Anti-neuroinflammatory effects of a food-grade phenolic-enriched maple syrup extract in a mouse model of Alzheimer’s disease

References

• Walters A, Phillips E, Zheng R, Biju M, Kuruvilla T. Evidence for neuroinflammation in Alzheimer ‘s disease. Prog Neurol Psychiatry. 2016;20:25–31. doi: 10.1002/pnp.444
   Google Scholar
• Heppner FL, Ransohoff RM, Becher B. Immune attack: The role of inflammation in Alzheimer disease. Nat Rev Neurosci. 2015;16:358–72. doi: 10.1038/nrn3880
   PubMed Web of Science ®Google Scholar
• Keren-Shaul H, Spinrad A, Weiner A, Matcovitch-Natan O, Dvit-Szternfeld R, Ulland TK, et al. A Unique microglia type associated with restricting development of Alzheimer’s disease. Cell. 2017;7:1276–90. doi: 10.1016/j.cell.2017.05.018
   Google Scholar
• Krasemann S, Madore C, Cialic R, Baufeld C, Calcagno N, El Fatimy R, et al. The TREM2-APOE pathway drives the rranscriptional phenotype of dysfunctional microglia in neurodegenerative diseases. Immunity. 2017;47:566–81. doi: 10.1016/j.immuni.2017.08.008
   PubMed Web of Science ®Google Scholar
• Breitner J, Baker L, Drye L, Evans D, Lyketsos C, Ryan L, et al. Results of a follow-up study to the randomized Alzheimer’s disease anti-inflammatory prevention trial (ADAPT). Alzheimer’s Dement. 2013;9:714–23. doi: 10.1016/j.jalz.2012.11.012
   PubMed Web of Science ®Google Scholar
• Miller MG, Thangthaeng N, Poulose SM, Shukitt-Hale B. Role of fruits, nuts, and vegetables in maintaining cognitive health. Ecp. Gerontol. 2017;96:24–28.
   Google Scholar
• Mendes D, Oliveria MM, Moreira PI, Coutinho J, Nunes FM, Pereira DM, et al. Beneficial effects of white wine polyphenols-enriched diet on Alzheimer’s disease-like pathology. J Nutr Biochem. 2018;55:165–77. doi: 10.1016/j.jnutbio.2018.02.001
   PubMed Web of Science ®Google Scholar
• Dal-Pan A, Dudonne S, Bourassa P, Bourdoulous M, Tremblay C, Desjardins Y, et al. Cognitive-enhancing effects of a polyphenols-rich extract from fruits without changes in neuropathology in an animal model of Alzheimer’s disease. J Alzheimer’s Dis. 2017;55:115–35. doi: 10.3233/JAD-160281
   PubMed Web of Science ®Google Scholar
• Hutton CP, Lemon JA, Sakic B, Rollo CD, Boreham DR, Fahenstock M, et al. Early intervention with a multi-ingredient dietary supplement improves mood and spatial memory in a triple transgenic mouse model of Alzheimer's disease. J Alzheimers Dis. 2018;64:835–57. doi: 10.3233/JAD-170921
   PubMed Web of Science ®Google Scholar
• Liu Y, Rose KN, DaSilva NA, Johnson SL, Seeram NP. Isolation, identification, and biological evaluation of phenolic compounds from a traditional north American confectionery, maple sugar. J Agric Food Chem. 2017;65:4289–95. doi: 10.1021/acs.jafc.7b01969
   PubMed Web of Science ®Google Scholar
• Zhang Y, Yuan T, Li L, Nahar P, Slitt A, Seeram NP. Chemical compositional, biological, and safety studies of a novel maple syrup derived extract for nutraceutical applications. J Agric Food Chem. 2014;62:6687–98. doi: 10.1021/jf501924y
   PubMed Web of Science ®Google Scholar
• Li L, Seeram NP. Further investigation into maple syrup yields 3 new lignans, a new phenylpropanoid, and 26 other Phytochemicals. J Agric Food Chem. 2011;59:7708–16. doi: 10.1021/jf2011613
   PubMed Web of Science ®Google Scholar
• Li L, Seeram NP. Maple syrup phytochemicals include lignans, coumarins, a stilbene, and other previously unreported phenolic compounds. J Agric Food Chem. 2010;58:11673–9. doi: 10.1021/jf1033398
   PubMed Web of Science ®Google Scholar
• Li L, Seeram NP. Quebecol, a novel phenolic compound isolated from Canadian maple syrup. J Funct Foods. 2011;3:125–8. doi: 10.1016/j.jff.2011.02.004
   Web of Science ®Google Scholar
• Yuan T, Li L, Zhang Y, Seeram NP. Pasteurized and sterilized maple sap as a functional beverage: chemical composition and antioxidant activites. J Funct Foods. 2013;5:1582–90. doi: 10.1016/j.jff.2013.06.009
   Web of Science ®Google Scholar
• Hawco CL, Wang Y, Taylor M, Weaver DF. A maple syrup extract prevents β-amyloid aggregation. Can J Neurol Sci. 2016;43:198–201. doi: 10.1017/cjn.2015.270
   PubMed Web of Science ®Google Scholar
• Ma H, DaSilva NA, Liu W, Nahar PP, Wei Z, Liu Y, et al. Effects of a standardized phenolic-enriched maple syrup extract on β-amyloid aggregation, neuroinflammation in microglial and neuronal cells, and β-amyloid induced neurotoxicity in Caenorhabditis elegans. Neurochem Res. 2016;41:2836–47. doi: 10.1007/s11064-016-1998-6
   PubMed Web of Science ®Google Scholar
• Yang JT, Wang ZJ, Cai HY, Hu MM, Wu MN, Qi JS. Sex differences in neuropathology and cognitive behavior in APP/PS1/tau triple-transgenic mouse model of Alzheimer's disease. Neurosci Bull. 2018;5:736–46. doi: 10.1007/s12264-018-0268-9
   Google Scholar
• Nair A, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7:27–31. doi: 10.4103/0976-0105.177703
   PubMedGoogle Scholar
• Jamwal R, Barlock BJ, Adusumalli S, Ogasawara K, Simons BL, Akhlaghi F. A multiplex and label-free relative quantification approach for studying protein abundance of drug metabolizing enzymes in human liver microsomes using SWATH-MS. J Proteome Res. 2017;16:4134–43. doi: 10.1021/acs.jproteome.7b00505
   PubMed Web of Science ®Google Scholar
• Amor S, Peferoen LA, Vogel DY, Breur M, Van Der Valk P, Baker D, et al. Inflammation in neurodegenerative diseases - an update. Immunology. 2014;142:151–66. doi: 10.1111/imm.12233
   PubMed Web of Science ®Google Scholar
• Heneka MT, Carson MJ, El Khoury J, Landreth GE, Brosseron F, Feinstein DL, et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 2015;14:388–405. doi: 10.1016/S1474-4422(15)70016-5
   PubMed Web of Science ®Google Scholar
• Walker DG, Lue LF, Beach TG. Gene expression profiling of amyloid beta peptide-stimulated human post-mortem brain microglia. Neurobiol Aging. 2001;22:957–66. doi: 10.1016/S0197-4580(01)00306-2
   PubMed Web of Science ®Google Scholar
• Hollingworth P, Harold D, Sims R, Gerrish A, Lambert JC, Carrasquillo MM, et al. Common variants at ABCA7, MS4A6A/MS4A4E, EPHA1, CD33 and CD2AP are associated with Alzheimer’s disease. Nat Genet. 2011;43:429–36. doi: 10.1038/ng.803
   PubMed Web of Science ®Google Scholar
• Liebert MA, Wen X, Lee JM, Seilhamer J, Somogyi R. A gene expression profile of Alzheimer ‘ s disease. DNA Cell Biol. 2001;20:683–95. doi: 10.1089/10445490152717541
   PubMed Web of Science ®Google Scholar
• Bradshaw EM, Chibnik LB, Keenan BT, Ottoboni L, Raj T, Tang A, et al. CD33 Alzheimer’s disease locus: altered monocyte function and amyloid biology. Nat Neurosci. 2014;16:848–50. doi: 10.1038/nn.3435
   Web of Science ®Google Scholar
• Rothman SM, Tanis KQ, Gandhi P, Malkov V, Marcus J, Pearson M, et al. Human Alzheimer’s disease gene expression signatures and immune profile in APP mouse models: A discrete transcriptomic view of Aβ plaque pathology. J Neuroinflamm. 2018;15. doi:10.1186/s12974-018-1265-7.
   PubMed Web of Science ®Google Scholar
• Zotova E, Nicoll JA, Kalaria R, Holmes C, Boche D. Inflammation in Alzheimer’s disease: relevance to pathogenesis and therapy. Alzheimers Res Ther. 2010;2. doi:10.1186/alzrt24.
   PubMed Web of Science ®Google Scholar
• Rao JS, Kellom M, Kim HW, Rapoport SI, Reese EA. Neuroinflammation and synaptic loss. Neurochem Res. 2012;37:903–10. doi: 10.1007/s11064-012-0708-2
   PubMed Web of Science ®Google Scholar
• Seo EJ, Pischer N, Efferth T. Phytochemicals as inhibitors of NF-kB for treatment of Alzheimer's disease. Pharmacol Res. 2018;129:262–73. doi: 10.1016/j.phrs.2017.11.030
   PubMed Web of Science ®Google Scholar
• Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Aβ and synaptic dysfunction. Neuron. 2003;39:409–21. doi: 10.1016/S0896-6273(03)00434-3
   PubMed Web of Science ®Google Scholar
• Montine TJ, Neely MD, Quinn JF, Beal MF, Markesbery WR, Roberts LJ, et al. Lipid peroxidation in aging brain and Alzheimer’s disease. Free Radic Biol Med. 2002;33:620–6. doi: 10.1016/S0891-5849(02)00807-9
   PubMed Web of Science ®Google Scholar
• Bradley-Whitman MA, Lovell MA. Biomarkers of lipid peroxidation in Alzheimer disease (AD): an update. Arch Toxicol. 2015;89:1035–44. doi: 10.1007/s00204-015-1517-6
   PubMed Web of Science ®Google Scholar
• Olmos-Alonso A, Schetters ST, Sri S, Askew K, Mancuso R, Cargas-Caballero M, et al. Pharmacological targeting of CSF1R inhibits microglial proliferation and prevents the progression of Alzheimer’s-like pathology. Brain. 2016;139:891–907. doi: 10.1093/brain/awv379
   PubMed Web of Science ®Google Scholar
• Šerý O, Janoutova J, Ewerlingova L, Halova A, Lochman J, Janout V, et al. CD36 gene polymorphism is associated with Alzheimer’s disease. Biochimie. 2017;135:46–53. doi: 10.1016/j.biochi.2017.01.009
   PubMed Web of Science ®Google Scholar
• Doens D, Valiente PA, Mfuh AM, Vo A XT, Tristan A, Carreno L, et al. Identification of inhibitors of CD36-amyloid beta binding as potential agents for Alzheimer’s disease. ACS Chem Neurosci. 2017;8:1232–41. doi: 10.1021/acschemneuro.6b00386
   PubMed Web of Science ®Google Scholar
• Rangaraju S, Manner EB, Raza SA, Rathakrishnan P, Xiao H, Gao T, et al. Identification and therapeutic modulation of a pro-inflammatory subset of disease-associated-microglia in Alzheimer’s disease. Mol Neurodegener. 2018;13; doi:10.1186/s13024-018-0254-8.
   Web of Science ®Google Scholar
• Barber GN. STING: infection, inflammation and cancer. Nat Rev Immunol. 2015;15:760–70. doi: 10.1038/nri3921
   PubMed Web of Science ®Google Scholar
• Nazmi A, Field RH, Griffin EW, Haugh O, Hennessey E, Cox D, et al. Chronic neurodegeneration induces type I interferon synthesis via STING, shaping microglial phenotype and accelerating disease progression. Glia. 2019. doi:10.1002/glia.23592.
   PubMed Web of Science ®Google Scholar
• Walker DG, Whetzel AM, Lue LF. Expression of suppressor of cytokine signaling genes in human elderly and Alzheimer’s disease brains and human microglia. Neuroscience. 2012;302:121–37. doi: 10.1016/j.neuroscience.2014.09.052
   Google Scholar
• Lin HY, Lai RH, Lin ST, Lin RC, Wang MJ, Lin CC, et al. Suppressor of cytokine signaling 6 (SOCS6) promotes mitochondrial fission via regulating DRP1 translocation. Cell Death Differ. 2013;20:139–53. doi: 10.1038/cdd.2012.106
   PubMed Web of Science ®Google Scholar
• Moreira PI, Carvalho C, Zhu X, Smith MA, Perry G. Mitochondrial dysfunction is a trigger of Alzheimer’s disease pathophysiology. Biochim Biophys Acta. 2010;1802:2–10. doi: 10.1016/j.bbadis.2009.10.006
   PubMed Web of Science ®Google Scholar
• Onyango IG, Dennis J, Khan SM. Mitochondrial dysfunction in Alzheimer’s disease and the rationale for bioenergetics based therapies. Aging Dis. 2016;7:201–14. doi: 10.14336/AD.2015.1007
   PubMed Web of Science ®Google Scholar
• Walter S, Letiembre M, Liu Y, Heine H, Penke B, Hao W, et al. Role of the toll-like receptor 4 in neuroinflammation in Alzheimer’s disease. Cell Physiol Biochem. 2007;20:947–56. doi: 10.1159/000110455
   PubMed Web of Science ®Google Scholar
• Wang LQ. Mammalian phytoestrogens: enterodiol and enterolactone. J Chromatogr B Anal Technol Biomed Life Sci. 2002;777:289–309. doi: 10.1016/S1570-0232(02)00281-7
   PubMed Web of Science ®Google Scholar
• Di Meo F, Lemaurt V, Cornil J, Lazzaroni R, Duroux JC, Olivier Y, et al. Free radical scavenging by natural polyphenols: Atom versus electron transfer. J Phys Chem A. 2013;117:2082–92. doi: 10.1021/jp3116319
   PubMed Web of Science ®Google Scholar
• Rahman I, Biswas SK, Kirkham PA. Regulation of inflammation and redox signaling by dietary polyphenols. Biochem Pharmacol. 2006;72:1439–52. doi: 10.1016/j.bcp.2006.07.004
   PubMed Web of Science ®Google Scholar