36815-36823.
79. Vetrivel KS, Cheng H, Kim SH, Chen Y, Barnes NY, Parent AT, Sisodia SS, Thinakaran G (2005) Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J Biol Chem 280, 25892-25900.
80. Osenkowski P, Ye W, Wang R, Wolfe MS, Selkoe DJ (2008) Direct and potent regulation of gamma-secretase by its lipid microenvironment. J Biol Chem 283, 22529-22540.
81. Guardia-Laguarta C, Coma M, Pera M, Clarimon J, Sereno L, Agullo JM, Molina-Porcel L, Gallardo E, Deng A, Bere-zovska O, Hyman BT, Blesa R, Gomez-Isla T, Lleo A (2009) Mild cholesterol depletion reduces amyloid-beta production by impairing APP trafficking to the cell surface. J Neurochem 110, 220-230.
82. Herculano-Houzel S, Lent R (2005) Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J Neurosci 25, 2518-2521.
83. Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104, 3562-3567.