Daidzein augments cholesterol homeostasis via apoE to promote functional recovery in chronic stroke

Journal of Neuroscience

Volumn 35, Issue 45, 2015, Pages 15113-15126

  Kim, Eunhee ^a,b   Woo, Moon Sook ^a   Qin, Luye ^a   Ma, Thong ^a   Beltran, Cesar D ^a   Bao, Yi ^a   Bailey, Jason A ^c   Corbett, Dale ^d   Ratan, Rajiv R ^a,b   Lahiri, Debomoy K ^c   Cho, Sunghee ^a,b  

^a Burke Cornell Medical Research Institute   (United States)

^b FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

ApoE; Cholesterol transporter; Daidzein; Motor gait function; Stroke recovery

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL; DAIDZEIN; N (2,2,2 TRIFLUOROETHYL) N [4 (2,2,2 TRIFLUORO 1 HYDROXY 1 TRIFLUOROMETHYLETHYL)PHENYL]BENZENESULFONAMIDE; GROWTH INHIBITOR; ISOFLAVONE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CATWALK GAIT ANALYSIS TEST; CEREBROVASCULAR ACCIDENT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG EFFICACY; GENE EXPRESSION; HEMISPHERIC DOMINANCE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAROD TEST; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CHRONIC DISEASE; CONVALESCENCE; DEFICIENCY; DRUG EFFECTS; HOMEOSTASIS; KNOCKOUT MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; STROKE; TUMOR CELL LINE;

ANIMALS; APOLIPOPROTEINS E; CELL LINE, TUMOR; CELLS, CULTURED; CHOLESTEROL; CHRONIC DISEASE; GROWTH INHIBITORS; HOMEOSTASIS; HUMANS; ISOFLAVONES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOVERY OF FUNCTION; STROKE;

EID: 84946924502     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2890-15.2015     Document Type: Article

References (59)

1. Boehm-Cagan A, Michaelson DM (2014) Reversal of apoE4-driven brain pathology and behavioral deficits by bexarotene. J Neurosci 34:7293–7301. CrossRef Medline
2. Carmichael ST (2005) Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2:396–409. CrossRef Medline
3. Carmichael ST (2006) Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 59:735–742. CrossRef Medline
4. Chen J, Zacharek A, Cui X, Shehadah A, Jiang H, Roberts C, Lu M, Chopp M (2010) Treatment of stroke with a synthetic liver X receptor agonist, TO901317, promotes synaptic plasticity and axonal regeneration in mice. J Cereb Blood Flow Metab 30:102–109. CrossRef Medline
5. Chen S, Wang JM, Irwin RW, Yao J, Liu L, Brinton RD (2011) Allopregnanolone promotes regeneration and reduces beta-amyloid burden in a preclinical model of Alzheimer’s disease. PLoS One 6: e24293. CrossRef Medline
6. Chisholm JW, Hong J, Mills SA, LawnRM (2003) The LXR ligand T0901317 induces severe lipogenesis in the db/db diabetic mouse. J Lipid Res 44: 2039–2048. CrossRef Medline
7. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305–309. CrossRef Medline
8. Coldham NG, Sauer MJ (2000) Pharmacokinetics of [(14)C]Genistein in the rat: gender-related differences, potential mechanisms of biological action, and implications for human health. Toxicol Appl Pharmacol 164: 206–215. CrossRef Medline
9. Cramer PE, Cirrito JR, Wesson DW, Lee CY, Karlo JC, Zinn AE, Casali BT, Restivo JL, Goebel WD, James MJ, Brunden KR, Wilson DA, Landreth GE (2012) ApoE-directed therapeutics rapidly clear beta-amyloid and reverse deficits in AD mouse models. Science 335:1503–1506. CrossRef Medline
10. Cramer SC, Procaccio V (2012) Correlation between genetic polymorphisms and stroke recovery: analysis of the GAIN Americas and GAIN International Studies. Eur J Neurol 19:718–724. CrossRef Medline
11. Darling WG, Pizzimenti MA, Hynes SM, Rotella DL, Headley G, Ge J, Stilwell-Morecraft KS, McNeal DW, Solon-Cline KM, Morecraft RJ (2011) Volumetric effects of motor cortex injury on recovery of ipsilesional dexterous movements. Exp Neurol 231:56–71. CrossRef Medline
12. Gao J, Xu Y, Yang Y, Yang Y, Zheng Z, Jiang W, Hong B, Yan X, Si S (2008) Identification of upregulators of human ATP-binding cassette transporter A1 via high-throughput screening of a synthetic and natural compound library. J Biomol Screen 13:648–656. CrossRef Medline
13. Gerasimenko Y, Roy RR, Edgerton VR (2008) Epidural stimulation: comparison of the spinal circuits that generate and control locomotion in rats, cats and humans. Exp Neurol 209:417–425. CrossRef Medline
14. Gonzalez CL, Gharbawie OA, Williams PT, Kleim JA, Kolb B, Whishaw IQ (2004) Evidence for bilateral control of skilled movements: ipsilateral skilled forelimb reaching deficits and functional recovery in rats follow motor cortex and lateral frontal cortex lesions. Eur J Neurosci 20:3442–3452. CrossRef Medline
15. Grefhorst A, Elzinga BM, Voshol PJ, Plösch T, Kok T, Bloks VW, van der Sluijs FH, Havekes LM, Romijn JA, Verkade HJ, Kuipers F (2002) Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J Biol Chem 277: 34182–34190. CrossRef Medline
16. Hanson AJ, Bayer-Carter JL, Green PS, Montine TJ, Wilkinson CW, Baker LD, Watson GS, Bonner LM, Callaghan M, Leverenz JB, Tsai E, Postupna N, Zhang J, Lampe J, Craft S (2013) Effect of apolipoprotein E genotype and diet on apolipoprotein E lipidation and amyloid peptides: randomized clinical trial. JAMA Neurol 70:972–980. CrossRef Medline
17. Haskew-Layton RE, Payappilly JB, Smirnova NA, Ma TC, Chan KK, Murphy TH, Guo H, Langley B, Sultana R, Butterfield DA, Santagata S, Alldred MJ, Gazaryan IG, Bell GW, Ginsberg SD, Ratan RR (2010) Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2-independent pathway. Proc Natl Acad Sci U S A 107:17385–17390. CrossRef Medline
18. Hurtado O, Ballesteros I, Cuartero MI, Moraga A, Pradillo JM, Ramírez- Franco J, Bartolomé-Martin D, Pascual D, Torres M, Sánchez-Prieto J, Salom JB, Lizasoain I, Moro MA (2012) Daidzein has neuroprotective effects through ligand-binding-independent PPARgamma activation. Neurochem Int 61:119–127. CrossRef Medline
19. Jung JH, Kim HS (2013) The inhibitory effect of black soybean on hepatic cholesterol accumulation in high cholesterol and high fat diet-induced non-alcoholic fatty liver disease. Food Chem Toxicol 60:404–412. CrossRef Medline
20. Karten B, Campenot RB, Vance DE, Vance JE (2006) Expression of ABCG1, but not ABCA1, correlates with cholesterol release by cerebellar astroglia. J Biol Chem 281:4049–4057. CrossRef Medline
21. Kennedy MA, Venkateswaran A, Tarr PT, Xenarios I, Kudoh J, Shimizu N, Edwards PA (2001) 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 276:39438–39447. CrossRef Medline
22. Kim E, Tolhurst AT, Qin LY, Chen XY, Febbraio M, Cho S (2008) CD36/ fatty acid translocase, an inflammatory mediator, is involved in hyperlipidemia-induced exacerbation in ischemic brain injury. J Neurosci 28:4661–4670. CrossRef Medline
23. Kim E, Febbraio M, Bao Y, Tolhurst AT, Epstein JM, Cho S (2012) CD36 in the periphery and brain synergizes in stroke injury in hyperlipidemia. Ann Neurol 71:753–764. CrossRef Medline
24. Kim E, Tolhurst AT, Cho S (2014) Deregulation of inflammatory response in the diabetic condition is associated with increased ischemic brain injury. J Neuroinflamm 11:83. CrossRef Medline
25. Kim WS, Weickert CS, Garner B (2008) Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. J Neurochem 104:1145–1166. CrossRef Medline
26. King RA, Bursill DB (1998) Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy meal in humans. Am J Clin Nutr 67:867–872. Medline
27. Kratzer A, Buchebner M, Pfeifer T, Becker TM, Uray G, Miyazaki M, Miyazaki-Anzai S, Ebner B, Chandak PG, Kadam RS, Calayir E, Rathke N, Ahammer H, Radovic B, Trauner M, Hoefler G, Kompella UB, Fauler G, Levi M, Levak-Frank S, et al. (2009) Synthetic LXR agonist attenuates plaque formation in apoEice without inducing liver steatosis and hypertriglyceridemia. J Lipid Res 50:312–326.Medline
28. Langmann T, Porsch-Ozcürümez M, Heimerl S, Probst M, Moehle C, Taher M, Borsukova H, Kielar D, Kaminski WE, Dittrich-Wengenroth E, Schmitz G (2002) Identification of sterol-independent regulatory elements in the human ATP-binding cassette transporter A1 promoter: role of Sp1/3, E-box binding factors, and an oncostatin M-responsive element. J Biol Chem 277:14443–14450. CrossRef Medline
29. Lin TN, He YY, Wu G, Khan M, Hsu CY (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24: 117–121. CrossRef Medline
30. Ma TC, Campana A, Lange PS, Lee HH, Banerjee K, Bryson JB, Mahishi L, Alam S, Giger RJ, Barnes S, Morris SM Jr, Willis DE, Twiss JL, Filbin MT, Ratan RR (2010) A large-scale chemical screen for regulators of the arginase 1 promoter identifies the soy isoflavone daidzeinas a clinically approved small molecule that can promote neuronal protection or regeneration via a cAMP-independent pathway. J Neurosci 30:739–748. CrossRef Medline
31. Mahley RW, Rall SC (2000) Apolipoprotein E: far more than a lipid transport protein. Annu Rev GenomHumGenet 1:507–537. CrossRef Medline
32. Mak AC, Pullinger CR, Tang LF, Wong JS, Deo RC, Schwarz JM, Gugliucci A, Movsesyan I, Ishida BY, Chu C, Poon A, Kim P, Stock EO, Schaefer EJ, Asztalos BF, Castellano JM, Wyss-Coray T, Duncan JL, Miller BL, Kane JP, et al. (2014) Effects of the absence of apolipoprotein E on lipoproteins, neurocognitive function, and retinal function. JAMA Neurol 71: 1228–1236. CrossRef Medline
33. Maloney B, Ge YW, Alley GM, Lahiri DK (2007) Important differences between human and mouse APOE gene promoters: limitation of mouse APOE model in studying Alzheimer’s disease. J Neurochem 103: 1237–1257. CrossRef Medline
34. Maloney B, Ge YW, Petersen RC, Hardy J, Rogers JT, Perez-Tur J, Lahiri DK (2010) Functional characterization of three single-nucleotide polymorphisms present in the human APOE promoter sequence: differential effects in neuronal cells and on DNA-protein interactions. AmJ Med Genet B Neuropsychiatr Genet 153B:185–201. CrossRef Medline
35. Mandrekar-Colucci S, Landreth GE (2011) Nuclear receptors as therapeutic targets for Alzheimer’s disease. Expert Opin Ther Targets 15:1085–1097. CrossRef Medline
36. Meisel C, Prass K, Braun J, Victorov I, Wolf T, Megow D, Halle E, Volk HD, Dirnagl U, Meisel A (2004) Preventive antibacterial treatment improves the general medical and neurological outcome in a mouse model of stroke. Stroke 35:2–6. CrossRef Medline
37. Mezei O, Banz WJ, Steger RW, Peluso MR, Winters TA, Shay N (2003) Soy isoflavones exert antidiabetic and hypolipidemic effects through the PPAR pathways in obese Zucker rats and murine RAW 264.7 cells. J Nutr 133:1238–1243.Medline
38. Michikawa M, Fan QW, Isobe I, Yanagisawa K (2000) Apolipoprotein E exhibits isoform-specific promotion of lipid efflux from astrocytes and neurons in culture. J Neurochem 74:1008–1016. CrossRef Medline
39. Nudo RJ (2007) Postinfarct cortical plasticity and behavioral recovery. Stroke 38:840–845. CrossRef Medline
40. Orgaard A, Jensen L (2008) The effects of soy isoflavones on obesity. Exp Biol Med 233:1066–1080. CrossRef Medline
41. Pandian S, Arya KN (2013) Motor impairment of the ipsilesional body side in poststroke subjects. J Bodyw Mov Ther 17:495–503. CrossRef Medline
42. Pfrieger FW (2003) Outsourcing in the brain: do neurons depend on cholesterol delivery by astrocytes? Bioessays 25:72–78. CrossRef Medline
43. Qin L, Jing D, Parauda S, Carmel J, Ratan RR, Lee FS, Cho S (2014) An adaptive role for BDNF Val66Met polymorphism in motor recovery in chronic stroke. J Neurosci 34:2493–2502. CrossRef Medline
44. Rasbach KA, Schnellmann RG (2008) Isoflavones promote mitochondrial biogenesis. J Pharmacol Exp Ther 325:536–543. CrossRef Medline
45. Ricketts ML, Moore DD, Banz WJ, Mezei O, Shay NF (2005) Molecular mechanisms of action of the soy isoflavones includes activation of promiscuous nuclear receptors: a review. J Nutr Biochem 16:321–330. CrossRef Medline
46. Rivera P, Pérez-Martín M, Pavón FJ, Serrano A, Crespillo A, Cifuentes M, López-Á valos MD, Grondona JM, Vida M, FernÁndez-Llebrez P, de Fonseca FR, Suárez J (2013) Pharmacological administration of the isoflavone daidzein enhances cell proliferation and reduces high fat dietinduced apoptosis and gliosis in the rat hippocampus. PLoS One 8:e64750. CrossRef Medline
47. Schaefer SY, Haaland KY, Sainburg RL (2009) Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy. Neuropsychologia 47:2953–2966. CrossRef Medline
48. Shih SJ, Allan C, Grehan S, Tse E, Moran C, Taylor JM (2000) Duplicated downstream enhancers control expression of the human apolipoprotein E gene in macrophages and adipose tissue. J Biol Chem 275:31567–31572. CrossRef Medline
49. Soumyakrishnan S, Divya T, Kalayarasan S, Sriram N, Sudhandiran G (2014) Daidzein exhibits anti-fibrotic effect by reducing the expressions of Proteinase activated receptor 2 and TGFbeta1/smad mediated inflammation and apoptosis in Bleomycin-induced experimental pulmonary fibrosis. Biochimie 103:23–36. CrossRef Medline
50. Stout JM, Knapp AN, Banz WJ, Wallace DG, Cheatwood JL (2013) Subcutaneous daidzein administration enhances recovery of skilled ladder rung walking performance following stroke in rats. Behav Brain Res 256: 428–431. CrossRef Medline
51. Sung JH, Choi SJ, Lee SW, Park KH, Moon TW (2004) Isoflavones found in Korean soybean paste as 3-hydroxy-3-methylglutaryl Coenzyme A reductase inhibitors. Biosci Biotech Bioch 68:1051–1058. CrossRef Medline
52. Swanson LW (1995) Mapping the human brain: past, present, and future. Trends Neurosci 18:471–474. CrossRef Medline
53. Terasaka N, Hiroshima A, Koieyama T, Ubukata N, Morikawa Y, Nakai D, Inaba T (2003) T-0901317, a synthetic liver X receptor ligand, inhibits development of atherosclerosis in LDL receptor-deficient mice. FEBS Lett 536:6–11.CrossRef Medline
54. van Meer MP, van der Marel K, Wang K, Otte WM, El Bouazati S, Roeling TA, Viergever MA, Berkelbach van der Sprenkel JW, Dijkhuizen RM (2010) Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci 30:3964–3972. CrossRef Medline
55. Verghese J, Holtzer R, Wang C, Katz MJ, Barzilai N, Lipton RB (2013) Role of APOE genotype in gait decline and disability in aging. J Gerontol A Biol Sci Med Sci 68:1395–1401. CrossRef Medline
56. Wang P, Jeng CJ, Chien CL, Wang SM (2008) Signaling mechanisms of daidzein-induced axonal outgrowth in hippocampal neurons. Biochem Biophys Res Commun 366:393–400. CrossRef Medline
57. Wenzel U, Fuchs D, Daniel H (2008) Protective effects of soy-isoflavones in cardiovascular disease: identification of molecular targets. Hamostaseologie 28:85–88. Medline
58. Whitney KD, Watson MA, Collins JL, Benson WG, Stone TM, Numerick MJ, Tippin TK, Wilson JG, Winegar DA, Kliewer SA (2002) Regulation of cholesterol homeostasis by the liver X receptors in the central nervous system. Mol Endocrinol 16:1378–1385. CrossRef Medline
59. Zeiler SR, Gibson EM, Hoesch RE, Li MY, Worley PF, O’Brien RJ, Krakauer JW (2013) Medial premotor cortex shows a reduction in inhibitory markers and mediates recovery in a mouse model of focal stroke. Stroke 44:483–489. CrossRef Medline