Stimulation of the retinoid X receptor facilitates beta-amyloid clearance across the blood-brain barrier

Journal of Molecular Neuroscience

Volumn 49, Issue 2, 2013, Pages 270-276

  Bachmeier, Corbin ^a   Beaulieu Abdelahad, David ^a   Crawford, Fiona ^a   Mullan, Michael ^a   Paris, Daniel ^a  

^a ROSKAMP INSTITUTE   (United States)

Author keywords

Alzheimer's disease; Amyloid; Apolipoprotein E; Blood brain barrier; Retinoid X receptor

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; APOLIPOPROTEIN E; RETINOID X RECEPTOR;

ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; TRANSCYTOSIS;

AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; BLOOD-BRAIN BARRIER; CELL LINE; MALE; MICE; MICE, KNOCKOUT; RETINOID X RECEPTORS; TETRAHYDRONAPHTHALENES; TRANSCYTOSIS;

EID: 84874343048     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9866-6     Document Type: Article

References (45)

1. Bachmeier C, Mullan M, Paris D (2010) Characterization and use of human brain microvascular endothelial cells to examine beta-amyloid exchange in the blood-brain barrier. Cytotechnology 62:519-529
2. Bachmeier C, Paris D, Beaulieu-Abdelahad D, Mouzon B, Mullan M, Crawford F (2012) A multifaceted role for apoe in the clearance of beta-amyloid across the blood-brain barrier. Neurodegener Dis. doi: 10.1159/000337231
3. Bachmeier CJ, Beaulieu-Abdelahad D, Mullan MJ, Paris D (2011) Epitope-dependent effects of beta-amyloid antibodies on beta-amyloid clearance in an in vitro model of the blood-brain barrier. Microcirculation 18:373-379
4. Bu G (2009) Apolipoprotein E and its receptors in Alzheimer's disease: pathways, pathogenesis and therapy. Nat Rev Neurosci 10:333-344
5. Burgess JW, Marcel YL (2001) Dynamic and stable pools of apoE differ functionally at the hepg2 cell surface. J Lipid Res 42:1413-1420 (Pubitemid 34007671)
6. Camacho IE, Serneels L, Spittaels K, Merchiers P, Dominguez D, De Strooper B (2004) Peroxisome-proliferator-activated receptor gamma induces a clearance mechanism for the amyloid-beta peptide. J Neurosci 24:10908-10917 (Pubitemid 39602402)
7. Castellano JM, Kim J, Stewart FR et al (2011) Human apoE isoforms differentially regulate brain amyloid-beta peptide clearance. Sci Transl Med 3:89ra57
8. Chan GN, Hoque MT, Cummins CL, Bendayan R (2011) Regulation of p-glycoprotein by orphan nuclear receptors in human brain microvessel endothelial cells. J Neurochem 118:163-175
9. Cirrito JR, Deane R, Fagan AM et al (2005) P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model. J Clin Invest 115:3285-3290 (Pubitemid 41567593)
10. Cramer PE, Cirrito JR, Wesson DW et al (2012) Apoe-directed therapeutics rapidly clear beta-amyloid and reverse deficits in ad mouse models. Science 335:1503-1506
11. Dawson MI, Xia Z (2012) The retinoid x receptors and their ligands. Biochim Biophys Acta 1821:21-56
12. Deane R, Sagare A, Hamm K et al (2008) Apoe isoform-specific disruption of amyloid beta peptide clearance from mouse brain. J Clin Invest 118:4002-4013
13. Do TM, Noel-Hudson MS, Ribes S et al (2012) Abcg2- and abcg4-mediated efflux of amyloid-beta peptide 1-40 at the mouse blood-brain barrier. J Alzheimers Dis 30:155-166
14. Fitz NF, Cronican A, Pham T et al (2010) Liver x receptor agonist treatment ameliorates amyloid pathology and memory deficits caused by high-fat diet in app 23 mice. J Neurosci 30:6862-6872
15. Gauthier A, Vassiliou G, Benoist F, McPherson R (2003) Adipocyte low density lipoprotein receptor-related protein gene expression and function is regulated by peroxisome proliferator-activated receptor gamma. J Biol Chem 278:11945-11953 (Pubitemid 36800168)
16. Hessel S, Lampen A (2010) All-trans retinoic acid enhances the transport of phase ii metabolites of benzo[a]pyrene by inducing the breast cancer resistance protein expression in caco-2 cells. Toxicol Lett 197:151-155
17. Jiang Q, Lee CY, Mandrekar S et al (2008) Apoe promotes the proteolytic degradation of abeta. Neuron 58:681-693 (Pubitemid 351778466)
18. Kim J, Basak JM, Holtzman DM (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63:287-303
19. Kockx M, Guo DL, Huby T et al (2007) Secretion of apolipoprotein e from macrophages occurs via a protein kinase A and calcium-dependent pathway along the microtubule network. Circ Res 101:607-616 (Pubitemid 351325878)
20. Kockx M, Jessup W, Kritharides L (2008) Regulation of endogenous apolipoprotein E secretion by macrophages. Arterioscler Thromb Vasc Biol 28:1060-1067
21. Krohn M, Lange C, Hofrichter J et al (2011) Cerebral amyloid-beta proteostasis is regulated by the membrane transport protein abcc1 in mice. J Clin Invest 121:3924-3931
22. Kuhnke D, Jedlitschky G, Grube M et al (2007) Mdr1-p-glycoprotein (abcb1) mediates transport of Alzheimer's amyloid-beta peptides-implications for the mechanisms of abeta clearance at the blood-brain barrier. Brain Pathol 17:347-353 (Pubitemid 47537591)
23. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8:499-509 (Pubitemid 46985362)
24. Lefebvre P, Benomar Y, Staels B (2010) Retinoid x receptors: common heterodimerization partners with distinct functions. Trends Endocrinol Metab 21:676-683
25. Liang Y, Lin S, Beyer TP et al (2004) A liver x receptor and retinoid x receptor heterodimer mediates apolipoprotein e expression, secretion and cholesterol homeostasis in astrocytes. J Neurochem 88:623-634 (Pubitemid 38140207)
26. Lucas M, Mazzone T (1996) Cell surface proteoglycans modulate net synthesis and secretion of macrophage apolipoprotein E. J Biol Chem 271:13454-13460 (Pubitemid 26185388)
27. Mawuenyega KG, Sigurdson W, Ovod V et al (2010) Decreased clearance of CNS beta-amyloid in Alzheimer's disease. Science 330:1774
28. McLean CA, Cherny RA, Fraser FW et al (1999) Soluble pool of abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46:860-866
29. Mehta PD (2007) Amyloid beta protein as a marker or risk factor of Alzheimer's disease. Curr Alzheimer Res 4:359-363 (Pubitemid 47416628)
30. Nordberg A (2008) Amyloid imaging in Alzheimer's disease. Neuropsychologia 46:1636-1641
31. Paris D, Bachmeier C, Patel N et al (2011) Selective antihypertensive dihydropyridines lower abeta accumulation by targeting both the production and the clearance of abeta across the blood-brain barrier. Mol Med 17:149-162
32. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N (1992) Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 89:4471-4475
33. Podlisny MB, Ostaszewski BL, Squazzo SL et al (1995) Aggregation of secreted amyloid beta-protein into sodium dodecyl sulfate-stable oligomers in cell culture. J Biol Chem 270:9564-9570
34. Podlisny MB, Walsh DM, Amarante P et al (1998) Oligomerization of endogenous and synthetic amyloid beta-protein at nanomolar levels in cell culture and stabilization of monomer by Congo red. Biochemistry 37:3602-3611 (Pubitemid 28162915)
35. Shibata M, Yamada S, Kumar SR et al (2000) Clearance of Alzheimer's amyloid-ss(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier. J Clin Invest 106:1489-1499 (Pubitemid 32038587)
36. Suon S, Zhao J, Villarreal SA et al (2010) Systemic treatment with liver x receptor agonists raises apolipoprotein E, cholesterol, and amyloid-beta peptides in the cerebral spinal fluid of rats. Mol Neurodegener 5:44
37. Tai LM, Loughlin AJ, Male DK, Romero IA (2009) P-glycoprotein and breast cancer resistance protein restrict apical-to-basolateral permeability of human brain endothelium to amyloid-beta. J Cereb Blood Flow Metab 29:1079-1083
38. Tao H, Aakula S, Abumrad NN, Hajri T (2010) Peroxisome proliferator-activated receptor-gamma regulates the expression and function of very-low-density lipoprotein receptor. Am J Physiol Endocrinol Metab 298:E68-E79
39. Tsukuda K, Mogi M, Iwanami J et al (2009) Cognitive deficit in amyloid-beta-injected mice was improved by pretreatment with a low dose of telmisartan partly because of peroxisome proliferator-activated receptor-gamma activation. Hypertension 54:782-787
40. Vogelgesang S, Cascorbi I, Schroeder E et al (2002) Deposition of Alzheimer's beta-amyloid is inversely correlated with p-glycoprotein expression in the brains of elderly non-demented humans. Pharmacogenetics 12:535-541 (Pubitemid 35177083)
41. Weller RO, Boche D, Nicoll JA (2009) Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy. Acta Neuropathol 118:87-102
42. Wells JM, Amaratunga A, McKenna DC, Abraham CR, Fine RE (1995) Amyloid β-protein precursor and apolipoprotein e production in cultured cerebral endothelial cells isolated from brains of patients with neurodegenerative disorders at autopsy. Amyloid 2:229-233 (Pubitemid 3011583)
43. Yue L, Mazzone T (2009) Peroxisome proliferator-activated receptor gamma stimulation of adipocyte apoe gene transcription mediated by the liver receptor x pathway. J Biol Chem 284:10453-10461
44. Zelcer N, Khanlou N, Clare R et al (2007) Attenuation of neuroinflammation and Alzheimer's disease pathology by liver x receptors. Proc Natl Acad Sci USA 104:10601-10606 (Pubitemid 47185711)
45. Zhong N, Weisgraber KH (2009) Understanding the basis for the association of apoe4 with Alzheimer's disease: opening the door for therapeutic approaches. Curr Alzheimer Res 6:415-418