Oleocanthal Enhances Amyloid-β Clearance from the Brains of TgSwDI Mice and in Vitro across a Human Blood-Brain Barrier Model

ACS Chemical Neuroscience

Volumn 6, Issue 11, 2015, Pages 1849-1859

  Qosa, Hisham ^a   Batarseh, Yazan S ^a   Mohyeldin, Mohamed M ^a   El Sayed, Khalid A ^a   Keller, Jeffrey N ^b   Kaddoumi, Amal ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Alzheimer's diseases; amyloid ; blood brain barrier; clearance; oleocanthal

Indexed keywords

AMYLOID BETA PROTEIN; EXTRA VIRGIN OLIVE OIL; INTERLEUKIN 1BETA; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MULTIDRUG RESISTANCE PROTEIN; OLEOCANTHAL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOID X RECEPTOR; SECOIRIDOID; TAU PROTEIN; TUBULIN; UNCLASSIFIED DRUG; ABC TRANSPORTER A1; ABCA1 PROTEIN, MOUSE; ALDEHYDE; APOLIPOPROTEIN E; MAPT PROTEIN, MOUSE; NEUROPROTECTIVE AGENT; PHENOL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN; CONTROLLED STUDY; ENTORHINAL CORTEX; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; THIN LAYER CHROMATOGRAPHY; WILD TYPE MOUSE; ALZHEIMER DISEASE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; MALE; METABOLISM; PHOSPHORYLATION; TRANSGENIC MOUSE;

ALDEHYDES; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEINS E; ASTROCYTES; ATP BINDING CASSETTE TRANSPORTER 1; BLOOD-BRAIN BARRIER; BRAIN; DISEASE MODELS, ANIMAL; MALE; MICE, TRANSGENIC; NEUROPROTECTIVE AGENTS; PHENOLS; PHOSPHORYLATION; PPAR GAMMA; TAU PROTEINS;

EID: 84947731754     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.5b00190     Document Type: Article

References (61)

1. Salvini, S., Sera, F., Caruso, D., Giovannelli, L., Visioli, F., Saieva, C., Masala, G., Ceroti, M., Giovacchini, V., Pitozzi, V., Galli, C., Romani, A., Mulinacci, N., Bortolomeazzi, R., Dolara, P., and Palli, D. (2006) Daily consumption of a high-phenol extra-virgin olive oil reduces oxidative DNA damage in postmenopausal women Br. J. Nutr. 95, 742-751 10.1079/BJN20051674
2. Filik, L. and Ozyilkan, O. (2003) Olive-oil consumption and cancer risk Eur. J. Clin. Nutr. 57, 191 10.1038/sj.ejcn.1601497
3. Scarmeas, N., Stern, Y., Mayeux, R., and Luchsinger, J. A. (2006) Mediterranean diet, Alzheimer disease, and vascular mediation Arch. Neurol. 63, 1709-1717 10.1001/archneur.63.12.noc60109
4. Valls-Pedret, C., Sala-Vila, A., Serra-Mir, M., Corella, D., de la Torre, R., Martinez-Gonzalez, M. A., Martinez-Lapiscina, E. H., Fito, M., Perez-Heras, A., Salas-Salvado, J., Estruch, R., and Ros, E. (2015) Mediterranean Diet and Age-Related Cognitive Decline: A Randomized Clinical Trial JAMA Intern Med. 175, 1094 10.1001/jamainternmed.2015.1668
5. Tuck, K. L. and Hayball, P. J. (2002) Major phenolic compounds in olive oil: metabolism and health effects J. Nutr. Biochem. 13, 636-644 10.1016/S0955-2863(02)00229-2
6. Shubair, M. M., McColl, R. S., and Hanning, R. M. (2005) Mediterranean dietary components and body mass index in adults: the peel nutrition and heart health survey Chronic Dis. Can. 26, 43-51
7. Corona, G., Spencer, J. P., and Dessi, M. A. (2009) Extra virgin olive oil phenolics: absorption, metabolism, and biological activities in the GI tract Toxicol. Ind. Health 25, 285-293 10.1177/0748233709102951
8. Scarmeas, N., Stern, Y., Mayeux, R., Manly, J. J., Schupf, N., and Luchsinger, J. A. (2009) Mediterranean diet and mild cognitive impairment Arch. Neurol. 66, 216-225 10.1001/archneurol.2008.536
9. Scarmeas, N., Stern, Y., Tang, M. X., Mayeux, R., and Luchsinger, J. A. (2006) Mediterranean diet and risk for Alzheimer's disease Ann. Neurol. 59, 912-921 10.1002/ana.20854
10. Tripoli, E., Giammanco, M., Tabacchi, G., Di Majo, D., Giammanco, S., and La Guardia, M. (2005) The phenolic compounds of olive oil: structure, biological activity and beneficial effects on human health Nutr. Res. Rev. 18, 98-112 10.1079/NRR200495
11. Aguilera, C. M., Mesa, M. D., Ramirez-Tortosa, M. C., Nestares, M. T., Ros, E., and Gil, A. (2004) Sunflower oil does not protect against LDL oxidation as virgin olive oil does in patients with peripheral vascular disease Clin. Nutr. 23, 673-681 10.1016/j.clnu.2003.11.005
12. Cicerale, S., Lucas, L., and Keast, R. (2010) Biological activities of phenolic compounds present in virgin olive oil Int. J. Mol. Sci. 11, 458-479 10.3390/ijms11020458
13. Lopez, S., Bermudez, B., Montserrat-de la Paz, S., Jaramillo, S., Varela, L. M., Ortega-Gomez, A., Abia, R., and Muriana, F. J. (2014) Membrane composition and dynamics: a target of bioactive virgin olive oil constituents Biochim. Biophys. Acta, Biomembr. 1838, 1638-1656 10.1016/j.bbamem.2014.01.007
14. Vissers, M. N., Zock, P. L., and Katan, M. B. (2004) Bioavailability and antioxidant effects of olive oil phenols in humans: a review Eur. J. Clin. Nutr. 58, 955-965 10.1038/sj.ejcn.1601917
15. Beauchamp, G. K., Keast, R. S., Morel, D., Lin, J., Pika, J., Han, Q., Lee, C. H., Smith, A. B., and Breslin, P. A. (2005) Phytochemistry: ibuprofen-like activity in extra-virgin olive oil Nature 437, 45-46 10.1038/437045a
16. Abuznait, A. H., Qosa, H., Busnena, B. A., El Sayed, K. A., and Kaddoumi, A. (2013) Olive-oil-derived oleocanthal enhances beta-amyloid clearance as a potential neuroprotective mechanism against Alzheimer's disease: in vitro and in vivo studies ACS Chem. Neurosci. 4, 973-982 10.1021/cn400024q
17. Farr, S. A., Price, T. O., Dominguez, L. J., Motisi, A., Saiano, F., Niehoff, M. L., Morley, J. E., Banks, W. A., Ercal, N., and Barbagallo, M. (2012) Extra virgin olive oil improves learning and memory in SAMP8 mice J. Alzheimer's Dis 28, 81-92
18. Grossi, C., Rigacci, S., Ambrosini, S., Ed Dami, T., Luccarini, I., Traini, C., Failli, P., Berti, A., Casamenti, F., and Stefani, M. (2013) The polyphenol oleuropein aglycone protects TgCRND8 mice against Ass plaque pathology PLoS One 8, e71702 10.1371/journal.pone.0071702
19. Luccarini, I., Ed Dami, T., Grossi, C., Rigacci, S., Stefani, M., and Casamenti, F. (2014) Oleuropein aglycone counteracts Abeta42 toxicity in the rat brain Neurosci. Lett. 558, 67-72 10.1016/j.neulet.2013.10.062
20. Pitozzi, V., Jacomelli, M., Zaid, M., Luceri, C., Bigagli, E., Lodovici, M., Ghelardini, C., Vivoli, E., Norcini, M., Gianfriddo, M., Esposto, S., Servili, M., Morozzi, G., Baldi, E., Bucherelli, C., Dolara, P., and Giovannelli, L. (2010) Effects of dietary extra-virgin olive oil on behaviour and brain biochemical parameters in ageing rats Br. J. Nutr. 103, 1674-1683 10.1017/S0007114509993655
21. Monti, M. C., Margarucci, L., Tosco, A., Riccio, R., and Casapullo, A. (2011) New insights on the interaction mechanism between tau protein and oleocanthal, an extra-virgin olive-oil bioactive component Food Funct. 2, 423-428 10.1039/c1fo10064e
22. Pitt, J., Roth, W., Lacor, P., Smith, A. B., 3rd, Blankenship, M., Velasco, P., De Felice, F., Breslin, P., and Klein, W. L. (2009) Alzheimer's-associated Abeta oligomers show altered structure, immunoreactivity and synaptotoxicity with low doses of oleocanthal Toxicol. Appl. Pharmacol. 240, 189-197 10.1016/j.taap.2009.07.018
23. Selkoe, D. J. (2001) Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81, 741-766
24. Gu, Y., Luchsinger, J. A., Stern, Y., and Scarmeas, N. (2010) Mediterranean diet, inflammatory and metabolic biomarkers, and risk of Alzheimer's disease J. Alzheimers Dis 22, 483-492 10.3233/JAD-2010-100897
25. Gardener, S., Gu, Y., Rainey-Smith, S. R., Keogh, J. B., Clifton, P. M., Mathieson, S. L., Taddei, K., Mondal, A., Ward, V. K., Scarmeas, N., Barnes, M., Ellis, K. A., Head, R., Masters, C. L., Ames, D., Macaulay, S. L., Rowe, C. C., Szoeke, C., and Martins, R. N. (2012) Adherence to a Mediterranean diet and Alzheimer's disease risk in an Australian population Transl. Psychiatry 2, e164 10.1038/tp.2012.91
26. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112 10.1038/nrm2101
27. Reilly, J. F., Games, D., Rydel, R. E., Freedman, S., Schenk, D., Young, W. G., Morrison, J. H., and Bloom, F. E. (2003) Amyloid deposition in the hippocampus and entorhinal cortex: quantitative analysis of a transgenic mouse model Proc. Natl. Acad. Sci. U. S. A. 100, 4837-4842 10.1073/pnas.0330745100
28. Davis, J., Xu, F., Deane, R., Romanov, G., Previti, M. L., Zeigler, K., Zlokovic, B. V., and Van Nostrand, W. E. (2004) Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor J. Biol. Chem. 279, 20296-20306 10.1074/jbc.M312946200
29. Zhang-Nunes, S. X., Maat-Schieman, M. L., van Duinen, S. G., Roos, R. A., Frosch, M. P., and Greenberg, S. M. (2006) The cerebral beta-amyloid angiopathies: hereditary and sporadic Brain Pathol. 16, 30-39 10.1111/j.1750-3639.2006.tb00559.x
30. Haass, C. (2004) Take five - BACE and the gamma-secretase quartet conduct Alzheimer's amyloid beta-peptide generation EMBO J. 23, 483-488 10.1038/sj.emboj.7600061
31. Selkoe, D. J. (1993) Physiological production of the beta-amyloid protein and the mechanism of Alzheimer's disease Trends Neurosci. 16, 403-409 10.1016/0166-2236(93)90008-A
32. Sisodia, S. S., Koo, E. H., Beyreuther, K., Unterbeck, A., and Price, D. L. (1990) Evidence that beta-amyloid protein in Alzheimer's disease is not derived by normal processing Science 248, 492-495 10.1126/science.1691865
33. Bell, R. D. and Zlokovic, B. V. (2009) Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease Acta Neuropathol. 118, 103-113 10.1007/s00401-009-0522-3
34. Deane, R., Wu, Z., Sagare, A., Davis, J., Du Yan, S., Hamm, K., Xu, F., Parisi, M., LaRue, B., Hu, H. W., Spijkers, P., Guo, H., Song, X., Lenting, P. J., Van Nostrand, W. E., and Zlokovic, B. V. (2004) LRP/amyloid beta-peptide interaction mediates differential brain efflux of Abeta isoforms Neuron 43, 333-344 10.1016/j.neuron.2004.07.017
35. Wang, Y. J., Zhou, H. D., and Zhou, X. F. (2006) Clearance of amyloid-beta in Alzheimer's disease: progress, problems and perspectives Drug Discovery Today 11, 931-938 10.1016/j.drudis.2006.08.004
36. Qosa, H., Abuasal, B. S., Romero, I. A., Weksler, B., Couraud, P. O., Keller, J. N., and Kaddoumi, A. (2014) Differences in amyloid-beta clearance across mouse and human blood-brain barrier models: Kinetic analysis and mechanistic modeling Neuropharmacology 79C, 668-678 10.1016/j.neuropharm.2014.01.023
37. Cirrito, J. R., Deane, R., Fagan, A. M., Spinner, M. L., Parsadanian, M., Finn, M. B., Jiang, H., Prior, J. L., Sagare, A., Bales, K. R., Paul, S. M., Zlokovic, B. V., Piwnica-Worms, D., and Holtzman, D. M. (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 10.1172/JCI25247
38. Shibata, M., Yamada, S., Kumar, S. R., Calero, M., Bading, J., Frangione, B., Holtzman, D. M., Miller, C. A., Strickland, D. K., Ghiso, J., and Zlokovic, B. V. (2000) Clearance of Alzheimer's amyloid-beta(1-40) peptide from brain by LDL receptor-related protein-1 at the blood-brain barrier J. Clin. Invest. 106, 1489-1499 10.1172/JCI10498
39. Qosa, H., Abuznait, A. H., Hill, R. A., and Kaddoumi, A. (2012) Enhanced brain amyloid-beta clearance by rifampicin and caffeine as a possible protective mechanism against Alzheimer's disease J. Alzheimers Dis 31, 151-165 10.3233/JAD-2012-120319
40. Kline, A. (2012) Apolipoprotein E, amyloid-ss clearance and therapeutic opportunities in Alzheimer's disease Alzheimer's Res. Ther. 4, 32 10.1186/alzrt135
41. Wildsmith, K. R., Holley, M., Savage, J. C., Skerrett, R., and Landreth, G. E. (2013) Evidence for impaired amyloid beta clearance in Alzheimer's disease Alzheimer's Res. Ther. 5, 33 10.1186/alzrt187
42. Chawla, A., Boisvert, W. A., Lee, C. H., Laffitte, B. A., Barak, Y., Joseph, S. B., Liao, D., Nagy, L., Edwards, P. A., Curtiss, L. K., Evans, R. M., and Tontonoz, P. (2001) A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis Mol. Cell 7, 161-171 10.1016/S1097-2765(01)00164-2
43. Zolezzi, J. M., Bastias-Candia, S., Santos, M. J., and Inestrosa, N. C. (2014) Alzheimer's disease: relevant molecular and physiopathological events affecting amyloid-beta brain balance and the putative role of PPARs Front. Aging Neurosci. 6, 176 10.3389/fnagi.2014.00176
44. 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 beta-amyloid and reverse deficits in AD mouse models Science 335, 1503-1506 10.1126/science.1217697
45. Kim, H. J., Moon, J. H., Kim, H. M., Yun, M. R., Jeon, B. H., Lee, B., Kang, E. S., Lee, H. C., and Cha, B. S. (2014) The hypolipidemic effect of cilostazol can be mediated by regulation of hepatic low-density lipoprotein receptor-related protein 1 (LRP1) expression Metab., Clin. Exp. 63, 112-119 10.1016/j.metabol.2013.09.006
46. Rocejanasaroj, A., Tencomnao, T., and Sangkitikomol, W. (2014) Thunbergia laurifolia extract minimizes the adverse effects of toxicants by regulating P-glycoprotein activity, CYP450, and lipid metabolism gene expression in HepG2 cells GMR, Genet. Mol. Res. 13, 205-219 10.4238/2014.January.10.12
47. Lefebvre, P., Benomar, Y., and Staels, B. (2010) Retinoid X receptors: common heterodimerization partners with distinct functions Trends Endocrinol. Metab. 21, 676-683 10.1016/j.tem.2010.06.009
48. Iqbal, K., Liu, F., Gong, C. X., Alonso, A. C., and Grundke-Iqbal, I. (2009) Mechanisms of tau-induced neurodegeneration Acta Neuropathol. 118, 53-69 10.1007/s00401-009-0486-3
49. Alonso, A. D., Di Clerico, J., Li, B., Corbo, C. P., Alaniz, M. E., Grundke-Iqbal, I., and Iqbal, K. (2010) Phosphorylation of tau at Thr212, Thr231, and Ser262 combined causes neurodegeneration J. Biol. Chem. 285, 30851-30860 10.1074/jbc.M110.110957
50. Oddo, S., Billings, L., Kesslak, J. P., Cribbs, D. H., and LaFerla, F. M. (2004) Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome Neuron 43, 321-332 10.1016/j.neuron.2004.07.003
51. Sofroniew, M. V. (2015) Astrogliosis Cold Spring Harbor Perspect. Biol. 7, a020420 10.1101/cshperspect.a020420
52. Verkhratsky, A., Rodríguez, J. J., and Steardo, L. (2014) Astrogliopathology: a central element of neuropsychiatric diseases? Neuroscientist 20, 576-588 10.1177/1073858413510208
53. Heppner, F. L., Ransohoff, R. M., and Becher, B. (2015) Immune attack: the role of inflammation in Alzheimer disease Nat. Rev. Neurosci. 16, 358-372 10.1038/nrn3880
54. Tong, L., Balazs, R., Soiampornkul, R., Thangnipon, W., and Cotman, C. W. (2008) Interleukin-1 beta impairs brain derived neurotrophic factor-induced signal transduction Neurobiol. Aging 29, 1380-1393 10.1016/j.neurobiolaging.2007.02.027
55. Fuller, S., Steele, M., and Münch, G. (2010) Activated astroglia during chronic inflammation in Alzheimer's disease-do they neglect their neurosupportive roles? Mutat. Res., Fundam. Mol. Mech. Mutagen. 690, 40-49 10.1016/j.mrfmmm.2009.08.016
56. Brahmachari, S., Fung, Y. K., and Pahan, K. (2006) Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide J. Neurosci. 26, 4930-4939 10.1523/JNEUROSCI.5480-05.2006
57. Iacono, A., Gómez, R., Sperry, J., Conde, J., Bianco, G., Meli, R., Gómez-Reino, J. J., Smith, A. B., 3rd, and Gualillo, O. (2010) Effect of oleocanthal and its derivatives on inflammatory response induced by lipopolysaccharide in a murine chondrocyte cell line Arthritis Rheum. 62, 1675-1682 10.1002/art.27437
58. Elnagar, A. Y., Sylvester, P. W., and El Sayed, K. A. (2011) -)-Oleocanthal as a c-Met inhibitor for the control of metastatic breast and prostate cancers Planta Med. 77, 1013-1019 10.1055/s-0030-1270724
59. Ly, P. T., Cai, F., and Song, W. (2011) Detection of neuritic plaques in Alzheimer's disease mouse model J. Visualized Exp. 53, e2831 10.3791/2831
60. Zinchuk, V., Zinchuk, O., and Okada, T. (2007) Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena Acta Histochem. Cytochem. 40, 101-111 10.1267/ahc.07002
61. Pacheco-Quinto, J. and Eckman, E. A. (2013) Endothelin-converting enzymes degrade intracellular beta-amyloid produced within the endosomal/lysosomal pathway and autophagosomes J. Biol. Chem. 288, 5606-5615 10.1074/jbc.M112.422964