Differential regulation of ABCA1 and ABCG1 gene expressions in the remodeling mouse hippocampus after entorhinal cortex lesion and liver-X receptor agonist treatment

Brain Research

Volumn 1562, Issue , 2014, Pages 39-51

  Bélanger Jasmin, Stéphanie ^a,b   Pearson, Vanessa ^a,b   Lalonde, Daphnée ^a,b   Domenger, Dorothée ^a,b   Théroux, Louise ^b   Poirier, Judes ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

Apolipoprotein E; ATP binding cassette transporter; Cholesterol; LXR; Reinnervation; TO901317

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ACETYLCHOLINESTERASE; APOLIPOPROTEIN E; CELL NUCLEUS RECEPTOR; LIPOPROTEIN; LIVER X RECEPTOR AGONIST; MESSENGER RNA; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; SYNAPTOPHYSIN; ABC TRANSPORTER; ABCA1 PROTEIN, MOUSE; ABCG1 PROTEIN, MOUSE; ACHE PROTEIN, MOUSE; FLUORINATED HYDROCARBON; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; LIVER X RECEPTOR; NEUROPROTECTIVE AGENT; ORPHAN NUCLEAR RECEPTOR; SULFONAMIDE; SYP PROTEIN, MOUSE; TO-901317;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX LESION; CHOLESTEROL TRANSPORT; CHOLINERGIC SYNAPSE; CONTROLLED STUDY; DEAFFERENTATION; DENTATE GYRUS; ENTORHINAL CORTEX; FRONTAL CORTEX; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HISTOCHEMISTRY; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REINNERVATION; SYNAPSE; AGONISTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; FRONTAL LOBE; GENE EXPRESSION; GENETICS; HEMISPHERIC DOMINANCE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TIME;

ACETYLCHOLINESTERASE; ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; ENTORHINAL CORTEX; FRONTAL LOBE; FUNCTIONAL LATERALITY; GENE EXPRESSION; GPI-LINKED PROTEINS; HIPPOCAMPUS; HYDROCARBONS, FLUORINATED; LIPOPROTEINS; MALE; MICE, INBRED C57BL; NEURONAL PLASTICITY; NEUROPROTECTIVE AGENTS; ORPHAN NUCLEAR RECEPTORS; RNA, MESSENGER; SULFONAMIDES; SYNAPTOPHYSIN; TIME FACTORS;

EID: 84899429186     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.03.016     Document Type: Article

References (70)

1. K. Abildayeva, P.J. Jansen, V. Hirsch-Reinshagen, V.W. Bloks, A.H.F. Bakker, F.C.S. Ramaekers, J. de Vente, A.K. Groen, C.L. Wellington, F. Kuipers, and M. Mulder 24(S)-hydroxycholesterol participates in a liver X receptor-controlled pathway in astrocytes that regulates apolipoprotein E-mediated cholesterol efflux J. Biol. Chem. 281 2006 12799 12808 10.1074/jbc.M601019200
2. J.-F. Blain, E. Paradis, S.B. Gaudreault, D. Champagne, D. Richard, and J. Poirier A role for lipoprotein lipase during synaptic remodeling in the adult mouse brain Neurobiol. Dis. 15 2004 510 519
3. B. Burgess, K. Naus, J. Chan, V. Hirsch-Reinshagen, G. Tansley, L. Matzke, B. Chan, A. Wilkinson, J. Fan, J. Donkin, D. Balik, T. Tanaka, G. Ou, R. Dyer, S. Innis, B. McManus, D. Lütjohann, and C. Wellington Overexpression of human ABCG1 does not affect atherosclerosis in fat-fed ApoE-deficient mice Arterioscler. Thromb. Vasc. Biol. 28 2008 1731 1737 10.1161/ATVBAHA.108.168542
4. B.L. Burgess, P.F. Parkinson, M.M. Racke, V. Hirsch-Reinshagen, J. Fan, C. Wong, S. Stukas, L. Theroux, J.Y. Chan, J. Donkin, A. Wilkinson, D. Balik, B. Christie, J. Poirier, D. Lütjohann, R.B. Demattos, and C.L. Wellington ABCG1 influences the brain cholesterol biosynthetic pathway but does not affect amyloid precursor protein or apolipoprotein E metabolism in vivo J. Lipid Res. 49 2008 1254 1267 10.1194/jlr.M700481-JLR200
5. M.P. Burns, L. Vardanian, A. Pajoohesh-Ganji, L. Wang, M. Cooper, D.C. Harris, K. Duff, and G.W. Rebeck The effects of ABCA1 on cholesterol efflux and Abeta levels in vitro and in vivo J. Neurochem. 98 2006 792 800 10.1111/j.1471-4159.2006.03925.x
6. D. Cao, K. Fukuchi, H. Wan, H. Kim, and L. Li Lack of LDL receptor aggravates learning deficits and amyloid deposits in Alzheimer transgenic mice Neurobiol. Aging 27 2006 1632 1643 10.1016/j.neurobiolaging.2005.09.011
7. D. Champagne, J.-B. Dupuy, J. Rochford, and J. Poirier Apolipoprotein E knockout mice display procedural deficits in the Morris water maze: analysis of learning strategies in three versions of the task Neuroscience 114 2002 641 654
8. D. Champagne, J. Rochford, and J. Poirier Effect of apolipoprotein E deficiency on reactive sprouting in the dentate gyrus of the hippocampus following entorhinal cortex lesion: role of the astroglial response Exp. Neurol. 194 2005 31 42 10.1016/j.expneurol.2005.01.016
9. J. Chen, A. Zacharek, X. Cui, A. Shehadah, H. Jiang, C. Roberts, M. Lu, and M. Chopp Treatment of stroke with a synthetic liver X receptor agonist, TO901317, promotes synaptic plasticity and axonal regeneration in mice J. Cereb. Blood Flow Metab. Off. J. Int. Soc. Cereb. Blood Flow Metab. 30 2010 102 109 10.1038/jcbfm.2009.187
10. Posse De Chaves, E.I. Vance, D.E. Campenot, R.B. Kiss, and R.S. Vance, J.E. Uptake of lipoproteins for axonal growth of sympathetic neurons J. Biol. Chem. 275 2000 19883 19890
11. E.I. De Chaves, A.E. Rusiñol, D.E. Vance, R.B. Campenot, and J.E. Vance Role of lipoproteins in the delivery of lipids to axons during axonal regeneration J. Biol. Chem. 272 1997 30766 30773
12. J.M. Dietschy Central nervous system: cholesterol turnover, brain development and neurodegeneration Biol. Chem. 390 2009 287 293 10.1515/BC.2009.035
13. J.M. Dietschy, and S.D. Turley Cholesterol metabolism in the brain Curr. Opin. Lipidol. 12 2001 105 112
14. T. Engel, S. Lorkowski, A. Lueken, S. Rust, B. Schlüter, G. Berger, P. Cullen, and G. Assmann The human ABCG4 gene is regulated by oxysterols and retinoids in monocyte-derived macrophages Biochem. Biophys. Res. Commun. 288 2001 483 488 10.1006/bbrc.2001.5756
15. A.M. Fagan, and F.H. Gage Mechanisms of sprouting in the adult central nervous system: cellular responses in areas of terminal degeneration and reinnervation in the rat hippocampus Neuroscience 58 1994 705 725
16. H. Fukumoto, A. Deng, M.C. Irizarry, M.L. Fitzgerald, and G.W. Rebeck 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 10.1074/jbc.M209085200
17. C. Gabbi, M. Warner, and J.-A. Gustafsson Minireview: liver X receptor beta: emerging roles in physiology and diseases Mol. Endocrinol. Baltimore Md 23 2009 129 136 10.1210/me.2008-0398
18. I.C. Gelissen, M. Harris, K.-A. Rye, C. Quinn, A.J. Brown, M. Kockx, S. Cartland, M. Packianathan, L. Kritharides, and W. Jessup ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I Arterioscler. Thromb. Vasc. Biol. 26 2006 534 540 10.1161/01.ATV.0000200082.58536.e1
19. G.A. Graf, L. Yu, W.-P. Li, R. Gerard, P.L. Tuma, J.C. Cohen, and H.H. Hobbs ABCG5 and ABCG8 are obligate heterodimers for protein trafficking and biliary cholesterol excretion J. Biol. Chem. 278 2003 48275 48282 10.1074/jbc.M310223200
20. V. Hirsch-Reinshagen, and C.L. Wellington Cholesterol metabolism, apolipoprotein E, adenosine triphosphate-binding cassette transporters, and Alzheimer's disease Curr. Opin. Lipidol. 18 2007 325 332 10.1097/MOL. 0b013e32813aeabf
21. V. Hirsch-Reinshagen, S. Zhou, B.L. Burgess, L. Bernier, S.A. McIsaac, J.Y. Chan, G.H. Tansley, J.S. Cohn, M.R. Hayden, and C.L. Wellington Deficiency of ABCA1 impairs apolipoprotein E metabolism in brain J. Biol. Chem. 279 2004 41197 41207 10.1074/jbc.M407962200
22. M.J. Ignatius, E.M. Shooter, R.E. Pitas, and R.W. Mahley Lipoprotein uptake by neuronal growth cones in vitro Science 236 1987 959 962
23. D.R. Illingworth, and J. Glover The composition of lipids in cerebrospinal fluid of children and adults J. Neurochem. 18 1971 769 776
24. K. Ishimoto, K. Tachibana, M. Sumitomo, S. Omote, I. Hanano, D. Yamasaki, Y. Watanabe, T. Tanaka, T. Hamakubo, J. Sakai, T. Kodama, and T. Doi Identification of human low-density lipoprotein receptor as a novel target gene regulated by liver X receptor alpha FEBS Lett. 580 2006 4929 4933 10.1016/j.febslet.2006.08.010
25. J.M. Karasinska, F. Rinninger, D. Lütjohann, P. Ruddle, S. Franciosi, J.K. Kruit, R.R. Singaraja, V. Hirsch-Reinshagen, J. Fan, L.R. Brunham, N. Bissada, R. Ramakrishnan, C.L. Wellington, J.S. Parks, and M.R. Hayden Specific loss of brain ABCA1 increases brain cholesterol uptake and influences neuronal structure and function J. Neurosci. Off. J. Soc. Neurosci. 29 2009 3579 3589 10.1523/JNEUROSCI.4741-08.2009
26. B. Karten, R.B. Campenot, D.E. Vance, and J.E. Vance Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia J. Biol. Chem. 281 2006 4049 4057 10.1074/jbc.M508915200
27. M.A. Kennedy, G.C. Barrera, K. Nakamura, A. Baldán, P. Tarr, M.C. Fishbein, J. Frank, O.L. Francone, and P.A. Edwards ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation Cell Metab. 1 2005 121 131 10.1016/j.cmet.2005.01.002
28. M.A. Kennedy, A. Venkateswaran, P.T. Tarr, I. Xenarios, J. Kudoh, N. Shimizu, and P.A. Edwards Characterization of the human ABCG1 gene: liver X receptor activates an internal promoter that produces a novel transcript encoding an alternative form of the protein J. Biol. Chem. 276 2001 39438 39447 10.1074/jbc.M105863200
29. J. Klucken, C. Büchler, E. Orsó, W.E. Kaminski, M. Porsch-Ozcürümez, G. Liebisch, M. Kapinsky, W. Diederich, W. Drobnik, M. Dean, R. Allikmets, and G. Schmitz ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport Proc. Natl. Acad. Sci. USA 97 2000 817 822
30. R. Koldamova, N.F. Fitz, and I. Lefterov The role of ATP-binding cassette transporter A1 in Alzheimer's disease and neurodegeneration Biochim. Biophys. Acta 1801 2010 824 830 10.1016/j.bbalip.2010.02.010
31. R.P. Koldamova, I.M. Lefterov, M.D. Ikonomovic, J. Skoko, P.I. Lefterov, B.A. Isanski, S.T. DeKosky, and J.S. Lazo 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 10.1074/jbc.M300044200
32. R.P. Koldamova, I.M. Lefterov, M. Staufenbiel, D. Wolfe, S. Huang, J.C. Glorioso, M. Walter, M.G. Roth, and J.S. Lazo 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 2005 4079 4088 10.1074/jbc.M411420200
33. H.J. Krugers, M. Mulder, J. Korf, L. Havekes, E.R. de Kloet, and M. Joëls Altered synaptic plasticity in hippocampal CA1 area of apolipoprotein E deficient mice Neuroreport 8 1997 2505 2510
34. M.J. LaDu, J.A. Shah, C.A. Reardon, G.S. Getz, G. Bu, J. Hu, L. Guo, and L.J. Van Eldik Apolipoprotein E and apolipoprotein E receptors modulate A beta-induced glial neuroinflammatory responses Neurochem. Int. 39 2001 427 434 (http://dx.doi.org/11578778)
35. I. Lefterov, N.F. Fitz, A. Cronican, P. Lefterov, M. Staufenbiel, and R. Koldamova Memory deficits in APP23/Abca1+/- mice correlate with the level of Aβ oligomers ASN Neuro 2009 1 10.1042/AN20090015
36. D.J. Loane, P.M. Washington, L. Vardanian, A. Pocivavsek, H.-S. Hoe, K.E. Duff, I. Cernak, G.W. Rebeck, A.I. Faden, and M.P. Burns Modulation of ABCA1 by an LXR agonist reduces β-amyloid levels and improves outcome after traumatic brain injury J. Neurotrauma 28 2011 225 236 10.1089/neu.2010.1595
37. E. Masliah, M. Mallory, N. Ge, M. Alford, I. Veinbergs, and A.D. Roses Neurodegeneration in the central nervous system of apoE-deficient mice Exp. Neurol. 136 1995 107 122 10.1006/exnr.1995.1088
38. D.A. Matthews, C. Cotman, and G. Lynch An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration Brain Res. 115 1976 1 21
39. D.H. Mauch, K. Nägler, S. Schumacher, C. Göritz, E.C. Müller, A. Otto, and F.W. Pfrieger CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357 10.1126/science.294.5545. 1354
40. J.R. Morales, I. Ballesteros, J.M. Deniz, O. Hurtado, J. Vivancos, F. Nombela, I. Lizasoain, A. Castrillo, and M.A. Moro Activation of liver X receptors promotes neuroprotection and reduces brain inflammation in experimental stroke Circulation 118 2008 1450 1459 10.1161/CIRCULATIONAHA.108. 782300
41. M. Mulder, P.J. Jansen, B.J.A. Janssen, W.D.J. van de Berg, H. van der Boom, L.M. Havekes, R.E. de Kloet, F.C.S. Ramaekers, and A. Blokland Low-density lipoprotein receptor-knockout mice display impaired spatial memory associated with a decreased synaptic density in the hippocampus Neurobiol. Dis. 16 2004 212 219 10.1016/j.nbd.2004.01.015
42. M. Mulder, G. Koopmans, G. Wassink, G. Al Mansouri, M.-L. Simard, L.M. Havekes, J. Prickaerts, and A. Blokland LDL receptor deficiency results in decreased cell proliferation and presynaptic bouton density in the murine hippocampus Neurosci. Res. 59 2007 251 256 10.1016/j.neures.2007.07.004
43. K. Nelissen, M. Mulder, I. Smets, S. Timmermans, K. Smeets, M. Ameloot, and J.J.A. Hendriks Liver X receptors regulate cholesterol homeostasis in oligodendrocytes J. Neurosci. Res. 90 2012 60 71 10.1002/jnr.22743
44. M.S. Oitzl, M. Mulder, P.J. Lucassen, L.M. Havekes, J. Grootendorst, and E.R. de Kloet Severe learning deficits in apolipoprotein E-knockout mice in a water maze task Brain Res. 752 1997 189 196
45. S. Oldfield, C. Lowry, J. Ruddick, and S. Lightman ABCG4: a novel human white family ABC-transporter expressed in the brain and eye Biochim. Biophys. Acta 1591 2002 175 179
46. P.F. Parkinson, T.S. Kannangara, B.D. Eadie, B.L. Burgess, C.L. Wellington, and B.R. Christie Cognition, learning behavior and hippocampal synaptic plasticity are not disrupted in mice over-expressing the cholesterol transporter ABCG1 Lipids Health Dis. 8 2009 5 10.1186/1476-511X-8-5
47. C. Petit-Turcotte, N. Aumont, U. Beffert, D. Dea, J. Herz, and J. Poirier The apoE receptor apoER2 is involved in the maintenance of efficient synaptic plasticity Neurobiol. Aging 26 2005 195 206 10.1016/j.neurobiolaging.2004.04.007
48. F.W. Pfrieger Cholesterol homeostasis and function in neurons of the central nervous system Cell. Mol. Life Sci. CMLS 60 2003 1158 1171 10.1007/s00018-003-3018-7
49. A.L. Phinney, M.E. Calhoun, A.G. Woods, T. Deller, and M. Jucker Stereological analysis of the reorganization of the dentate gyrus following entorhinal cortex lesion in mice Eur. J. Neurosci. 19 2004 1731 1740 10.1111/j.1460-9568.2004.03280.x
50. J. Poirier Apolipoprotein E in animal models of CNS injury and in Alzheimer's disease Trends Neurosci. 17 1994 525 530 (http://dx.doi.org/7532337)
51. J. Poirier, M. Hess, P.C. May, and C.E. Finch Astrocytic apolipoprotein E mRNA and GFAP mRNA in hippocampus after entorhinal cortex lesioning Brain Res. Mol. Brain Res. 11 1991 97 106
52. J. Poirier, L. Lamarre-Théroux, D. Dea, N. Aumont, and J.F. Blain Cholesterol transport and production in Alzheimer's disease A. Fisher, M. Memo, F. Stocchi, I. Hanin, Advances in Alzheimer's and Parkinson's Disease 2008 Springer, US Boston, MA 211 219
53. J.K. Poirier, A. Baccichet, D. Dea, and S. Gauthier Cholesterol synthesis and lipoprotein reuptake during synaptic remodelling in hippocampus in adult rats Neuroscience 55 1993 81 90 (http://dx.doi.org/8350994)
54. J.J. Repa, H. Li, T.C. Frank-Cannon, M.A. Valasek, S.D. Turley, M.G. Tansey, and J.M. Dietschy Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse J. Neurosci. Off. J. Soc. Neurosci. 27 2007 14470 14480 10.1523/JNEUROSCI.4823-07.2007
55. D.R. Riddell, H. Zhou, T.A. Comery, E. Kouranova, C.F. Lo, H.K. Warwick, R.H. Ring, Y. Kirksey, S. Aschmies, J. Xu, K. Kubek, W.D. Hirst, C. Gonzales, Y. Chen, E. Murphy, S. Leonard, D. Vasylyev, A. Oganesian, R.L. Martone, M.N. Pangalos, P.H. Reinhart, and J.S. Jacobsen The LXR agonist TO901317 selectively lowers hippocampal Abeta42 and improves memory in the Tg2576 mouse model of Alzheimer's disease Mol. Cell. Neurosci. 34 2007 621 628 10.1016/j.mcn.2007.01. 011
56. S. Savary, F. Denizot, M. Luciani, M. Mattei, and G. Chimini Molecular cloning of a mammalian ABC transporter homologous to Drosophila white gene Mamm. Genome Off. J. Int. Mamm. Genome Soc. 7 1996 673 676
57. C.P. Sparrow, J. Baffic, M.-H. Lam, E.G. Lund, A.D. Adams, X. Fu, N. Hayes, A.B. Jones, K.L. Macnaul, J. Ondeyka, S. Singh, J. Wang, G. Zhou, D.E. Moller, S.D. Wright, and J.G. Menke A potent synthetic LXR agonist is more effective than cholesterol loading at inducing ABCA1 mRNA and stimulating cholesterol efflux J. Biol. Chem. 277 2002 10021 10027 10.1074/jbc.M108225200
58. O. Steward, C.W. Cotman, and G.S. Lynch Re-establishment of electrophysiologically functional entorhinal cortical input to the dentate gyrus deafferented by ipsilateral entorhinal lesions: innervation by the contralateral entorhinal cortex Exp. Brain Res. 18 1973 396 414
59. O. Steward, S.L. Vinsant, and L. Davis The process of reinnervation in the dentate gyrus of adult rats: an ultrastructural study of changes in presynaptic terminals as a result of sprouting J. Comp. Neurol. 267 1988 203 210 10.1002/cne.902670205
60. M. Tachikawa, M. Watanabe, S. Hori, M. Fukaya, S. Ohtsuki, T. Asashima, and T. Terasaki Distinct spatio-temporal expression of ABCA and ABCG transporters in the developing and adult mouse brain J. Neurochem. 95 2005 294 304 10.1111/j.1471-4159.2005.03369.x
61. T. Vanmierlo, K. Rutten, J. Dederen, V.W. Bloks, L.C. van Vark-van der Zee, F. Kuipers, A. Kiliaan, A. Blokland, E.J.G. Sijbrands, H. Steinbusch, J. Prickaerts, D. Lütjohann, and M. Mulder Liver X receptor activation restores memory in aged AD mice without reducing amyloid Neurobiol. Aging 32 2011 1262 1272 10.1016/j.neurobiolaging.2009.07.005
62. A.M. Vaughan, and J.F. Oram ABCG1 redistributes cell cholesterol to domains removable by high density lipoprotein but not by lipid-depleted apolipoproteins J. Biol. Chem. 280 2005 30150 30157 10.1074/jbc.M505368200
63. A.M. Vaughan, and J.F. Oram ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL J. Lipid Res. 47 2006 2433 2443 10.1194/jlr.M600218-JLR200
64. I. Veinbergs, M. Mante, M.W. Jung, E. Van Uden, and E. Masliah Synaptotagmin and synaptic transmission alterations in apolipoprotein E-deficient mice Prog. Neuropsychopharmacol. Biol. Psychiatry 23 1999 519 531
65. A. Venkateswaran, B.A. Laffitte, S.B. Joseph, P.A. Mak, D.C. Wilpitz, P.A. Edwards, and P. Tontonoz Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα Proc. Natl. Acad. Sci. 97 2000 12097 12102 10.1073/pnas.200367697
66. S.E. Wahrle, H. Jiang, M. Parsadanian, J. Kim, A. Li, A. Knoten, S. Jain, V. Hirsch-Reinshagen, C.L. Wellington, K.R. Bales, S.M. Paul, and D.M. Holtzman Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease J. Clin. Invest. 118 2008 671 682 10.1172/JCI33622
67. S.E. Wahrle, H. Jiang, M. Parsadanian, J. Legleiter, X. Han, J.D. Fryer, T. Kowalewski, and D.M. Holtzman ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocyte-secreted apoE J. Biol. Chem. 279 2004 40987 40993 10.1074/jbc.M407963200
68. N. Wang, L. Yvan-Charvet, D. Lütjohann, M. Mulder, T. Vanmierlo, T.-W. Kim, and A.R. Tall ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol 22 2008 1073 1082 10.1096/fj.07-9944com
69. G. Wójcicka, A. Jamroz-Wiśniewska, K. Horoszewicz, and J. Bełtowski Liver X receptors (LXRs). Part I: structure, function, regulation of activity, and role in lipid metabolism Postȩpy Hig. Med. Dośw. 61 2007 736 759 (Online)
70. J. Xu Characterization of oligomeric human half-ABC transporter ATP-binding cassette G2 J. Biol. Chem. 279 2004 19781 19789 10.1074/jbc. M310785200