Effects of oxysterols on the blood-brain barrier: Implications for Alzheimer's disease

Biochemical and Biophysical Research Communications

Volumn 446, Issue 3, 2014, Pages 687-691

  Gosselet, Fabien ^a,b   Saint Pol, Julien ^a   Fenart, Laurence ^a  

^a UNIV LILLE   (France)

^b UNIVERSITÉ D'ARTOIS   (France)

Author keywords

ABCA1; ABCB1; Alzheimer's disease; Blood brain barrier; LXR; Oxysterols

Indexed keywords

26 HYDROXYCHOLESTEROL; ABC TRANSPORTER A1; ABC TRANSPORTER G1; ACETYL COENZYME A; APOLIPOPROTEIN E; CHOLESTEROL; CYTOCHROME P450; LIVER X RECEPTOR; OXYSTEROL;

ALZHEIMER DISEASE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN PERICYTE; CHEMICAL STRUCTURE; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; GLIA CELL; HOMEOSTASIS; HUMAN; MYELINATION; NEUROTRANSMITTER RELEASE; NONHUMAN; PEPTIDE SYNTHESIS; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SYNAPTOGENESIS; TIGHT JUNCTION; UPREGULATION;

ABCA1; ABCB1; ALZHEIMER'S DISEASE; BLOOD-BRAIN BARRIER; LXR; OXYSTEROLS;

ALZHEIMER DISEASE; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CHOLESTEROL; HOMEOSTASIS; HUMANS; HYDROXYCHOLESTEROLS;

EID: 84898831894     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.11.059     Document Type: Article

References (61)

1. J.E. Vance Dysregulation of cholesterol balance in the brain: contribution to neurodegenerative diseases Dis. Model. Mech. 5 2012 746 755
2. I.J. Martins, T. Berger, M.J. Sharman, G. Verdile, S.J. Fuller, and R.N. Martins Cholesterol metabolism and transport in the pathogenesis of Alzheimer's disease J. Neurochem. 111 2009 1275 1308
3. 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
4. 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
5. 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
6. E.G. Lund, J.M. Guileyardo, and D.W. Russell CDNA cloning of cholesterol 24-hydroxylase, a mediator of cholesterol homeostasis in the brain Proc. Natl. Acad. Sci. USA 96 1999 7238 7243
7. Y. Ohyama, S. Meaney, M. Heverin, L. Ekstrom, A. Brafman, M. Shafir, U. Andersson, M. Olin, G. Eggertsen, U. Diczfalusy, E. Feinstein, and I. Bjorkhem Studies on the transcriptional regulation of cholesterol 24-hydroxylase (CYP46A1): marked insensitivity toward different regulatory axes J. Biol. Chem. 281 2006 3810 3820
8. D. Lutjohann, O. Breuer, G. Ahlborg, I. Nennesmo, A. Siden, U. Diczfalusy, and I. Bjorkhem Cholesterol homeostasis in human brain: evidence for an age-dependent flux of 24S-hydroxycholesterol from the brain into the circulation Proc. Natl. Acad. Sci. USA 93 1996 9799 9804
9. M. Heverin, S. Meaney, D. Lutjohann, U. Diczfalusy, J. Wahren, and I. Bjorkhem Crossing the barrier: net flux of 27-hydroxycholesterol into the human brain J. Lipid Res. 46 2005 1047 1052
10. J. Vaya, and H.M. Schipper Oxysterols, cholesterol homeostasis, and Alzheimer disease J. Neurochem. 102 2007 1727 1737
11. D.K. Spady, M. Huettinger, D.W. Bilheimer, and J.M. Dietschy Role of receptor-independent low density lipoprotein transport in the maintenance of tissue cholesterol balance in the normal and WHHL rabbit J. Lipid Res. 28 1987 32 41
12. J.D. Wilson The measurement of the exchangeable pools of cholesterol in the baboon J. Clin. Invest. 49 1970 655 665
13. A.V. Chobanian, B.A. Burrows, and W. Hollander Body cholesterol metabolism in man. II. Measurement of the body cholesterol miscible pool and turnover rate J. Clin. Invest. 41 1962 1738 1744
14. A.V. Chobanian, and W. Hollander Body cholesterol metabolism in man. I. The equilibration of serum and tissue cholesterol J. Clin. Invest. 41 1962 1732 1737
15. B.A. Golomb, H. Stattin, and S. Mednick Low cholesterol and violent crime J. Psychiatr. Res. 34 2000 301 309
16. M. Virkkunen, and H. Penttinen Serum cholesterol in aggressive conduct disorder: a preliminary study Biol. Psychiatry 19 1984 435 439
17. B.A. Golomb Cholesterol and violence: is there a connection? Ann. Intern. Med. 128 1998 478 487
18. N.F. Fitz, A.A. Cronican, M. Saleem, A.H. Fauq, R. Chapman, I. Lefterov, and R. Koldamova Abca1 deficiency affects Alzheimer's disease-like phenotype in human ApoE4 but not in ApoE3-targeted replacement mice J. Neurosci. 32 2012 13125 13136
19. A.J. George, R.M. Holsinger, C.A. McLean, K.M. Laughton, K. Beyreuther, G. Evin, C.L. Masters, and Q.X. Li APP intracellular domain is increased and soluble Abeta is reduced with diet-induced hypercholesterolemia in a transgenic mouse model of Alzheimer disease Neurobiol. Dis. 16 2004 124 132
20. L.M. Refolo, B. Malester, J. LaFrancois, T. Bryant-Thomas, R. Wang, G.S. Tint, K. Sambamurti, K. Duff, and M.A. Pappolla Hypercholesterolemia accelerates the Alzheimer's amyloid pathology in a transgenic mouse model Neurobiol. Dis. 7 2000 321 331
21. D.L. Sparks, S.W. Scheff, J.C. Hunsaker III, H. Liu, T. Landers, and D.R. Gross Induction of Alzheimer-like beta-amyloid immunoreactivity in the brains of rabbits with dietary cholesterol Exp. Neurol. 126 1994 88 94
22. A. Solomon, M. Kivipelto, B. Wolozin, J. Zhou, and R.A. Whitmer Midlife serum cholesterol and increased risk of Alzheimer's and vascular dementia three decades later Dement. Geriatr. Cogn. Disord. 28 2009 75 80
23. M. Kivipelto, E.L. Helkala, M.P. Laakso, T. Hanninen, M. Hallikainen, K. Alhainen, H. Soininen, J. Tuomilehto, and A. Nissinen Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study BMJ 322 2001 1447 1451
24. J.M. Karasinska, F. Rinninger, D. Lutjohann, 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. 29 2009 3579 3589
25. P. Candela, F. Gosselet, F. Miller, V. Buee-Scherrer, G. Torpier, R. Cecchelli, and L. Fenart Physiological pathway for low-density lipoproteins across the blood-brain barrier: transcytosis through brain capillary endothelial cells in vitro Endothelium 15 2008 254 264
26. B. Dehouck, M.P. Dehouck, J.C. Fruchart, and R. Cecchelli Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes J. Cell Biol. 126 1994 465 473
27. B. Dehouck, L. Fenart, M.P. Dehouck, A. Pierce, G. Torpier, and R. Cecchelli A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier J. Cell Biol. 138 1997 877 889
28. F. Gosselet The mysterious link between cholesterol and Alzheimer's Disease: is the blood-brain barrier a suspect? J. Alzheimer's Dis. Parkinsonism 1 2011 10.4172/2161-0460.1000103e
29. R. Cecchelli, V. Berezowski, S. Lundquist, M. Culot, M. Renftel, M.P. Dehouck, and L. Fenart Modelling of the blood-brain barrier in drug discovery and development Nat. Rev. Drug Discov. 6 2007 650 661
30. N.J. Abbott, A.A. Patabendige, D.E. Dolman, S.R. Yusof, and D.J. Begley Structure and function of the blood-brain barrier Neurobiol. Dis. 37 2010 13 25
31. F. Gosselet, P. Candela, R. Cecchelli, and L. Fenart Role of the blood-brain barrier in Alzheimer's disease Med. Sci. (Paris) 27 2011 987 992
32. N.J. Abbott, L. Ronnback, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat. Rev. Neurosci. 7 2006 41 53
33. S. Ohtsuki, Y. Watanabe, S. Hori, H. Suzuki, J. Bhongsatiern, M. Fujiyoshi, M. Kamoi, N. Kamiya, H. Takanaga, and T. Terasaki MRNA expression of the ATP-binding cassette transporter subfamily A (ABCA) in rat and human brain capillary endothelial cells Biol. Pharm. Bull. 27 2004 1437 1440
34. S. Akanuma, S. Hori, S. Ohtsuki, M. Fujiyoshi, and T. Terasaki Expression of nuclear receptor mRNA and liver X receptor-mediated regulation of ABC transporter A1 at rat blood-brain barrier Neurochem. Int. 52 2008 669 674
35. F. Gosselet, P. Candela, E. Sevin, V. Berezowski, R. Cecchelli, and L. Fenart Transcriptional profiles of receptors and transporters involved in brain cholesterol homeostasis at the blood-brain barrier: use of an in vitro model Brain Res. 1249 2009 34 42
36. U. Panzenboeck, Z. Balazs, A. Sovic, A. Hrzenjak, S. Levak-Frank, A. Wintersperger, E. Malle, and W. Sattler ABCA1 and scavenger receptor class B, type I, are modulators of reverse sterol transport at an in vitro blood-brain barrier constituted of porcine brain capillary endothelial cells J. Biol. Chem. 277 2002 42781 42789
37. T.M. Do, M. Ouellet, F. Calon, G. Chimini, H. Chacun, R. Farinotti, and F. Bourasset Direct evidence of abca1-mediated efflux of cholesterol at the mouse blood-brain barrier Mol. Cell. Biochem. 357 2011 397 404
38. J. Saint-Pol, P. Candela, M.C. Boucau, L. Fenart, and F. Gosselet Oxysterols decrease apical-to-basolateral transport of Ass peptides via an ABCB1-mediated process in an in vitro blood-brain barrier model constituted of bovine brain capillary endothelial cells Brain Res. 1517 2013 1 15
39. J. Saint-Pol, E. Vandenhaute, M.C. Boucau, P. Candela, L. Dehouck, R. Cecchelli, M.P. Dehouck, L. Fenart, and F. Gosselet Brain pericytes ABCA1 expression mediates cholesterol efflux but not cellular amyloid-beta peptide accumulation J. Alzheimers Dis. 30 2012 489 503
40. U. Panzenboeck, I. Kratzer, A. Sovic, A. Wintersperger, E. Bernhart, A. Hammer, E. Malle, and W. Sattler Regulatory effects of synthetic liver X receptor- and peroxisome-proliferator activated receptor agonists on sterol transport pathways in polarized cerebrovascular endothelial cells Int. J. Biochem. Cell Biol. 38 2006 1314 1329
41. C. Schweinzer, A. Kober, I. Lang, K. Etschmaier, M. Scholler, A. Kresse, W. Sattler, and U. Panzenboeck Processing of endogenous AbetaPP in blood-brain barrier endothelial cells is modulated by liver-X receptor agonists and altered cellular cholesterol homeostasis J. Alzheimers Dis. 27 2011 341 360
42. S. Meaney, K. Bodin, U. Diczfalusy, and I. Bjorkhem On the rate of translocation in vitro and kinetics in vivo of the major oxysterols in human circulation: critical importance of the position of the oxygen function J. Lipid Res. 43 2002 2130 2135
43. S. Ohtsuki, S. Ito, A. Matsuda, S. Hori, T. Abe, and T. Terasaki Brain-to-blood elimination of 24S-hydroxycholesterol from rat brain is mediated by organic anion transporting polypeptide 2 (oatp2) at the blood-brain barrier J. Neurochem. 103 2007 1430 1438
44. V. Leoni, and C. Caccia 24S-hydroxycholesterol in plasma: a marker of cholesterol turnover in neurodegenerative diseases Biochimie 95 2013 595 612
45. T.M. Jeitner, I. Voloshyna, and A.B. Reiss Oxysterol derivatives of cholesterol in neurodegenerative disorders Curr. Med. Chem. 18 2011 1515 1525
46. J.A. Lynch, A.M. George, P.B. Eisenhauer, K. Conn, W. Gao, I. Carreras, J.M. Wells, A. McKee, M.D. Ullman, and R.E. Fine Insulin degrading enzyme is localized predominantly at the cell surface of polarized and unpolarized human cerebrovascular endothelial cell cultures J. Neurosci. Res. 83 2006 1262 1270
47. P. Candela, F. Gosselet, J. Saint-Pol, E. Sevin, M.C. Boucau, E. Boulanger, R. Cecchelli, and L. Fenart Apical-to-basolateral transport of amyloid-beta peptides through blood-brain barrier cells is mediated by the receptor for advanced glycation end-products and is restricted by P-glycoprotein J. Alzheimers Dis. 22 2010 849 859
48. J. Pahnke, O. Wolkenhauer, M. Krohn, and L.C. Walker Clinico-pathologic function of cerebral ABC transporters - implications for the pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 5 2008 396 405
49. J.R. Cirrito, R. Deane, A.M. Fagan, M.L. Spinner, M. Parsadanian, M.B. Finn, H. Jiang, J.L. Prior, A. Sagare, K.R. Bales, S.M. Paul, B.V. Zlokovic, D. Piwnica-Worms, and D.M. Holtzman P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model J. Clin. Invest. 115 2005 3285 3290
50. M. Krohn, C. Lange, J. Hofrichter, K. Scheffler, J. Stenzel, J. Steffen, T. Schumacher, T. Bruning, A.S. Plath, F. Alfen, A. Schmidt, F. Winter, K. Rateitschak, A. Wree, J. Gsponer, L.C. Walker, and J. Pahnke Cerebral amyloid-beta proteostasis is regulated by the membrane transport protein ABCC1 in mice J. Clin. Invest. 121 2011 3924 3931
51. A. ElAli, and D.M. Hermann Liver X receptor activation enhances blood-brain barrier integrity in the ischemic brain and increases the abundance of ATP-binding cassette transporters ABCB1 and ABCC1 on brain capillary cells Brain Pathol. 22 2012 175 187
52. D.M. van Assema, M. Lubberink, M. Bauer, W.M. van der Flier, R.C. Schuit, A.D. Windhorst, E.F. Comans, N.J. Hoetjes, N. Tolboom, O. Langer, M. Muller, P. Scheltens, A.A. Lammertsma, and B.N. van Berckel Blood-brain barrier P-glycoprotein function in Alzheimer's disease Brain 135 2012 181 189
53. S. Vogelgesang, R.W. Warzok, I. Cascorbi, C. Kunert-Keil, E. Schroeder, H.K. Kroemer, W. Siegmund, L.C. Walker, and J. Pahnke The role of P-glycoprotein in cerebral amyloid angiopathy; implications for the early pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 1 2004 121 125
54. H. Qosa, A.H. Abuznait, R.A. Hill, and A. Kaddoumi Enhanced brain amyloid-beta clearance by rifampicin and caffeine as a possible protective mechanism against Alzheimer's disease J. Alzheimers Dis. 31 2012 151 165
55. A.M. Hartz, D.S. Miller, and B. Bauer Restoring blood-brain barrier P-glycoprotein reduces brain amyloid-beta in a mouse model of Alzheimer's disease Mol. Pharmacol. 77 2010 715 723
56. G.N. Chan, M.T. Hoque, and R. Bendayan Role of nuclear receptors in the regulation of drug transporters in the brain Trends Pharmacol. Sci. 34 2013 361 372
57. E. Hudry, D. Van Dam, W. Kulik, P.P. De Deyn, F.S. Stet, O. Ahouansou, A. Benraiss, A. Delacourte, P. Bougneres, P. Aubourg, and N. Cartier Adeno-associated virus gene therapy with cholesterol 24-hydroxylase reduces the amyloid pathology before or after the onset of amyloid plaques in mouse models of Alzheimer's disease Mol. Ther. 18 2010 44 53
58. S. Akanuma, S. Ohtsuki, Y. Doi, M. Tachikawa, S. Ito, S. Hori, T. Asashima, T. Hashimoto, K. Yamada, K. Ueda, T. Iwatsubo, and T. Terasaki ATP-binding cassette transporter A1 (ABCA1) deficiency does not attenuate the brain-to-blood efflux transport of human amyloid-beta peptide (1-40) at the blood-brain barrier Neurochem. Int. 52 2008 956 961
59. R.D. Bell, A.P. Sagare, A.E. Friedman, G.S. Bedi, D.M. Holtzman, R. Deane, and B.V. Zlokovic 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. 27 2007 909 918
60. 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
61. R. Ehehalt, P. Keller, C. Haass, C. Thiele, and K. Simons Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts J. Cell Biol. 160 2003 113 123