Retinoic acid isomers facilitate apolipoprotein e production and lipidation in astrocytes through the retinoid X receptor/retinoic acid receptor pathway

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11282-11292

  Zhao, Jing ^a,b   Fu, Yuan ^b   Liu, Chia Chen ^b,c   Shinohara, Mitsuru ^b   Nielsen, Henrietta M ^b   Dong, Qiang ^a   Kanekiyo, Takahisa ^b   Bu, Guojun ^b,c  

^a FUDAN UNIVERSITY   (China)

^b MAYO GRADUATE SCHOOL   (United States)

^c XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEINS;

ACID RECEPTORS; ALL-TRANS-RETINOIC ACID; ALZHEIMER DISEASE; APOLIPOPROTEIN E; APOLIPOPROTEIN E (APOE); LIPIDATION; RETINOIC ACIDS; RETINOID X RECEPTOR;

ISOMERS;

ABC TRANSPORTER A1; ABC TRANSPORTER G1; ALITRETINOIN; AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; ASPARTATE AMINOTRANSFERASE; BEXAROTENE; ISOTRETINOIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR ALPHA; RETINOID X RECEPTOR; RETINOID X RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; ASTROCYTE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DRUG CYTOTOXICITY; FEMALE; MALE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID; APOE; CHOLESTEROL; RETINOIC ACID; RETINOID;

ALLELES; ALZHEIMER DISEASE; ANIMALS; ANTICARCINOGENIC AGENTS; APOLIPOPROTEINS E; ASTROCYTES; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN; CELL LINE, TRANSFORMED; HUMANS; LIPOPROTEINS; LIPOYLATION; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; TETRAHYDRONAPHTHALENES; TRETINOIN;

EID: 84898938661     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.526095     Document Type: Article

References (73)

1. Zheng, H., and Koo, E. H. (2011) Biology and pathophysiology of the amyloid precursor protein. Mol. Neurodegener. 6, 27
2. Hardy, J., and Selkoe, D. J. (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356
3. Blennow, K., de Leon, M. J., and Zetterberg, H. (2006) Alzheimer's disease. Lancet 368, 387-403
4. Thies, W., and Bleiler, L. (2013) 2013 Alzheimer's disease facts and figures. Alzheimers Dement. 9, 208-245
5. Rayaprolu, S., Mullen, B., Baker, M., Lynch, T., Finger, E., Seeley, W. W., Hatanpaa, K. J., Lomen-Hoerth, C., Kertesz, A., Bigio, E. H., Lippa, C., Josephs, K. A., Knopman, D. S., White, C. L., 3rd, Caselli, R., Mackenzie, I. R., Miller, B. L., Boczarska-Jedynak, M., Opala, G., Krygowska-Wajs, A., Barcikowska, M., Younkin, S. G., Petersen, R. C., Ertekin-Taner, N., Uitti, R. J., Meschia, J. F., Boylan, K. B., Boeve, B. F., Graff-Radford, N. R., Wszolek, Z. K., Dickson, D. W., Rademakers, R., and Ross, O. A. (2013) TREM2 in neurodegeneration: Evidence for association of the p.R47H variant with frontotemporal dementia and Parkinson's disease. Mol. Neurodegener. 8, 19
6. 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. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261, 921-923
7. Strittmatter, W. J., Saunders, A. M., Schmechel, D., Pericak-Vance, M., Enghild, J., Salvesen, G. S., and Roses, A. D. (1993) Apolipoprotein E: High-avidity binding toβ-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 90, 1977-1981
8. Liu, C. C., Liu, C. C., Kanekiyo, T., Xu, H., and Bu, G. (2013) Apolipoprotein E and Alzheimer disease: Risk, mechanisms and therapy. Nat. Rev. Neurol. 9, 106-118
9. Kanekiyo, T., Xu, H., and Bu, G. (2014) ApoE and Aβ in Alzheimer's disease: Accidental encounters or partners? Neuron 81, 740-754
10. Huang, Y., and Mucke, L. (2012) Alzheimer mechanisms and therapeutic strategies. Cell 148, 1204-1222
11. Kim, J., Basak, J. M., and Holtzman, D. M. (2009) The role of apolipoprotein E in Alzheimer's disease. Neuron 63, 287-303
12. Song, H., and Bu, G. (2009) MicroRNA-205 inhibits tumor cell migration through down-regulating the expression of the LDL receptor-related protein 1. Biochem. Biophys. Res. Commun. 388, 400-405
13. Liraz, O., Boehm-Cagan, A., and Michaelson, D. M. (2013) ApoE4 induces Aβ42, tau, and neuronal pathology in the hippocampus of young targeted replacement apoE4 mice. Mol. Neurodegener. 8, 16
14. Vance, J. E., and Hayashi, H. (2010) Formation and function of apolipoprotein E-containing lipoproteins in the nervous system. Biochim. Biophys. Acta 1801, 806-818
15. Pfrieger, F. W. (2003) Cholesterol homeostasis and function in neurons of the central nervous system. Cell. Mol. Life Sci. 60, 1158-1171
16. Cruchaga, C., Kauwe, J. S., Nowotny, P., Bales, K., Pickering, E. H., Mayo, K., Bertelsen, S., Hinrichs, A., Alzheimer's Disease Neuroimaging Initiative, Fagan, A. M., Holtzman, D. M., Morris, J. C., and Goate, A. M. (2012) Cerebrospinal fluid APOE levels: An endophenotype for genetic studies for Alzheimer's disease. Hum. Mol. Genet. 21, 4558-4571
17. Reitz, C., Tang, M. X., Luchsinger, J., and Mayeux, R. (2004) Relation of plasma lipids to Alzheimer disease and vascular dementia. Arch. Neurol. 61, 705-714
18. Donkin, J. J., Stukas, S., Hirsch-Reinshagen, V., Namjoshi, D., Wilkinson, A., May, S., Chan, J., Fan, J., Collins, J., and Wellington, C. L. (2010) ATPbinding cassette transporter A1 mediates the beneficial effects of the liver X receptor agonist GW3965 on object recognition memory and amyloid burden in amyloid precursor protein/presenilin 1 mice. J. Biol. Chem. 285, 34144-34154
19. Fitz, N. F., Cronican, A., Pham, T., Fogg, A., Fauq, A. H., Chapman, R., Lefterov, I., and Koldamova, R. (2010) Liver X receptor agonist treatment ameliorates amyloid pathology and memory deficits caused by high-fat diet in APP23 mice. J. Neurosci. 30, 6862-6872
20. Koldamova, R. P., Lefterov, I. M., Staufenbiel, M., Wolfe, D., Huang, S., Glorioso, J. C., Walter, M., Roth, M. G., and Lazo, J. S. (2005) The liver X receptor ligand T0901317 decreases amyloid β production in vitro and in a mouse model of Alzheimer's disease. J. Biol. Chem. 280, 4079-4088
21. Cramer, P. E., Cirrito, J. R., Wesson, D. W., Lee, C. Y., Karlo, J. C., Zinn, A. E., Casali, B. T., Restivo, J. L., Goebel, W. D., James, M. J., Brunden, K. R., Wilson, D. A., and Landreth, G. E. (2012) ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science 335, 1503-1506
22. Groot, P. H., Pearce, N. J., Yates, J. W., Stocker, C., Sauermelch, C., Doe, C. P., Willette, R. N., Olzinski, A., Peters, T., d'Epagnier, D., Morasco, K. O., Krawiec, J. A., Webb, C. L., Aravindhan, K., Jucker, B., Burgert, M., Ma, C., Marino, J. P., Collins, J. L., Macphee, C. H., Thompson, S. K., and Jaye, M. (2005) Synthetic LXR agonists increase LDL in CETP species. J. Lipid Res. 46, 2182-2191
23. Morikawa, M., Fryer, J. D., Sullivan, P. M., Christopher, E. A., Wahrle, S. E., DeMattos, R. B., O'Dell, M. A., Fagan, A. M., Lashuel, H. A., Walz, T., Asai, K., and Holtzman, D. M. (2005) Production and characterization of astrocyte-derived human apolipoprotein E isoforms from immortalized astrocytes and their interactions with amyloid-β. Neurobiol. Dis. 19, 66-76
24. Liu, Q., Zerbinatti, C. V., Zhang, J., Hoe, H. S., Wang, B., Cole, S. L., Herz, J., Muglia, L., and Bu, G. (2007) Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1. Neuron 56, 66-78
25. Weinstein, D. E. (2001) Isolation and purification of primary rodent astrocytes. Curr. Protoc. Neurosci. 10.1002/0471142301.ns0305s00
26. Krul, E. S., Tikkanen, M. J., and Schonfeld, G. (1988) Heterogeneity of apolipoprotein E epitope expression on human lipoproteins: Importance for apolipoprotein E function. J. Lipid Res. 29, 1309-1325
27. Wahrle, S. E., Shah, A. R., Fagan, A. M., Smemo, S., Kauwe, J. S., Grupe, A., Hinrichs, A., Mayo, K., Jiang, H., Thal, L. J., Goate, A. M., and Holtzman, D. M. (2007) Apolipoprotein E levels in cerebrospinal fluid and the effects of ABCA1 polymorphisms. Mol. Neurodegener. 2, 7
28. Li, J., Kanekiyo, T., Shinohara, M., Zhang, Y., LaDu, M. J., Xu, H., and Bu, G. (2012) Differential regulation of amyloid-β endocytic trafficking and lysosomal degradation by apolipoprotein E isoforms. J. Biol. Chem. 287, 44593-44601
29. Fagan, A. M., Holtzman, D. M., Munson, G., Mathur, T., Schneider, D., Chang, L. K., Getz, G. S., Reardon, C. A., Lukens, J., Shah, J. A., and LaDu, M. J. (1999) Unique lipoproteins secreted by primary astrocytes from wild type, apoE (-/-), and human apoE transgenic mice. J. Biol. Chem. 274, 30001-30007
30. Fagan, A. M., Younkin, L. H., Morris, J. C., Fryer, J. D., Cole, T. G., Younkin, S. G., and Holtzman, D. M. (2000) Differences in theAβ40/Aβ42 ratio associated with cerebrospinal fluid lipoproteins as a function of apolipoprotein E genotype. Ann. Neurol. 48, 201-210
31. Chen, J., Costa, L. G., and Guizzetti, M. (2011) 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, 870-878
32. Liu, C. C., Pearson, C., and Bu, G. (2009) Cooperative folding and ligandbinding properties of LRP6 β-propeller domains. J. Biol. Chem. 284, 15299-15307
33. Väkevä, L., Ranki, A., and Hahtola, S. (2012) Ten-year experience of bexarotene therapy for cutaneous T-cell lymphoma in Finland. Acta Derm. Venereol. 92, 258-263
34. Nielsen, H. M., Mulder, S. D., Beliën, J. A., Musters, R. J., Eikelenboom, P., and Veerhuis, R. (2010) Astrocytic Aβ 1-42 uptake is determined by Aβ-aggregation state and the presence of amyloid-associated proteins. Glia 58, 1235-1246
35. Idres, N., Marill, J., Flexor, M. A., and Chabot, G. G. (2002) Activation of retinoic acid receptor-dependent transcription by all-trans-retinoic acid metabolites and isomers. J. Biol. Chem. 277, 31491-31498
36. Blaner, W. S. (2001) Cellular metabolism and actions of 13-cis-retinoic acid. J. Am. Acad. Dermatol. 45, S129-135
37. Bastien, J., and Rochette-Egly, C. (2004) Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 328, 1-16
38. Germain, P., Chambon, P., Eichele, G., Evans, R. M., Lazar, M. A., Leid, M., De Lera, A. R., Lotan, R., Mangelsdorf, D. J., and Gronemeyer, H. (2006) International Union of Pharmacology. LXIII. Retinoid X receptors. Pharmacol. Rev. 58, 760-772
39. Germain, P., Chambon, P., Eichele, G., Evans, R. M., Lazar, M. A., Leid, M., De Lera, A. R., Lotan, R., Mangelsdorf, D. J., and Gronemeyer, H. (2006) International Union of Pharmacology. LX. Retinoic acid receptors. Pharmacol. Rev. 58, 712-725
40. Willy, P. J., Umesono, K., Ong, E. S., Evans, R. M., Heyman, R. A., and Mangelsdorf, D. J. (1995) LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9, 1033-1045
41. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
42. Maden, M., and Hind, M. (2003) Retinoic acid, a regeneration-inducing molecule. Dev. Dyn. 226, 237-244
43. Tafti, M., and Ghyselinck, N. B. (2007) Functional implication of the vitamin A signaling pathway in the brain. Arch. Neurol. 64, 1706-1711
44. Cocco, S., Diaz, G., Stancampiano, R., Diana, A., Carta, M., Curreli, R., Sarais, L., and Fadda, F. (2002) Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 115, 475-482
45. Shudo, K., Fukasawa, H., Nakagomi, M., and Yamagata, N. (2009) Towards retinoid therapy for Alzheimer's disease. Curr. Alzheimer Res. 6, 302-311
46. Ahlemeyer, B., and Krieglstein, J. (2000) Inhibition of glutathione depletion by retinoic acid and tocopherol protects cultured neurons from staurosporine- induced oxidative stress and apoptosis. Neurochem. Int. 36, 1-5
47. Shen, H., Luo, Y., Kuo, C. C., Deng, X., Chang, C. F., Harvey, B. K., Hoffer, B. J., and Wang, Y. (2009) 9-cis-Retinoic acid reduces ischemic brain injury in rodents via bone morphogenetic protein. J. Neurosci. Res. 87, 545-555
48. Grant, W. B. (1999) Dietary links to Alzheimer's disease: 1999 update. J. Alzheimers Dis. 1, 197-201
49. Ding, Y., Qiao, A., Wang, Z., Goodwin, J. S., Lee, E. S., Block, M. L., Allsbrook, M., McDonald, M. P., and Fan, G. H. (2008) Retinoic acid attenuates β-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model. J. Neurosci. 28, 11622-11634
50. Koldamova, R. P., Lefterov, I. M., Ikonomovic, M. D., Skoko, J., Lefterov, P. I., Isanski, B. A., DeKosky, S. T., and Lazo, J. S. (2003) 22R-Hydroxycholesterol and 9-cis-retinoic acid induce ATP-binding cassette transporter A1 expression and cholesterol efflux in brain cells and decrease amyloid β secretion. J. Biol. Chem. 278, 13244-13256
51. Walter, J., and van Echten-Deckert, G. (2013) Cross-talk of membrane lipids and Alzheimer-related proteins. Mol. Neurodegener. 8, 34
52. Wahrle, S. E., Jiang, H., Parsadanian, M., Legleiter, J., Han, X., Fryer, J. D., Kowalewski, T., and Holtzman, D. M. (2004) ABCA1 is required for normal central nervous system ApoE levels and for lipidation of astrocytesecreted apoE. J. Biol. Chem. 279, 40987-40993
53. Oram, J. F., and Lawn, R. M. (2001) ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 42, 1173-1179
54. Karten, B., Campenot, R. B., Vance, D. E., and Vance, J. E. (2006) Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J. Biol. Chem. 281, 4049-4057
55. Wang, N., Lan, D., Chen, W., Matsuura, F., and Tall, A. R. (2004) ATPbinding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. U.S.A. 101, 9774-9779
56. 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. (2005) The absence of ABCA1decreases soluble apoE levels but does not diminish amyloid deposition in two murine models of Alzheimer disease. J. Biol. Chem. 280, 43243-43256
57. Koldamova, R., Staufenbiel, M., and Lefterov, I. (2005) Lack of ABCA1 considerably decreases brain apoE level and increases amyloid deposition in APP23 mice. J. Biol. Chem. 280, 43224-43235
58. Wahrle, S. E., Jiang, H., Parsadanian, M., Hartman, R. E., Bales, K. R., Paul, S. M., and Holtzman, D. M. (2005) Deletion of Abca1 increases Aβ deposition in the PDAPP transgenic mouse model of Alzheimer disease. J. Biol. Chem. 280, 43236-43242
59. Fan, J., Donkin, J., and Wellington, C. (2009) Greasing the wheels of Aβ clearance in Alzheimer's disease: the role of lipids and apolipoprotein E. Biofactors 35, 239-248
60. Koldamova, R., Fitz, N. F., and Lefterov, I. (2010) The role of ATP-binding cassette transporter A1 in Alzheimer's disease and neurodegeneration. Biochim. Biophys. Acta 1801, 824-830
61. DeMattos, R. B., Cirrito, J. R., Parsadanian, M., May, P. C., O'Dell, M. A., Taylor, J. W., Harmony, J. A., Aronow, B. J., Bales, K. R., Paul, S. M., and Holtzman, D. M. (2004) ApoE and clusterin cooperatively suppress Aβ levels and deposition: evidence that ApoE regulates extracellular Aβ metabolism in vivo. Neuron 41, 193-202
62. Ma, J., Yee, A., Brewer, H. B., Jr., Das, S., and Potter, H. (1994) Amyloidassociated proteins β1-antichymotrypsin and apolipoprotein E promote assembly of Alzheimer β-protein into filaments. Nature 372, 92-94
63. Koistinaho, M., Lin, S., Wu, X., Esterman, M., Koger, D., Hanson, J., Higgs, R., Liu, F., Malkani, S., Bales, K. R., and Paul, S. M. (2004) Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-β peptides. Nat. Med. 10, 719-726
64. Manelli, A. M., Stine, W. B., Van Eldik, L. J., and LaDu, M. J. (2004) ApoE and Aβ1-42 interactions: effects of isoform and conformation on structure and function. J. Mol. Neurosci. 23, 235-246
65. Trommer, B. L., Shah, C., Yun, S. H., Gamkrelidze, G., Pasternak, E. S., Stine, W. B., Manelli, A., Sullivan, P., Pasternak, J. F., and LaDu, M. J. (2005) ApoE isoform-specific effects on LTP: Blockade by oligomeric amyloid-β1-42. Neurobiol. Dis. 18, 75-82
66. Stratman, N. C., Castle, C. K., Taylor, B. M., Epps, D. E., Melchior, G. W., and Carter, D. B. (2005) Isoform-specific interactions of human apolipoprotein E to an intermediate conformation of human Alzheimer amyloid-β peptide. Chem. Phys. Lipids 137, 52-61
67. Verghese, P. B., Castellano, J. M., Garai, K., Wang, Y., Jiang, H., Shah, A., Bu, G., Frieden, C., and Holtzman, D. M. (2013) ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions. Proc. Natl. Acad. Sci. U.S.A. 110, E1807-E1816
68. Wang, Y., Yao, R., Maciag, A., Grubbs, C. J., Lubet, R. A., and You, M. (2006) Organ-specific expression profiles of rat mammary gland, liver, and lung tissues treated with targretin, 9-cis retinoic acid, and 4- hydroxyphenylretinamide. Mol. Cancer Ther. 5, 1060-1072
69. Veeraraghavalu, K., Zhang, C., Miller, S., Hefendehl, J. K., Rajapaksha, T. W., Ulrich, J., Jucker, M., Holtzman, D. M., Tanzi, R. E., Vassar, R., and Sisodia, S. S. (2013) Comment on "ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models". Science 340, 924
70. Tesseur, I., Lo, A. C., Roberfroid, A., Dietvorst, S., Van Broeck, B., Borgers, M., Gijsen, H., Moechars, D., Mercken, M., Kemp, J., D'Hooge, R., and De Strooper, B. (2013) Comment on "ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models". Science 340, 924
71. Price, A. R., Xu, G., Siemienski, Z. B., Smithson, L. A., Borchelt, D. R., Golde, T. E., and Felsenstein, K. M. (2013) Comment on "ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models". Science 340, 924
72. Fitz, N. F., Cronican, A. A., Lefterov, I., and Koldamova, R. (2013) Comment on "ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models". Science 340, 924-c
73. LaClair, K. D., Manaye, K. F., Lee, D. L., Allard, J. S., Savonenko, A. V., Troncoso, J. C., and Wong, P. C. (2013) Treatment with bexarotene, a compound that increases apolipoprotein-E, provides no cognitive benefit in mutant APP/PS1 mice. Mol. Neurodegener. 8, 18