Ferulic Acid Is a Nutraceutical β-Secretase Modulator That Improves Behavioral Impairment and Alzheimer-like Pathology in Transgenic Mice

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Mori, Takashi ^a   Koyama, Naoki ^a   Guillot Sestier, Marie Victoire ^b   Tan, Jun ^c   Town, Terrence ^b,d  

^a SAITAMA MEDICAL UNIVERSITY   (Japan)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; FERULIC ACID; OLIGOMER; PRESENILIN 1;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BEHAVIOR DISORDER; BRAIN BLOOD VESSEL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; FEMALE; HYPERACTIVITY; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATTERN RECOGNITION; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; REFERENCE MEMORY; SPATIAL DISCRIMINATION; TREATMENT DURATION; WILD TYPE; WORKING MEMORY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CEREBRAL AMYLOID ANGIOPATHY; COUMARIC ACIDS; DISEASE MODELS, ANIMAL; FEMALE; INFLAMMATION; MALE; MICE; MICE, TRANSGENIC; NEURONS; OXIDATIVE STRESS;

EID: 84873646515     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055774     Document Type: Article

References (84)

1. Brookmeyer R, Gray S, (2000) Methods for projecting the incidence and prevalence of chronic diseases in aging populations: application to Alzheimer's disease. Stat Med 19: 1481-1493.
2. Rozemuller JM, Eikelenboom P, Stam FC, Beyreuther K, Masters CL, (1989) A4 protein in Alzheimer's disease: primary and secondary cellular events in extracellular amyloid deposition. J Neuropathol Exp Neurol 48: 674-691.
3. Hardy J, Allsop D, (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12: 383-388.
4. Selkoe DJ, (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741-766.
5. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, et al. (1999) Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400: 173-177.
6. Weggen S, Eriksen JL, Das P, Sagi SA, Wang R, et al. (2001) A subset of NSAIDs lower amyloidogenic Aβ42 independently of cyclooxygenase activity. Nature 414: 212-216.
7. Tan J, Town T, Crawford F, Mori T, DelleDonne A, et al. (2002) Role of CD40 ligand in amyloidosis in transgenic Alzheimer's mice. Nat Neurosci 5: 1288-1293.
8. Kukar TL, Ladd TB, Bann MA, Fraering PC, Narlawar R, et al. (2008) Substrate-targeting γ-secretase modulators. Nature 453: 925-929.
9. Town T, Laouar Y, Pittenger C, Mori T, Szekely CA, et al. (2008) Blocking TGF-β-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat Med 14: 681-687.
10. Zhu Y, Hou H, Rezai-Zadeh K, Giunta B, Ruscin A, et al. (2011) CD45 deficiency drives amyloid-β peptide oligomers and neuronal loss in Alzheimer's disease mice. J Neurosci 31: 1355-1365.
11. Breitner J, Evans D, Lyketsos C, Martin B, Meinert C, (2007) ADAPT trial data. Am J Med 120: e3.
12. Montine TJ, Sonnen JA, Milne G, Baker LD, Breitner JC, (2010) Elevated ratio of urinary metabolites of thromboxane and prostacyclin is associated with adverse cardiovascular events in ADAPT. PLoS ONE 5: e9340.
13. Georgiou NA, Garssen J, Witkamp RF, (2011) Pharma-nutrition interface: the gap is narrowing. Eur J Pharmacol 651: 1-8.
14. Soobrattee MA, Neergheen VS, Luximon-Ramma A, Aruoma OI, Bahorun T, (2005) Phenolics as potential antioxidant therapeutic agents: mechanism and actions. Mutat Res 579: 200-213.
15. Srinivasan M, Sudheer AR, Menon VP, (2007) Ferulic acid: therapeutic potential through its antioxidant property. J Clin Biochem Nutr 40: 92-100.
16. Cheng CY, Su SY, Tang NY, Ho TY, Chiang SY, et al. (2008) Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting ICAM-1 mRNA expression in rats. Brain Res 1209: 136-150.
17. Cheng CY, Su SY, Tang NY, Ho TY, Lo WY, et al. (2010) Ferulic acid inhibits nitric oxide-induced apoptosis by enhancing GABAB1 receptor expression in transient focal cerebral ischemia in rats. Acta Pharmacol Sin 31: 889-899.
18. Koh PO, (2012) Ferulic acid prevents the cerebral ischemic injury-induced decrease of Akt and Bad phosphorylation. Neurosci Lett 507: 156-160.
19. Yabe T, Hirahara H, Harada N, Ito N, Nagai T, et al. (2010) Ferulic acid induces neural progenitor cell proliferation in vitro and in vivo. Neuroscience 165: 515-524.
20. King DL, Arendash GW, Crawford F, Sterk T, Menendez J, et al. (1999) Progressive and gender-dependent cognitive impairment in the APPSW transgenic mouse model for Alzheimer's disease. Behav Brain Res 103: 145-162.
21. Arendash GW, King DL, Gordon MN, Morgan D, Hatcher JM, et al. (2001) Progressive, age-related behavioral impairments in transgenic mice carrying both mutant amyloid precursor protein and presenilin-1 transgenes. Brain Res 891: 42-53.
22. Mori T, Rezai-Zadeh K, Koyama N, Arendash GW, Yamaguchi H, et al. (2012) Tannic acid is a natural β-secretase inhibitor that prevents cognitive impairment and mitigates Alzheimer-like pathology in transgenic mice. J Biol Chem 287: 6912-6927.
23. Kim KS, Han PL, (2006) Optimization of chronic stress paradigms using anxiety- and depression-like behavioral parameters. J Neurosci Res 83: 497-507.
24. De Rosa R, Garcia AA, Braschi C, Capsoni S, Maffei L, et al. (2005) Intranasal administration of nerve growth factor (NGF) rescues recognition memory deficits in AD11 anti-NGF transgenic mice. Proc Natl Acad Sci U S A 102: 3811-3816.
25. Morris RG, Garrud P, Rawlins JN, O'Keefe J, (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
26. Good M, Honey RC, (1997) Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning. Behav Neurosci 111: 487-493.
27. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, et al. (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19: 939-945.
28. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, et al. (2006) Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24: 516-524.
29. Mori T, Town T, Tan J, Yada N, Horikoshi Y, et al. (2006) Arundic acid ameliorates cerebral amyloidosis and gliosis in Alzheimer transgenic mice. J Pharmacol Exp Ther 318: 571-578.
30. Mori T, Koyama N, Arendash GW, Horikoshi-Sakuraba Y, Tan J, et al. (2010) Overexpression of human S100B exacerbates cerebral amyloidosis and gliosis in the Tg2576 mouse model of Alzheimer's disease. Glia 58: 300-314.
31. Ellis RJ, Olichney JM, Thal LJ, Mirra SS, Morris JC, et al. (1996) Cerebral amyloid angiopathy in the brains of patients with Alzheimer's disease: the CERAD experience, Part XV. Neurology 46: 1592-1596.
32. DeMattos RB, Bales KR, Cummins DJ, Paul SM, Holtzman DM, (2002) Brain to plasma amyloid-β efflux: a measure of brain amyloid burden in a mouse model of Alzheimer's disease. Science 295: 2264-2267.
33. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, et al. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391: 387-390.
34. Sinha S, Lieberburg I, (1999) Cellular mechanisms of β-amyloid production and secretion. Proc Natl Acad Sci U S A 96: 11049-11053.
35. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, et al. (1999) β-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741.
36. Vassar R, Kovacs DM, Yan R, Wong PC, (2009) The β-secretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J Neurosci 29: 12787-12794.
37. Yan R, Bienkowski MJ, Shuck ME, Miao H, Tory MC, et al. (1999) Membrane-anchored aspartyl protease with Alzheimer's disease β-secretase activity. Nature 402: 533-537.
38. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, et al. (2000) Inflammation and Alzheimer's disease. Neurobiol Aging 21: 383-421.
39. Yan SD, Chen X, Fu J, Chen M, Zhu H, et al. (1996) RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382: 685-691.
40. Markesbery WR, (1997) Oxidative stress hypothesis in Alzheimer's disease. Free Radic Biol Med 23: 134-147.
41. Kawabata K, Yamamoto T, Hara A, Shimizu M, Yamada Y, et al. (2000) Modifying effects of ferulic acid on azoxymethane-induced colon carcinogenesis in F344 rats. Cancer Lett 157: 15-21.
42. Balasubashini MS, Rukkumani R, Viswanathan P, Menon VP, (2004) Ferulic acid alleviates lipid peroxidation in diabetic rats. Phytother Res 18: 310-314.
43. Barnes DG, Dourson M, (1988) Reference dose (RfD): description and use in health risk assessments. Regul Toxicol Pharmacol 8: 471-486.
44. Dourson ML, Felter SP, Robinson D, (1996) Evolution of science-based uncertainty factors in noncancer risk assessment. Regul Toxicol Pharmacol 24: 108-120.
45. Zhao Z, Egashira Y, Sanada H, (2004) Ferulic acid is quickly absorbed from rat stomach as the free form and then conjugated mainly in liver. J Nutr 134: 3083-3088.
46. Sultana R, Ravagna A, Mohmmad-Abdul H, Calabrese V, Butterfield DA, (2005) Ferulic acid ethyl ester protects neurons against amyloid β-peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity. J Neurochem 92: 749-758.
47. Qin J, Chen D, Lu W, Xu H, Yan C, et al. (2008) Preparation, characterization, and evaluation of liposomal ferulic acid in vitro and in vivo. Drug Dev Ind Pharm 34: 602-608.
48. Lichtenthaler SF, Dominguez DI, Westmeyer GG, Reiss K, Haass C, et al. (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J Biol Chem 278: 48713-48719.
49. Li Q, Südhof TC, (2004) Cleavage of amyloid-β precursor protein and amyloid-β precursor-like protein by BACE 1. J Biol Chem 279: 10542-10550.
50. Pastorino L, Ikin AF, Lamprianou S, Vacaresse N, Revelli JP, et al. (2004) BACE (β-secretase) modulates the processing of APLP2 in vivo. Mol Cell Neurosci 25: 642-649.
51. von Arnim CA, Kinoshita A, Peltan ID, Tangredi MM, Herl L, et al. (2005) The low density lipoprotein receptor-related protein (LRP) is a novel β-secretase (BACE1) substrate. J Biol Chem 280: 17777-17785.
52. Wong HK, Sakurai T, Oyama F, Kaneko K, Wada K, et al. (2005) β subunits of voltage-gated sodium channels are novel substrates of β-site amyloid precursor protein-cleaving enzyme (BACE1) and γ-secretase. J Biol Chem 280: 23009-23017.
53. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S, et al. (2006) Control of peripheral nerve myelination by the β-secretase BACE1. Science 314: 664-666.
54. Hu X, He W, Diaconu C, Tang X, Kidd GJ, et al. (2008) Genetic deletion of BACE1 in mice affects remyelination of sciatic nerves. FASEB J 22: 2970-2980.
55. Gandhi S, Refolo LM, Sambamurti K, (2004) Amyloid precursor protein compartmentalization restricts β-amyloid production. Therapeutic targets based on BACE compartmentalization. J Mol Neurosci 24: 137-143.
56. Rezai-Zadeh K, Shytle D, Sun N, Mori T, Hou H, et al. (2005) Green tea epigallocatechin-3-gallate (EGCG) modulates amyloid precursor protein cleavage and reduces cerebral amyloidosis in Alzheimer transgenic mice. J Neurosci 25: 8807-8814.
57. Obregon DF, Rezai-Zadeh K, Bai Y, Sun N, Hou H, et al. (2006) ADAM10 activation is required for green tea (-)-epigallocatechin-3-gallate-induced α-secretase cleavage of amyloid precursor protein. J Biol Chem 281: 16419-16427.
58. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, et al. (2002) Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539.
59. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, et al. (2005) Natural oligomers of the amyloid-β protein specifically disrupt cognitive function. Nat Neurosci 8: 79-84.
60. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, et al. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842.
61. Holcomb LA, Gordon MN, Jantzen P, Hsiao K, Duff K, et al. (1999) Behavioral changes in transgenic mice expressing both amyloid precursor protein and presenilin-1 mutations: lack of association with amyloid deposits. Behav Genet 29: 177-185.
62. Westerman MA, Cooper-Blacketer D, Mariash A, Kotilinek L, Kawarabayashi T, et al. (2002) The relationship between Aβ and memory in the Tg2576 mouse model of Alzheimer's disease. J Neurosci 22: 1858-1867.
63. Kotilinek LA, Bacskai B, Westerman M, Kawarabayashi T, Younkin L, et al. (2002) Reversible memory loss in a mouse transgenic model of Alzheimer's disease. J Neurosci 22: 6331-6335.
64. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, et al. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440: 352-357.
65. Mouri A, Noda Y, Hara H, Mizoguchi H, Tabira T, et al. (2007) Oral vaccination with a viral vector containing Aβ cDNA attenuates age-related Aβ accumulation and memory deficits without causing inflammation in a mouse Alzheimer model. FASEB J 21: 2135-2148.
66. Oddo S, Vasilevko V, Caccamo A, Kitazawa M, Cribbs DH, et al. (2006) Reduction of soluble Aβ and tau, but not soluble Aβ alone, ameliorates cognitive decline in transgenic mice with plaques and tangles. J Biol Chem 281: 39413-39423.
67. McGeer PL, Itagaki S, Tago H, McGeer EG, (1987) Reactive microglia in patients with senile dementia of the Alzheimer type are positive for the histocompatibility glycoprotein HLA-DR. Neurosci Lett 79: 195-200.
68. Benzing WC, Wujek JR, Ward EK, Shaffer D, Ashe KH, et al. (1999) Evidence for glial-mediated inflammation in aged APPSW transgenic mice. Neurobiol Aging 20: 581-589.
69. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, et al. (1999) Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 154: 1673-1684.
70. Lim GP, Yang F, Chu T, Chen P, Beech W, et al. (2000) Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 20: 5709-5714.
71. Pappolla MA, Chyan YJ, Omar RA, Hsiao K, Perry G, et al. (1998) Evidence of oxidative stress and in vivo neurotoxicity of β-amyloid in a transgenic mouse model of Alzheimer's disease. A chronic oxidative paradigm for testing antioxidant therapies in vivo. Am J Pathol 152: 871-877.
72. Goldsbury C, Whiteman IT, Jeong EV, Lim YA, (2008) Oxidative stress increases levels of endogenous amyloid-β peptides secreted from primary chick brain neurons. Aging Cell 7: 771-775.
73. Kanski J, Aksenova M, Stoyanova A, Butterfield DA, (2002) Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell culture systems in vitro: structure-activity studies. J Nutr Biochem 13: 273-281.
74. Jankowsky JL, Slunt HH, Gonzales V, Jenkins NA, Copeland NG, et al. (2004) APP processing and amyloid deposition in mice haplo-insufficient for presenilin 1. Neurobiol Aging 25: 885-892.
75. Laghmouch A, Bertholet JY, Crusio WE, (1997) Hippocampal morphology and open-field behavior in Mus musculus domesticus and Mus spretus inbred mice. Behav Genet 27: 67-73.
76. Franklin KBJ, Paxinos G (2001) The Mouse Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA.
77. Thinakaran G, Teplow DB, Siman R, Greenberg B, Sisodia SS, (1996) Metabolism of the "Swedish" amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the "β-secretase" site occurs in the golgi apparatus. J Biol Chem 271: 9390-9397.
78. Rezai-Zadeh K, Douglas Shytle R, Bai Y, Tian J, Hou H, et al. (2009) Flavonoid-mediated presenilin-1 phosphorylation reduces Alzheimer's disease β-amyloid production. J Cell Mol Med 13: 574-588.
79. Tan J, Town T, Mori T, Wu Y, Saxe M, et al. (2000) CD45 opposes β-amyloid peptide-induced microglial activation via inhibition of p44/42 mitogen-activated protein kinase. J Neurosci 20: 7587-7594.
80. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, et al. (2001) Age-dependent changes in brain, CSF, and plasma amyloid β protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21: 372-381.
81. Jankowsky JL, Slunt HH, Gonzales V, Savonenko AV, Wen JC, et al. (2005) Persistent amyloidosis following suppression of Aβ production in a transgenic model of Alzheimer disease. PLoS Med 2: e355.
82. Horikoshi Y, Sakaguchi G, Becker AG, Gray AJ, Duff K, et al. (2004) Development of Aβ terminal end-specific antibodies and sensitive ELISA for Aβ variant. Biochem Biophys Res Commun 319: 733-737.
83. Xia W, Yang T, Shankar G, Smith IM, Shen Y, et al. (2009) A specific enzyme-linked immunosorbent assay for measuring β-amyloid protein oligomers in human plasma and brain tissue of patients with Alzheimer disease. Arch Neurol 66: 190-199.
84. Monney L, Sabatos CA, Gaglia JL, Ryu A, Waldner H, et al. (2002) Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415: 536-541.