Increased expression of cholesterol transporter ABCA1 is highly correlated with severity of dementia in AD hippocampus

Brain Research

Volumn 1318, Issue , 2010, Pages 167-177

  Akram, Afia ^a   Schmeidler, James ^a   Katsel, Pavel ^a   Hof, Patrick R ^a   Haroutunian, Vahram ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

ABCA1; Alzheimer's disease; Cholesterol; Dementia; Hippocampus

Indexed keywords

ABC TRANSPORTER A1; CHOLESTEROL; MESSENGER RNA;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CADAVER; CELL MEMBRANE; CHOLESTEROL TRANSPORT; COGNITION; CONTROLLED STUDY; DEMENTIA; DISEASE COURSE; DISEASE SEVERITY; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RATING SCALE; RNA TRANSLATION; WESTERN BLOTTING;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ATP-BINDING CASSETTE TRANSPORTERS; BLOTTING, WESTERN; COHORT STUDIES; FEMALE; HIPPOCAMPUS; HUMANS; MALE; POLYMERASE CHAIN REACTION; PSYCHIATRIC STATUS RATING SCALES; RNA, MESSENGER; SENILE PLAQUES; SEVERITY OF ILLNESS INDEX;

EID: 76449103011     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.01.006     Document Type: Article

References (93)

1. Abad-Rodriguez J., Ledesma M.D., Craessaerts K., Perga S., Medina M., Delacourte A., Dingwall C., De Strooper B., and Dotti C.G. Neuronal membrane cholesterol loss enhances amyloid peptide generation. J. Cell Biol. 167 (2004) 953-960
2. Akram A., Katsel P., Hof P.R., and Haroutunian V. Coordinated transcriptional and translational changes in cholesterol transporters correlate with cognitive decline in Alzheimer's disease. Program No. 45.8. 2008 Neuroscience Meeting Planner (2008), Society for Neuroscience, Washington, DC Online
3. Akram A., Katsel P., Hof P.R., and Haroutunian V. Changes in the expression of genes involved in cholesterol trafficking with the progression of Alzheimer's disease. Program No. 795.9. 2007 Neuroscience Meeting Planner (2007), Society for Neuroscience, San Diego, CA Online
4. Arispe N., and Doh M. Plasma membrane cholesterol controls the cytotoxicity of Alzheimer's disease Aβ(1-40) and (1-42) peptides. FASEB J. 16 (2002) 1526-1536
5. Bair W. Visual receptive field organization. Curr. Opin. Neurobiol. 15 (2005) 459-464
6. Barton A.J., Pearson R.C., Najlerahim A., and Harrison P.J. Pre- and postmortem influences on brain RNA. J. Neurochem. 61 (1993) 1-11
7. Bauer D.E., Haroutunian V., McCullumsmith R.E., and Meador-Woodruff J.H. Expression of four housekeeping proteins in elderly patients with schizophrenia. J. Neural. Transm. 116 (2009) 487-491
8. Blanchette-Mackie E.J., Dwyer N.K., Amende L.M., Kruth H.S., Butler J.D., Sokol J., Comly M.E., Vanier M.T., August J.T., Brady R.O., and Pentchev P.G. Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 8022-8026
9. Bodovitz S., and Klein W.L. Cholesterol modulates alpha-secretase cleavage of amyloid precursor protein. J. Biol. Chem. 271 (1996) 4436-4440
10. Bodzioch M., Orso E., Klucken J., Langmann T., Bottcher A., Diederich W., Drobnik W., Barlage S., Buchler C., Porsch-Ozcurumez M., Kaminski W.E., Hahmann H.W., Oette K., Rothe G., Aslanidis C., Lackner K.J., and Schmitz G. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22 (1999) 347-351
11. Bouras C., Hof P.R., Giannakopoulos P., Michel J.P., and Morrison J.H. Regional distribution of neurofibrillary tangles and senile plaques in the cerebral cortex of elderly patients: a quantitative evaluation of a one-year autopsy population from a geriatric hospital. Cereb. Cortex 4 (1994) 138-150
12. Braak H., and Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. (Berl.) 82 (1991) 239-259
13. Brooks-Wilson A., et al. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22 (1999) 336-345
14. Brown M.S., and Goldstein J.L. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11041-11048
15. Burke W.J., Miller J.P., Rubin E.H., Morris J.C., Coben L.A., Duchek J., Wittels I.G., and Berg L. Reliability of the Washington University Clinical Dementia Rating. Arch. Neurol. 45 (1988) 31-32
16. Burns M.P., Vardanian L., Pajoohesh-Ganji A., Wang L., Cooper M., Harris D.C., Duff K., and Rebeck G.W. The effects of ABCA1 on cholesterol efflux and Abeta levels in vitro and in vivo. J. Neurochem. 98 (2006) 792-800
17. Byne W., Dracheva S., Chin B., Schmeidler J.M., Davis K.L., and Haroutunian V. Schizophrenia and sex-associated differences in the expression of neuronal and oligodendrocyte specific genes in individual thalamic nuclei. Schizophr. Res. 98 (2008) 118-128
18. Chomczynski P., and Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162 (1987) 156-159
19. Combes V., Coltel N., Alibert M., van Eck M., Raymond C., Juhan-Vague I., Grau G.E., and Chimini G. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am. J. Pathol. 166 (2005) 295-302
20. 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. Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's Disease in late onset families. Science 261 (1993) 921-923
21. Crameri A., Biondi E., Kuehnle K., Lutjohann D., Thelen K.M., Perga S., Dotti C.G., Nitsch R.M., Ledesma M.D., and Mohajeri M.H. The role of seladin-1/DHCR24 in cholesterol biosynthesis, APP processing and Abeta generation in vivo. EMBO J. 25 (2006) 432-443
22. Dietschy J.M., and Turley S.D. Cholesterol metabolism in the brain. Curr. Opin. Lipidol. 12 (2001) 105-112
23. Distl R., Treiber-Held S., Albert F., Meske V., Harzer K., and Ohm T.G. Cholesterol storage and tau pathology in Niemann-Pick type C disease in the brain. J. Pathol. 200 (2003) 104-111
24. Dracheva S., Elhakem S.L., Gluck M.R., Siever L.J., Davis K.L., and Haroutunian V. Glutamate synthesis and NMDA receptor and PSD-95 expression in DLPFC and occipital cortices of schizophrenics (2001), Society for Neuroscience Abstracts
25. Duong P.T., Collins H.L., Nickel M., Lund-Katz S., Rothblat G.H., and Phillips M.C. Characterization of nascent HDL particles and microparticles formed by ABCA1-mediated efflux of cellular lipids to apoA-I. J. Lipid Res. 47 (2006) 832-843
26. Ehehalt R., Keller P., Haass C., Thiele C., and Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160 (2003) 113-123
27. Fan Q.W., Yu W., Senda T., Yanagisawa K., and Michikawa M. Cholesterol-dependent modulation of tau phosphorylation in cultured neurons. J. Neurochem. 76 (2001) 391-400
28. 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., and Hartmann T. Simvastatin strongly reduces levels of Alzheimer's disease beta -amyloid peptides Abeta 42 and Abeta 40 in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5856-5861
29. Fielding C.J., and Fielding P.E. Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36 (1995) 211-228
30. Fukumoto H., Deng A., Irizarry M.C., Fitzgerald M.L., and Rebeck G.W. Induction of the cholesterol transporter ABCA1 in central nervous system cells by liver X receptor agonists increases secreted Abeta levels. J. Biol. Chem. 277 (2002) 48508-48513
31. Goodwin J.S., Drake K.R., Remmert C.L., and Kenworthy A.K. Ras diffusion is sensitive to plasma membrane viscosity. Biophys. J. 89 (2005) 1398-1410
32. Hao J., Li K., Li K., Zhang D., Wang W., Yang Y., Yan B., Shan B., and Zhou X. Visual attention deficits in Alzheimer's disease: an fMRI study. Neurosci. Lett. 385 (2005) 18-23
33. Hirsch-Reinshagen V., Chan J.Y., Wilkinson A., Tanaka T., Fan J., Ou G., Maia L.F., Singaraja R.R., Hayden M.R., and Wellington C.L. Physiologically regulated transgenic ABCA1 does not reduce amyloid burden or amyloid-beta peptide levels in vivo. J. Lipid Res. 48 (2007) 914-923
34. Hirsch-Reinshagen V., Maia L.F., Burgess B.L., Blain J.F., Naus K.E., McIsaac S.A., Parkinson P.F., Chan J.Y., Tansley G.H., Hayden M.R., Poirier J., Van Nostrand W., and Wellington C.L. The absence of ABCA1 decreases soluble ApoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J. Biol. Chem. 280 (2005) 43243-43256
35. Hof P.R., Bierer L.M., Perl D.P., Delacourte A., Buee L., Bouras C., and Morrison J.H. Evidence for early vulnerability of the medial and inferior aspects of the temporal lobe in an 82-year-old patient with preclinical signs of dementia. Regional and laminar distribution of neurofibrillary tangles and senile plaques. Arch. Neurol. 49 (1992) 946-953
36. Hughes C.P., Berg L., Danziger W.L., Coben L.A., and Martin R.L. A new clinical scale for the staging of dementia. Br. J. Psychiatry 140 (1982) 566-572
37. Hutter-Paier B., Huttunen H.J., Puglielli L., Eckman C.B., Kim D.Y., Hofmeister A., Moir R.D., Domnitz S.B., Frosch M.P., Windisch M., and Kovacs D.M. The ACAT inhibitor CP-113, 818 markedly reduces amyloid pathology in a mouse model of Alzheimer's disease. Neuron 44 (2004) 227-238
38. Hyman B.T., Van Hoesen G.W., and Damasio A.R. Memory-related neural systems in Alzheimer's disease: an anatomic study. Neurology 40 (1990) 1721-1730
39. Johnson S.A., Morgan D.G., and Finch C.E. Extensive postmortem stability of RNA from rat and human brain. J. Neurosci. Res. 16 (1986) 267-280
40. Katsel P., Tan W., and Haroutunian V. Gain in brain immunity in the oldest-old differentiates cognitively normal from demented individuals. PloS ONE 4 (2009) e7642
41. Katzov H., Chalmers K., Palmgren J., Andreasen N., Johansson B., Cairns N.J., Gatz M., Wilcock G.K., Love S., Pedersen N.L., Brookes A.J., Blennow K., Kehoe P.G., and Prince J.A. Genetic variants of ABCA1 modify Alzheimer disease risk and quantitative traits related to beta-amyloid metabolism. Hum. Mutat. 23 (2004) 358-367
42. Kergoat H., Kergoat M.J., Justino L., Chertkow H., Robillard A., and Bergman H. Visual retinocortical function in dementia of the Alzheimer type. Gerontology 48 (2002) 197-203
43. Kim W.S., Guillemin G.J., Glaros E.N., Lim C.K., and Garner B. Quantitation of ATP-binding cassette subfamily-A transporter gene expression in primary human brain cells. Neuroreport 17 (2006) 891-896
44. Kim W.S., Rahmanto A.S., Kamili A., Rye K.A., Guillemin G.J., Gelissen I.C., Jessup W., Hill A.F., and 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. 282 (2007) 2851-2861
45. Kivipelto M., Helkala E.L., Laakso M.P., Hanninen T., Hallikainen M., Alhainen K., Soininen H., Tuomilehto J., and Nissinen A. Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study. Br. Med. J. 322 (2001) 1447-1451
46. Kojro E., Gimpl G., Lammich S., Marz W., and Fahrenholz F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5815-5820
47. Koldamova R.P., Lefterov I.M., Ikonomovic M.D., Skoko J., Lefterov P.I., Isanski B.A., DeKosky S.T., and Lazo J.S. 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 (2003) 13244-13256
48. Koudinov A.R., and Koudinova N.V. Essential role for cholesterol in synaptic plasticity and neuronal degeneration. FASEB J. 15 (2001) 1858-1860
49. Landry A., and Xavier R. Isolation and analysis of lipid rafts in cell-cell interactions. Methods Mol. Biol. 341 (2006) 251-282
50. Landry Y.D., Denis M., Nandi S., Bell S., Vaughan A.M., and Zha X. ATP-binding cassette transporter A1 expression disrupts raft membrane microdomains through its ATPase-related functions. J. Biol. Chem. 281 (2006) 36091-36101
51. Langmann T., Klucken J., Reil M., Liebisch G., Luciani M.F., Chimini G., Kaminski W.E., and Schmitz G. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem. Biophys. Res. Commun. 257 (1999) 29-33
52. Ledesma M.D., Abad-Rodriguez J., Galvan C., Biondi E., Navarro P., Delacourte A., Dingwall C., and Dotti C.G. Raft disorganization leads to reduced plasmin activity in Alzheimer's disease brains. EMBO Rep. 4 (2003) 1190-1196
53. Ledesma M.D., Da Silva J.S., Crassaerts K., Delacourte A., De S.B., and Dotti C.G. Brain plasmin enhances APP alpha-cleavage and Abeta degradation and is reduced in Alzheimer's disease brains. EMBO Rep. 1 (2000) 530-535
54. Ledesma M.D., and Dotti C.G. The conflicting role of brain cholesterol in Alzheimer's disease: lessons from the brain plasminogen system. Biochem. Soc. Symp. (2005) 129-138
55. Lee A.G., and Martin C.O. Neuro-ophthalmic findings in the visual variant of Alzheimer's disease. Ophthalmology 111 (2004) 376-380
56. Lewis D.A., Campbell M.J., Terry R.D., and Morrison J.H. Laminar and regional distributions of neurofibrillary tangles and neuritic plaques in Alzheimer's disease: a quantitative study of visual and auditory cortices. J. Neurosci. 7 (1987) 1799-1808
57. Lipska B.K., Deep-Soboslay A., Weickert C.S., Hyde T.M., Martin C.E., Herman M.M., and Kleinman J.E. Critical factors in gene expression in postmortem human brain: Focus on studies in schizophrenia. Biol. Psychiatry. 60 (2006) 650-658
58. Maldonado R.A., Irvine D.J., Schreiber R., and Glimcher L.H. A role for the immunological synapse in lineage commitment of CD4 lymphocytes. Nature 431 (2004) 527-532
59. Marchetti M., Monier M.N., Fradagrada A., Mitchell K., Baychelier F., Eid P., Johannes L., and Lamaze C. Stat-mediated signaling induced by type I and type II interferons (IFNs) is differentially controlled through lipid microdomain association and clathrin-dependent endocytosis of IFN receptors. Mol. Biol. Cell 17 (2006) 2896-2909
60. Mason R.P., Shoemaker W.J., Shajenko L., Chambers T.E., and Herbette L.G. Evidence for changes in the Alzheimer's disease brain cortical membrane structure mediated by cholesterol. Neurobiol. Aging 13 (1992) 413-419
61. Mirra S.S., Heyman A., McKeel D., Sumi S.M., Crain B.J., Brownlee L.M., Vogel F.S., Hughes J.P., van Belle G., and 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 41 (1991) 479-486
62. Mirra S.S., Vogel F.S., and Heyman A. Guide to the CERAD protocol for the neuropathological assessment of Alzheimer's disease (1987), CERAD, Durham, NC
63. Molander-Melin M., Blennow K., Bogdanovic N., Dellheden B., Mansson J.E., and Fredman P. Structural membrane alterations in Alzheimer brains found to be associated with regional disease development; increased density of gangliosides GM1 and GM2 and loss of cholesterol in detergent-resistant membrane domains. J. Neurochem. 92 (2005) 171-182
64. Morris J.C. The clinical dementia rating (CDR): current version and scoring rules. Neurology 43 (1993) 2412-2414
65. Morrison J.H., Lewis D.A., Campbell M.J., Huntley G.W., Benson D.L., and Bouras C. A monoclonal antibody to non-phosphorylated neurofilament protein marks the vulnerable cortical neurons in Alzheimer's disease. Brain Res. 416 (1987) 331-336
66. Naslund J., Schierhorn A., Hellman U., Lannfelt L., Roses A.D., Tjernberg L.O., Silberring J., Gandy S.E., Winblad B., and Greengard P. Relative abundance of Alzheimer A beta amyloid peptide variants in Alzheimer disease and normal aging. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 8378-8382
67. Puglielli L., Tanzi R.E., and Kovacs D.M. Alzheimer's disease: the cholesterol connection. Nat. Neurosci. 6 (2003) 345-351
68. Purohit D.P., Perl D.P., Haroutunian V., Powchik P., Davidson M., and Davis K.L. Alzheimer disease and related neurodegenerative diseases in elderly patients with schizophrenia: a postmortem neuropathologic study of 100 cases. Arch. Gen. Psychiatry 55 (1998) 205-211
69. Refolo L.M., Pappolla M.A., LaFrancois J., Malester B., Schmidt S.D., Thomas-Bryant T., Tint G.S., Wang R., Mercken M., Petanceska S.S., and Duff K.E. A cholesterol-lowering drug reduces beta-amyloid pathology in a transgenic mouse model of Alzheimer's disease. Neurobiol. Dis. 8 (2001) 890-899
70. Repa J.J., and Mangelsdorf D.J. The liver X receptor gene team: potential new players in atherosclerosis. Nat. Med. 8 (2002) 1243-1248
71. Reynolds C.A., Hong M.G., Eriksson U.K., Blennow K., Bennet A.M., Johansson B., Malmberg B., Berg S., Wiklund F., Gatz M., Pedersen N.L., and Prince J.A. A survey of ABCA1 sequence variation confirms association with dementia. Hum. Mutat. 30 (2009) 1348-1354
72. Rodríguez-Rodríguez E., Mateo I., Llorca J., Sánchez-Quintana C., Infante J., García-Gorostiaga I., Sánchez-Juan P., Berciano J., and Combarros O. Association of genetic variants of ABCA1 with Alzheimer's disease risk. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144B (2007) 964-968
73. Russell D.W. Oxysterol biosynthetic enzymes. Biochim. Biophys. Acta 1529 (2000) 126-135
74. Sawamura N., Gong J.S., Chang T.Y., Yanagisawa K., and Michikawa M. Promotion of tau phosphorylation by MAP kinase Erk1/2 is accompanied by reduced cholesterol level in detergent-insoluble membrane fraction in Niemann-Pick C1-deficient cells. J. Neurochem. 84 (2003) 1086-1096
75. Shobab L.A., Hsiung G.Y., and Feldman H.H. Cholesterol in Alzheimer's disease. Lancet Neurol. 4 (2005) 841-852
76. Simons M., Keller P., De Strooper B., Beyreuther K., Dotti C.G., and Simons K. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6460-6464
77. Stefani M., and Liguri G. Cholesterol in Alzheimer's disease: unresolved questions. Curr. Alzheimer Res. 6 (2009) 15-29
78. Sun Y., Yao J., Kim T.W., and Tall A.R. Expression of liver X receptor target genes decreases cellular amyloid beta peptide secretion. J. Biol. Chem. 278 (2003) 27688-27694
79. Suzuki K., Parker C.C., Pentchev P.G., Katz D., Ghetti B., D'Agostino A.N., and Carstea E.D. Neurofibrillary tangles in Niemann-Pick disease type C. Acta Neuropathol. (Berl.) 89 (1995) 227-238
80. Tachikawa M., Watanabe M., Hori S., Fukaya M., Ohtsuki S., Asashima T., and Terasaki T. Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain. J. Neurochem. 95 (2005) 294-304
81. Tucker H.M., Kihiko-Ehmann M., Wright S., Rydel R.E., and Estus S. Tissue plasminogen activator requires plasminogen to modulate amyloid-beta neurotoxicity and deposition. J. Neurochem. 75 (2000) 2172-2177
82. Vance J.E., Hayashi H., and Karten B. Cholesterol homeostasis in neurons and glial cells. Semin. Cell Dev. Biol. 16 (2005) 193-212
83. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., and Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (2002) 0034.1-0034.11
84. Vanier M.T., and Suzuki K. Recent advances in elucidating Niemann-Pick C disease. Brain Pathol. 8 (1998) 163-174
85. Vawter M.P., Tomita H., Meng F., Bolstad B., Li J., Evans S., Choudary P., Atz M., Shao L., Neal C., Walsh D.M., Burmeister M., Speed T., Myers R., Jones E.G., Watson S.J., Akil H., and Bunney W.B. Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders. Mol. Psychiatry 11 (2006) 663-679
86. Wahrle S., Das P., Nyborg A.C., McLendon C., Shoji M., Kawarabayashi T., Younkin L.H., Younkin S.G., and Golde T.E. Cholesterol-dependent gamma-secretase activity in buoyant cholesterol-rich membrane microdomains. Neurobiol. Dis. 9 (2002) 11-23
87. Wahrle S.E., Jiang H., Parsadanian M., Hartman R.E., Bales K.R., Paul S.M., and Holtzman D.M. Deletion of Abca1 increases Abeta deposition in the PDAPP transgenic mouse model of Alzheimer disease. J. Biol. Chem. 280 (2005) 43236-43242
88. Wellington C.L., Walker E.K., Suarez A., Kwok A., Bissada N., Singaraja R., Yang Y.Z., Zhang L.H., James E., Wilson J.E., Francone O., McManus B.M., and Hayden M.R. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab. Invest. 82 (2002) 273-283
89. Wollmer M.A., Streffer J.R., Lütjohann D., Tsolaki M., Iakovidou V., Hegi T., Pasch T., Jung H.H., Bergmann K., Nitsch R.M., Hock C., and Papassotiropoulos A. ABCA1 modulates CSF cholesterol levels and influences the age at onset of Alzheimer's disease. Neurobiol. Aging 24 (2003) 421-426
90. Wolozin B., Kellman W., Ruosseau P., Celesia G.G., and Siegel G. Decreased prevalence of Alzheimer disease associated with 3-hydroxy-3-methyglutaryl coenzyme A reductase inhibitors. Arch. Neurol. 57 (2000) 1439-1443
91. Yancey P.G., Bortnick A.E., Kellner-Weibel G., Llera-Moya M., Phillips M.C., and Rothblat G.H. Importance of different pathways of cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 712-719
92. Zarubica A., Plazzo A.P., Stockl M., Trombik T., Hamon Y., Muller P., Pomorski T., Herrmann A., and Chimini G. Functional implications of the influence of ABCA1 on lipid microenvironment at the plasma membrane: a biophysical study. FASEB J. 23 (2009) 1775-1785
93. Zarubica A., Trompier D., and Chimini G. ABCA1, from pathology to membrane function. Pflugers Arch. 453 (2007) 569-579