Cholesterol efflux is differentially regulated in neurons and astrocytes: Implications for brain cholesterol homeostasis

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1831, Issue 2, 2013, Pages 263-275

  Chen, Jing ^b   Zhang, Xiaolu ^a   Kusumo, Handojo ^a   Costa, Lucio G ^b,c   Guizzetti, Marina ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF PARMA MEDICAL SCHOOL   (Italy)

Author keywords

ABCA1; ABCG1; ABCG4; Astrocytes; Cholesterol efflux; Neurons

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ABCG4 PROTEIN; APOLIPOPROTEIN; CARRIER PROTEINS AND BINDING PROTEINS; CHOLESTEROL; LIPOPROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CHOLESTEROL EFFLUX; CHOLESTEROL METABOLISM; CONTROLLED STUDY; FETUS; GENE SILENCING; HOMEOSTASIS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; ASTROCYTES; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; BRAIN; CELLS, CULTURED; CHOLESTEROL; HOMEOSTASIS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84868516421     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2012.09.007     Document Type: Article

References (52)

1. J.E. Vance, B. Karten, and H. Hayashi Lipid dynamics in neurons Biochem. Soc. Trans. 34 2006 399 403
2. M. Guizzetti, J. Chen, and L.G. Costa Disruption of cholesterol homeostasis in developmental neurotoxicity R.C. Gupta, Reproductive and Developmental Toxicology 2011 Elsevier New York 855 862
3. I. Bjorkhem, V. Leoni, and S. Meaney Genetic connections between neurological disorders and cholesterol metabolism J. Lipid Res. 51 2010 2489 2503
4. M.J. LaDu, S.M. Gilligan, J.R. Lukens, V.G. Cabana, C.A. Reardon, L.J. Van Eldik, and D.M. Holtzman Nascent astrocyte particles differ from lipoproteins in CSF J. Neurochem. 70 1998 2070 2081
5. C. Yu, K.L. Youmans, and M.J. LaDu Proposed mechanism for lipoprotein remodelling in the brain Biochim. Biophys. Acta 1801 2010 819 823
6. R.E. Pitas, J.K. Boyles, S.H. Lee, D. Hui, and K.H. Weisgraber Lipoproteins and their receptors in the central nervous system. Characterization of the lipoproteins in cerebrospinal fluid and identification of apolipoprotein B, E(LDL) receptors in the brain J. Biol. Chem. 262 1987 14352 14360
7. W.S. Kim, A.S. Rahmanto, A. Kamili, K.A. Rye, G.J. Guillemin, I.C. Gelissen, W. Jessup, A.F. Hill, and B. Garner 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
8. D.H. Mauch, K. Nagler, S. Schumacher, C. Goritz, E.C. Muller, A. Otto, and F.W. Pfrieger CNS synaptogenesis promoted by glia-derived cholesterol Science 294 2001 1354 1357
9. M. Matsuo, R.B. Campenot, D.E. Vance, K. Ueda, and J.E. Vance Involvement of low-density lipoprotein receptor-related protein and ABCG1 in stimulation of axonal extension by apoE-containing lipoproteins Biochim. Biophys. Acta 1811 2011 31 38
10. D.M. Ramirez, S. Andersson, and D.W. Russell Neuronal expression and subcellular localization of cholesterol 24-hydroxylase in the mouse brain J. Comp. Neurol. 507 2008 1676 1693
11. K. Nieweg, H. Schaller, and F.W. Pfrieger Marked differences in cholesterol synthesis between neurons and glial cells from postnatal rats J. Neurochem. 109 2009 125 134
12. A. Chawla, W.A. Boisvert, C.H. Lee, B.A. Laffitte, Y. Barak, S.B. Joseph, D. Liao, L. Nagy, P.A. Edwards, L.K. Curtiss, R.M. Evans, and P. Tontonoz A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis Mol. Cell 7 2001 161 171
13. S.R. Bates, J.Q. Tao, K.J. Yu, Z. Borok, E.D. Crandall, H.L. Collins, and G.H. Rothblat Expression and biological activity of ABCA1 in alveolar epithelial cells Am. J. Respir. Cell Mol. Biol. 38 2008 283 292
14. K. Abildayeva, P.J. Jansen, V. Hirsch-Reinshagen, V.W. Bloks, A.H. Bakker, F.C. 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
15. J. Chen, L.G. Costa, and M. Guizzetti Retinoic acid isomers up-regulate ATP binding cassette A1 and G1 and cholesterol efflux in rat astrocytes: implications for their therapeutic and teratogenic effects J. Pharmacol. Exp. Ther. 338 2011 870 878
16. 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
17. P.T. Tarr, and P.A. Edwards ABCG1 and ABCG4 are coexpressed in neurons and astrocytes of the CNS and regulate cholesterol homeostasis through SREBP-2 J. Lipid Res. 49 2008 169 182
18. W.S. Kim, G.J. Guillemin, E.N. Glaros, C.K. Lim, and B. Garner Quantitation of ATP-binding cassette subfamily-A transporter gene expression in primary human brain cells Neuroreport 17 2006 891 896
19. M. Guizzetti, J. Chen, J.F. Oram, R. Tsuji, K. Dao, T. Moller, and L.G. Costa Ethanol induces cholesterol efflux and up-regulates ATP-binding cassette cholesterol transporters in fetal astrocytes J. Biol. Chem. 282 2007 18740 18749
20. M. Guizzetti, and L.G. Costa Inhibition of muscarinic receptor-stimulated glial cell proliferation by ethanol J. Neurochem. 67 1996 2236 2245
21. G.J. Brewer Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus J. Neurosci. Res. 42 1995 674 683
22. 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
23. J.F. Oram, and R.M. Lawn ABCA1. The gatekeeper for eliminating excess tissue cholesterol J. Lipid Res. 42 2001 1173 1179
24. 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
25. P.G. Yancey, A.E. Bortnick, G. Kellner-Weibel, M. de la Llera-Moya, M.C. Phillips, and G.H. Rothblat Importance of different pathways of cellular cholesterol efflux Arterioscler. Thromb. Vasc. Biol. 23 2003 712 719
26. P. Costet, Y. Luo, N. Wang, and A.R. Tall Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor J. Biol. Chem. 275 2000 28240 28245
27. S. Murthy, E. Born, S.N. Mathur, and F.J. Field LXR/RXR activation enhances basolateral efflux of cholesterol in CaCo-2 cells J. Lipid Res. 43 2002 1054 1064
28. 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
29. Y. Wang, and J.F. Oram Unsaturated fatty acids phosphorylate and destabilize ABCA1 through a phospholipase D2 pathway J. Biol. Chem. 280 2005 35896 35903
30. J.P. Slotte, J.F. Oram, and E.L. Bierman Binding of high density lipoproteins to cell receptors promotes translocation of cholesterol from intracellular membranes to the cell surface J. Biol. Chem. 262 1987 12904 12907
31. J.F. Oram, A.J. Mendez, J.P. Slotte, and T.F. Johnson High density lipoprotein apolipoproteins mediate removal of sterol from intracellular pools but not from plasma membranes of cholesterol-loaded fibroblasts Arterioscler. Thromb. 11 1991 403 414
32. E. Favari, I. Zanotti, F. Zimetti, N. Ronda, F. Bernini, and G.H. Rothblat Probucol inhibits ABCA1-mediated cellular lipid efflux Arterioscler. Thromb. Vasc. Biol. 24 2004 2345 2350
33. C.A. Wu, M. Tsujita, M. Hayashi, and S. Yokoyama Probucol inactivates ABCA1 in the plasma membrane with respect to its mediation of apolipoprotein binding and high density lipoprotein assembly and to its proteolytic degradation J. Biol. Chem. 279 2004 30168 30174
34. S. Treiber-Held, R. Distl, V. Meske, F. Albert, and T.G. Ohm Spatial and temporal distribution of intracellular free cholesterol in brains of a Niemann-Pick type C mouse model showing hyperphosphorylated tau protein. Implications for Alzheimer's disease J. Pathol. 200 2003 95 103
35. M. Guizzetti, and L.G. Costa Cholesterol homeostasis in the developing brain: a possible new target for ethanol Hum. Exp. Toxicol. 26 2007 355 360
36. J.F. Blain, and J. Poirier Cholesterol homeostasis and the pathophysiology of Alzheimer's disease Expert Rev. Neurother. 4 2004 823 829
37. I. Bjorkhem, and S. Meaney Brain cholesterol: long secret life behind a barrier Arterioscler. Thromb. Vasc. Biol. 24 2004 806 815
38. J.M. Dietschy, and S.D. Turley Thematic review series: brain Lipids. Cholesterol metabolism in the central nervous system during early development and in the mature animal J. Lipid Res. 45 2004 1375 1397
39. M. Walter, N.R. Forsyth, W.E. Wright, J.W. Shay, and M.G. Roth The establishment of telomerase-immortalized Tangier disease cell lines indicates the existence of an apolipoprotein A-I-inducible but ABCA1-independent cholesterol efflux pathway J. Biol. Chem. 279 2004 20866 20873
40. J.F. Oram, and A.M. Vaughan ABCA1-mediated transport of cellular cholesterol and phospholipids to HDL apolipoproteins Curr. Opin. Lipidol. 11 2000 253 260
41. B. Yu, J. Wu, X.Y. Zhang, L.H. Chen, G.R. Yang, M.F. Wei, C.Y. Xing, and Y.F. Guan Liver X receptors mediate cholesterol efflux in mouse glomerular mesangial cells Beijing Da Xue Xue Bao 38 2006 244 248
42. K.D. Whitney, M.A. Watson, J.L. Collins, W.G. Benson, T.M. Stone, M.J. Numerick, T.K. Tippin, J.G. Wilson, D.A. Winegar, and S.A. Kliewer Regulation of cholesterol homeostasis by the liver X receptors in the central nervous system Mol. Endocrinol. 16 2002 1378 1385
43. 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
44. A. Chait, C.Y. Han, J.F. Oram, and J.W. Heinecke Thematic review series: the immune system and atherogenesis. Lipoprotein-associated inflammatory proteins: markers or mediators of cardiovascular disease? J. Lipid Res. 46 2005 389 403
45. A.D. Howard, P.B. Verghese, E.L. Arrese, and J.L. Soulages Characterization of apoA-I-dependent lipid efflux from adipocytes and role of ABCA1 Mol. Cell. Biochem. 343 2010 115 124
46. E.G. Lund, C. Xie, T. Kotti, S.D. Turley, J.M. Dietschy, and D.W. Russell Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover J. Biol. Chem. 278 2003 22980 22988
47. H. Minagawa, J.S. Gong, C.G. Jung, A. Watanabe, S. Lund-Katz, M.C. Phillips, H. Saito, and M. Michikawa Mechanism underlying apolipoprotein E (ApoE) isoform-dependent lipid efflux from neural cells in culture J. Neurosci. Res. 87 2009 2498 2508
48. W.J. Johnson, F.H. Mahlberg, G.H. Rothblat, and M.C. Phillips Cholesterol transport between cells and high-density lipoproteins Biochim. Biophys. Acta 1085 1991 273 298
49. D.L. Williams, M.A. Connelly, R.E. Temel, S. Swarnakar, M.C. Phillips, M. de la Llera-Moya, and G.H. Rothblat Scavenger receptor BI and cholesterol trafficking Curr. Opin. Lipidol. 10 1999 329 339
50. J.F. Oram ATP-binding cassette transporter A1 and cholesterol trafficking Curr. Opin. Lipidol. 13 2002 373 381
51. N. Wang, D. Lan, W. Chen, F. Matsuura, and A.R. Tall ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins Proc. Natl. Acad. Sci. U. S. A. 101 2004 9774 9779
52. A. Rigotti, H.E. Miettinen, and M. Krieger The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues Endocr. Rev. 24 2003 357 387