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Research Paper

A modified Mediterranean-style diet enhances brain function via specific gut-microbiome-brain mechanisms

ORCID Icon, ORCID Icon, , , , , , , & ORCID Icon show all
Article: 2323752 | Received 08 Sep 2023, Accepted 22 Feb 2024, Published online: 06 Mar 2024

References

  • Dhana K, Evans DA, Rajan KB, Bennett DA, Morris MC. Healthy lifestyle and the risk of Alzheimer dementia: findings from 2 longitudinal studies. Neurology. 2020;95(4):e374–28. doi:10.1212/WNL.0000000000009816.
  • Norton S, Matthews FE, Barnes DE, Yaffe K, Brayne C. Potential for primary prevention of alzheimer’s disease: an analysis of population-based data. Lancet Neurol. 2014;13(8):788–794. doi:10.1016/S1474-4422(14)70136-X.
  • David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi:10.1038/nature12820.
  • Morais LH, Schreiber HL, Mazmanian SK. The gut microbiota–brain axis in behaviour and brain disorders. Nat Rev Microbiol. 2021;19(4):241–255. doi:10.1038/s41579-020-00460-0.
  • Quigley EMM. Microbiota-brain-gut axis and neurodegenerative diseases. Curr Neurol Neurosci Rep. 2017;17(12):94. doi:10.1007/s11910-017-0802-6.
  • Gates EJ, Bernath AK, Klegeris A. Modifying the diet and gut microbiota to prevent and manage neurodegenerative diseases. Rev Neurosci. 2022;33(7):767–787. doi:10.1515/revneuro-2021-0146.
  • Zhao J, Bi W, Xiao S, Lan X, Cheng X, Zhang J, Lu D, Wei W, Wang Y, Li H. Neuroinflammation induced by lipopolysaccharide causes cognitive impairment in mice. Sci Rep. 2019;9(1):5790. doi:10.1038/s41598-019-42286-8.
  • Kumar DKV, Choi SH, Washicosky KJ, Eimer WA, Tucker S, Ghofrani J, Lefkowitz A, McColl G, Goldstein LE, Tanzi RE. Amyloid-β peptide protects against microbial infection in mouse and worm models of Alzheimer’s disease. Sci Transl Med. 2016;8(340):ra34072–ra34072. doi:10.1126/scitranslmed.aaf1059.
  • Friedland RP, Chapman MR, Bliska JB. The role of microbial amyloid in neurodegeneration. PloS Pathog. 2017;13(12):e1006654. doi:10.1371/journal.ppat.1006654.
  • Więckowska-Gacek A, Mietelska-Porowska A, Wydrych M, Wojda U. Western diet as a trigger of Alzheimer’s disease: From metabolic syndrome and systemic inflammation to neuroinflammation and neurodegeneration. Ageing Res Rev. 2021;70:101397. doi:10.1016/j.arr.2021.101397.
  • Tosti V, Bertozzi B, Fontana L. Health benefits of the Mediterranean diet: metabolic and molecular mechanisms. J Gerontol A Biol Sci Med Sci. 2018;73:318–326. doi:10.1093/gerona/glx227.
  • Maggi S, Ticinesi A, Limongi F, Noale M, Ecarnot F. The role of nutrition and the Mediterranean diet on the trajectories of cognitive decline. Exp Gerontol. 2023;173:112110. doi:10.1016/j.exger.2023.112110.
  • Jensen NJ, Wodschow HZ, Nilsson M, Rungby J. Effects of ketone bodies on brain metabolism and function in neurodegenerative diseases. Int J Mol Sci. 2020;21(22):8767. doi:10.3390/ijms21228767.
  • Lilamand M, Porte B, Cognat E, Hugon J, Mouton-Liger F, Paquet C. Are ketogenic diets promising for Alzheimer’s disease? A translational review. Alz Res Therapy. 2020;12(1):42. doi:10.1186/s13195-020-00615-4.
  • Włodarek D. Role of ketogenic diets in neurodegenerative diseases (Alzheimer’s disease and Parkinson’s disease). Nutrients. 2019;11(1):169. doi:10.3390/nu11010169.
  • Heikura IA, Burke LM, Hawley JA, Ross ML, Garvican-Lewis L, Sharma AP, McKay AKA, Leckey JJ, Welvaert M, McCall L. et al. A short-term ketogenic diet impairs markers of bone health in response to exercise. Front Endocrinol. 2020 [accessed 2023 Aug 8];10. doi:10.3389/fendo.2019.00880.
  • Long F, Bhatti MR, Kellenberger A, Sun W, Modica S, Höring M, Liebisch G, Krieger JP, Wolfrum C, Challa TD. A low-carbohydrate diet induces hepatic insulin resistance and metabolic associated fatty liver disease in mice. Mol Metab. 2023;69:101675. doi:10.1016/j.molmet.2023.101675.
  • Nagpal R, Neth BJ, Wang S, Craft S, Yadav H. Modified Mediterranean-ketogenic diet modulates gut microbiome and short-chain fatty acids in association with Alzheimer’s disease markers in subjects with mild cognitive impairment. EBioMedicine. 2019;47:529–542. doi:10.1016/j.ebiom.2019.08.032.
  • Nagpal R, Neth BJ, Wang S, Mishra SP, Craft S, Yadav H. Gut mycobiome and its interaction with diet, gut bacteria and alzheimer’s disease markers in subjects with mild cognitive impairment: a pilot study. EBioMedicine [Internet]. 2020 [accessed 2023 Aug 8];59. doi:10.1016/j.ebiom.2020.102950.
  • Kumar A, Sharma M, Su Y, Singh S, Hsu FC, Neth BJ, Register TC, Blennow K, Zetterberg H, Craft S. et al. Small extracellular vesicles in plasma reveal molecular effects of modified Mediterranean-ketogenic diet in participants with mild cognitive impairment. Brain Communicat. 2022;4(6):fcac262. doi:10.1093/braincomms/fcac262.
  • Rao YL, Ganaraja B, Murlimanju BV, Joy T, Krishnamurthy A, Agrawal A. Hippocampus and its involvement in Alzheimer’s disease: a review. 3 biotech. 3 Biotech. 2022;12(2):55. doi:10.1007/s13205-022-03123-4.
  • Vercruysse P, Vieau D, Blum D, Petersén Å, Dupuis L. Hypothalamic alterations in neurodegenerative diseases and their relation to abnormal energy metabolism. Front Mol Neurosci. 2018;11:2. doi:10.3389/fnmol.2018.00002.
  • Craft S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Arch Neurol. 2009;66(3):300–305. doi:10.1001/archneurol.2009.27.
  • Meex RCR, Watt MJ. Hepatokines: linking nonalcoholic fatty liver disease and insulin resistance. Nat Rev Endocrinol. 2017;13(9):509–520. doi:10.1038/nrendo.2017.56.
  • Finucane FM, Sharp SJ, Hatunic M, Sleigh A, De Lucia Rolfe E, Aihie Sayer A, Cooper C, Griffin SJ, Wareham NJ. Liver fat accumulation is associated with reduced hepatic insulin extraction and beta cell dysfunction in healthy older individuals. Diabetol Metab Syndr. 2014;6(1):43. doi:10.1186/1758-5996-6-43.
  • Shively CA, Appt SE, Vitolins MZ, Uberseder B, Michalson KT, Silverstein-Metzler MG, Register TC. Mediterranean versus Western diet effects on caloric intake, obesity, metabolism, and hepatosteatosis in nonhuman primates. Obesity. 2019;27(5):777–784. doi:10.1002/oby.22436.
  • Zhao T, Zhan L, Zhou W, Chen W, Luo J, Zhang L, Weng Z, Zhao C, Liu S. The effects of erchen decoction on gut microbiota and lipid metabolism disorders in Zucker diabetic fatty rats. Front Pharmacol. 2021;12:647529. doi:10.3389/fphar.2021.647529.
  • Khan MT, Nieuwdorp M, Bäckhed F. Microbial modulation of insulin sensitivity. Cell Metab. 2014;20(5):753–760. doi:10.1016/j.cmet.2014.07.006.
  • Ding Y-L, Wang Y-H, Huang W, Liu G, Ross C, Hayden MR, Yang JK. Glucose intolerance and decreased early insulin response in mice with severe hypertriglyceridemia. Exp Biol Med (Maywood). 2010;235(1):40–46. doi:10.1258/ebm.2009.009100.
  • Nagpal R, Shively CA, Appt SA, Register TC, Michalson KT, Vitolins MZ, Yadav H. Gut microbiome composition in non-human primates consuming a Western or Mediterranean diet. Front Nutr[internet]. 2018 [accessed 2023 Jul 28];5. doi:10.3389/fnut.2018.00028.
  • McLeod A, Bernabe BP, Xia Y, Sanchez-Flack J, Lamar M, Schiffer L, Hemphill NON, Fantuzzi G, Maki P, Fitzgibbon M. et al. Exploring the effects of a Mediterranean diet and weight loss on the gut microbiome and cognitive performance in older, African American obese adults: a post hoc analysis. Nutrients. 2023;15(15):3332. doi:10.3390/nu15153332.
  • Newman TM, Shively CA, Register TC, Appt SE, Yadav H, Colwell RR, Fanelli B, Dadlani M, Graubics K, Nguyen UT. et al. Diet, obesity, and the gut microbiome as determinants modulating metabolic outcomes in a non-human primate model. Microbiome. 2021;9(1):100. doi:10.1186/s40168-021-01069-y.
  • Ma D, Wang AC, Parikh I, Green SJ, Hoffman JD, Chlipala G, Murphy MP, Sokola BS, Bauer B, Hartz AMS. et al. Ketogenic diet enhances neurovascular function with altered gut microbiome in young healthy mice. Sci Rep. 2018;8(1):6670. doi:10.1038/s41598-018-25190-5.
  • Huang HJ, Chen JL, Liao JF, Chen YH, Chieu MW, Ke YY, Hsu CC, Tsai YC, Hsieh-Li HM. Lactobacillus plantarum PS128 prevents cognitive dysfunction in Alzheimer’s disease mice by modulating propionic acid levels, glycogen synthase kinase 3 beta activity, and gliosis. BMC Complement Med Ther. 2021;21(1):259. doi:10.1186/s12906-021-03426-8.
  • Song X, Zhao Z, Zhao Y, Wang Z, Wang C, Yang G, Li S. Lactobacillus plantarum DP189 prevents cognitive dysfunction in D-galactose/AlCl3 induced mouse model of Alzheimer’s disease via modulating gut microbiota and PI3K/Akt/GSK-3β signaling pathway. Nutr Neurosci. 2022;25(12):2588–2600. doi:10.1080/1028415X.2021.1991556.
  • Li Y, Sun H, Chen Z, Xu H, Bu G, Zheng H. Implications of GABAergic neurotransmission in Alzheimer’s disease. Front Aging Neurosci. 2016 [accessed 2023 Jul 28];8. doi:10.3389/fnagi.2016.00031.
  • Yunes RA, Poluektova EU, Dyachkova MS, Klimina KM, Kovtun AS, Averina OV, Orlova VS, Danilenko VN. GABA production and structure of gadB/gadC genes in lactobacillus and bifidobacterium strains from human microbiota. Anaerobe. 2016;42:197–204. doi:10.1016/j.anaerobe.2016.10.011.
  • Al-Sarraf H. Transport of 14C-γ-aminobutyric acid into brain, cerebrospinal fluid and choroid plexus in neonatal and adult rats. Dev Brain Res. 2002;139(2):121–129. doi:10.1016/S0165-3806(02)00537-0.
  • Kuriyama K, Sze PY. Blood-brain barrier to H3-γ-aminobutyric acid in normal and amino oxyacetic acid-treated animals. Neuropharmacol. 1971;10(1):103–108. doi:10.1016/0028-3908(71)90013-X.
  • Janik R, Thomason LAM, Stanisz AM, Forsythe P, Bienenstock J, Stanisz GJ. Magnetic resonance spectroscopy reveals oral lactobacillus promotion of increases in brain GABA, N-acetyl aspartate and glutamate. Neuroimage. 2016;125:988–995. doi:10.1016/j.neuroimage.2015.11.018.
  • Olson CA, Vuong HE, Yano JM, Liang QY, Nusbaum DJ, Hsiao EY. The gut microbiota mediates the anti-seizure effects of the ketogenic diet. Cell. 2018;173(7):1728–1741.e13. doi:10.1016/j.cell.2018.04.027.
  • Wang Y, Wu J, Lv M, Shao Z, Hungwe M, Wang J, Bai X, Xie J, Wang Y, Geng W. Metabolism characteristics of lactic acid bacteria and the expanding applications in food industry. Front Bioeng Biotechnol. 2021 [accessed 2023 Jul 29];9. doi:10.3389/fbioe.2021.612285.
  • Lee YS, Kim TY, Kim Y, Lee SH, Kim S, Kang SW, Yang JY, Baek IJ, Sung YH, Park YY. et al. Microbiota-derived lactate accelerates intestinal stem-cell-mediated epithelial development. Cell Host Microbe. 2018;24(6):833–846.e6. doi:10.1016/j.chom.2018.11.002.
  • Duncan SH, Louis P, Flint HJ. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microb. 2004;70:5810–5817. doi:10.1128/AEM.70.10.5810-5817.2004.
  • Iraporda C, Errea A, Romanin DE, Cayet D, Pereyra E, Pignataro O, Sirard JC, Garrote GL, Abraham AG, Rumbo M. Lactate and short chain fatty acids produced by microbial fermentation downregulate proinflammatory responses in intestinal epithelial cells and myeloid cells. Immunobiol. 2015;220(10):1161–1169. doi:10.1016/j.imbio.2015.06.004.
  • Iraporda C, Romanin DE, Bengoa AA, Errea AJ, Cayet D, Foligné B, Sirard JC, Garrote GL, Abraham AG, Rumbo M. Local treatment with lactate prevents intestinal inflammation in the TNBS-Induced colitis model. Front Immunol. 2016 [accessed 2024 Jan 3];7. doi:10.3389/fimmu.2016.00651.
  • Tang H, Pang S, Wang M, Xiao X, Rong Y, Wang H, Zang YQ. TLR4 activation is required for IL-17–induced multiple tissue inflammation and wasting in mice. J Immunol. 2010;185(4):2563–2569. doi:10.4049/jimmunol.0903664.
  • Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol. 2014;6(3):703–713. doi:10.1093/gbe/evu050.
  • Detman A, Laubitz D, Chojnacka A, Kiela PR, Salamon A, Barberán A, Chen Y, Yang F, Błaszczyk MK, Sikora A. Dynamics of dark fermentation microbial communities in the light of lactate and butyrate production. Microbiome. 2021;9(1):158. doi:10.1186/s40168-021-01105-x.
  • Rutsch A, Kantsjö JB, Ronchi F. The gut-brain axis: how microbiota and host inflammasome influence brain physiology and pathology. Front Immunol. 2020 [accessed 2023 Aug 1];11. doi:10.3389/fimmu.2020.604179.
  • Morland C, Lauritzen KH, Puchades M, Holm-Hansen S, Andersson K, Gjedde A, Attramadal H, Storm-Mathisen J, Bergersen LH. The lactate receptor, G-protein-coupled receptor 81/hydroxycarboxylic acid receptor 1: expression and action in brain. J Neurosci Res. 2015;93(7):1045–1055. doi:10.1002/jnr.23593.
  • Morland C, Andersson KA, Haugen ØP, Hadzic A, Kleppa L, Gille A, Rinholm JE, Palibrk V, Diget EH, Kennedy LH. et al. Exercise induces cerebral VEGF and angiogenesis via the lactate receptor HCAR1. Nat Commun. 2017;8(1):15557. doi:10.1038/ncomms15557.
  • Dong S, Maniar S, Manole MD, Sun D. Cerebral hypoperfusion and other shared brain pathologies in ischemic stroke and Alzheimer’s disease. Transl Stroke Res. 2018;9(3):238–250. doi:10.1007/s12975-017-0570-2.
  • Colucci ACM, Tassinari ID, Loss E, de Fraga S. History and function of the lactate receptor GPR81/HCAR1 in the brain: a putative therapeutic target for the treatment of cerebral ischemia. Neuroscience. 2023;526:144–163. doi:10.1016/j.neuroscience.2023.06.022.
  • Kong L, Wang Z, Liang X, Wang Y, Gao L, Ma C. Monocarboxylate transporter 1 promotes classical microglial activation and pro-inflammatory effect via 6-phosphofructo-2-kinase/fructose-2, 6-biphosphatase 3. J Neuroinflammat. 2019;16(1):240. doi:10.1186/s12974-019-1648-4.
  • Lyra eSilva NM, Gonçalves RA, Pascoal TA, Lima-Filho RAS, Resende EPF, Vieira ELM, Teixeira AL, de Souza LC, Peny JA, Fortuna JTS. et al. Pro-inflammatory interleukin-6 signaling links cognitive impairments and peripheral metabolic alterations in Alzheimer’s disease. Transl Psychiatry. 2021;11(1):1–15. doi:10.1038/s41398-021-01349-z.
  • Mao JH, Kim YM, Zhou YX, Hu D, Zhong C, Chang H, Brislawn CJ, Fansler S, Langley S, Wang Y. et al. Genetic and metabolic links between the murine microbiome and memory. Microbiome. 2020;8(1):53. doi:10.1186/s40168-020-00817-w.
  • Song B, Zheng C, Zha C, Hu S, Yang X, Wang L, Xiao H. Dietary leucine supplementation improves intestinal health of mice through intestinal SIgA secretion. J Appl Microbiol. 2020;128(2):574–583. doi:10.1111/jam.14464.
  • Tărlungeanu DC, Deliu E, Dotter CP, Kara M, Janiesch PC, Scalise M, Galluccio M, Tesulov M, Morelli E, Sonmez FM. et al. Impaired amino acid transport at the blood brain barrier is a cause of autism spectrum disorder. Cell. 2016;167(6):1481–1494.e18. doi:10.1016/j.cell.2016.11.013.
  • Yudkoff M, Daikhin Y, Nissim I, Horyn O, Luhovyy B, Lazarow A, Nissim I. Brain amino acid requirements and toxicity: the example of leucine. J Nutr. 2005;135(6):1531S–1538S. doi:10.1093/jn/135.6.1531S.
  • Kanamori K, Ross BD, Kondrat RW. Rate of glutamate synthesis from leucine in rat brain measured in vivo by 15N NMR. J Neurochem. 1998;70(3):1304–1315. doi:10.1046/j.1471-4159.1998.70031304.x.
  • Ikeuchi T, Kanda M, Kitamura H, Morikawa F, Toru S, Nishimura C, Kasuga K, Tokutake T, Takahashi T, Kuroha Y. et al. Decreased circulating branched-chain amino acids are associated with development of Alzheimer’s disease in elderly individuals with mild cognitive impairment. Front Nutr. 2022 [accessed 2023 Aug 3];9. doi:10.3389/fnut.2022.1040476.
  • Yudkoff M, Daikhin Y, Grunstein L, Nissim I, Stern J, Pleasure D, Nissim I. Astrocyte leucine metabolism: significance of branched-chain amino acid transamination. J Neurochem. 1996;66(1):378–385. doi:10.1046/j.1471-4159.1996.66010378.x.
  • Greene C, Hanley N, Campbell M. Claudin-5: gatekeeper of neurological function. Fluids Barriers CNS. 2019;16(1):3. doi:10.1186/s12987-019-0123-z.
  • Liu Y, Beyer A, Aebersold R. On the dependency of cellular protein levels on mRNA abundance. Cell. 2016;165(3):535–550. doi:10.1016/j.cell.2016.03.014.
  • Kato H, Miura K, Nakano S, Suzuki K, Bannai M, Inoue Y. Leucine-enriched essential amino acids attenuate inflammation in rat muscle and enhance muscle repair after eccentric contraction. Amino Acids. 2016;48(9):2145–2155. doi:10.1007/s00726-016-2240-1.
  • Theis N, Brown MA, Wood P, Waldron M. Leucine supplementation increases muscle strength and volume, reduces inflammation, and affects wellbeing in adults and adolescents with cerebral palsy. J Nutr. 2021;151(1):59–64. doi:10.1093/jn/nxaa006.
  • Feijó G, dos S, Jantsch J, Correia LL, Eller S, Furtado-Filho OV, Giovenardi M, Porawski M, Braganhol E. Neuroinflammatory responses following zinc or branched-chain amino acids supplementation in obese rats. Metab Brain Dis. 2022;37(6):1875–1886. doi:10.1007/s11011-022-00996-5.
  • Lynch CJ, Adams SH. Branched-chain amino acids in metabolic signalling and insulin resistance. Nat Rev Endocrinol. 2014;10(12):723–736. doi:10.1038/nrendo.2014.171.
  • Holeček M. Branched-chain amino acids in health and disease: metabolism, alterations in blood plasma, and as supplements. Nutr Metab. 2018;15(1):33. doi:10.1186/s12986-018-0271-1.
  • Solon-Biet SM, Cogger VC, Pulpitel T, Wahl D, Clark X, Bagley EE, Gregoriou GC, Senior AM, Wang QP, Brandon AE. et al. Branched-chain amino acids impact health and lifespan indirectly via amino acid balance and appetite control. Nat Metab. 2019;1(5):532–545. doi:10.1038/s42255-019-0059-2.
  • Bourdeau-Julien I, Castonguay-Paradis S, Rochefort G, Perron J, Lamarche B, Flamand N, Di Marzo V, Veilleux A, Raymond F. The diet rapidly and differentially affects the gut microbiota and host lipid mediators in a healthy population. Microbiome. 2023;11(1):26. doi:10.1186/s40168-023-01469-2.
  • Xu R, Zhang Y, Chen S, Zeng Y, Fu X, Chen T, Luo S, Zhang X. The role of the probiotic akkermansia muciniphila in brain functions: insights underpinning therapeutic potential. Crit Rev Microbiol. 2023;49(2):151–176. doi:10.1080/1040841X.2022.2044286.
  • Galié S, García-Gavilán J, Camacho-Barcía L, Atzeni A, Muralidharan J, Papandreou C, Arcelin P, Palau-Galindo A, Garcia D, Basora J. et al. Effects of the Mediterranean diet or nut consumption on gut microbiota composition and fecal metabolites and their relationship with cardiometabolic risk factors. Mol Nutr Food Res. 2021;65(19):2000982. doi:10.1002/mnfr.202000982.
  • Meslier V, Laiola M, Roager HM, Filippis FD, Roume H, Quinquis B, Giacco R, Mennella I, Ferracane R, Pons N. et al. Mediterranean diet intervention in overweight and obese subjects lowers plasma cholesterol and causes changes in the gut microbiome and metabolome independently of energy intake. Gut. 2020;69(7):1258–1268. doi:10.1136/gutjnl-2019-320438.
  • Collins SL, Stine JG, Bisanz JE, Okafor CD, Patterson AD. Bile acids and the gut microbiota: metabolic interactions and impacts on disease. Nat Rev Microbiol. 2023;21(4):236–247. doi:10.1038/s41579-022-00805-x.
  • Wan YW, Al-Ouran R, Mangleburg CG, Perumal TM, Lee TV, Allison K, Swarup V, Funk CC, Gaiteri C, Allen M. et al. Meta-analysis of the Alzheimer’s disease human brain transcriptome and functional dissection in mouse models. Cell Rep. 2020;32(2):107908. doi:10.1016/j.celrep.2020.107908.
  • Moreno MDJM. Cognitive improvement in mild to moderate Alzheimer’s dementia after treatment with the acetylcholine precursor choline alfoscerate: a multicenter, double-blind, randomized, placebo-controlled trial. Clin Ther. 2003;25(1):178–193. doi:10.1016/S0149-2918(03)90023-3.
  • Parnetti L, Mignini F, Tomassoni D, Traini E, Amenta F. Cholinergic precursors in the treatment of cognitive impairment of vascular origin: ineffective approaches or need for re-evaluation? J Neurol Sci. 2007;257(1–2):264–269. doi:10.1016/j.jns.2007.01.043.
  • Silbergeld EK, Hruska RE, Bradley D, Lamon JM, Frykholm BC. Neurotoxic aspects of porphyrinopathies: lead and succinylacetone. Environ Res. 1982;29(2):459–471. doi:10.1016/0013-9351(82)90046-9.
  • Escartin C, Galea E, Lakatos A, O’Callaghan JP, Petzold GC, Serrano-Pozo A, Steinhäuser C, Volterra A, Carmignoto G, Agarwal A. et al. Reactive astrocyte nomenclature, definitions, and future directions. Nat Neurosci. 2021;24(3):312–325. doi:10.1038/s41593-020-00783-4.
  • Jurga AM, Paleczna M, Kuter KZ. Overview of general and discriminating markers of differential microglia phenotypes. Front Cell Neurosci. 2020 [accessed 2024 Jan 2];14. doi:10.3389/fncel.2020.00198.
  • Fujita A, Yamaguchi H, Yamasaki R, Cui Y, Matsuoka Y, Yamada K, Kira J. Connexin 30 deficiency attenuates A2 astrocyte responses and induces severe neurodegeneration in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine hydrochloride Parkinson’s disease animal model. J Neuroinflammat. 2018;15(1):227. doi:10.1186/s12974-018-1251-0.
  • Ayers KL, Mirshahi UL, Wardeh AH, Murray MF, Hao K, Glicksberg BS, Li S, Carey DJ, Chen R. A loss of function variant in CASP7 protects against Alzheimer’s disease in homozygous APOE ε4 allele carriers. BMC Genomics. 2016;17(S2):445. doi:10.1186/s12864-016-2725-z.
  • Brás JP, Bravo J, Freitas J, Barbosa MA, Santos SG, Summavielle T, Almeida MI. TNF-alpha-induced microglia activation requires miR-342: impact on NF-kB signaling and neurotoxicity. Cell Death Disease. 2020;11(6):1–15. doi:10.1038/s41419-020-2626-6.
  • Visser PJ, Reus LM, Gobom J, Jansen I, Dicks E, van der Lee SJ, Tsolaki M, Verhey FRJ, Popp J, Martinez-Lage P. et al. Cerebrospinal fluid tau levels are associated with abnormal neuronal plasticity markers in Alzheimer’s disease. Mol Neurodegener. 2022;17(1):27. doi:10.1186/s13024-022-00521-3.
  • Hampel H, Blennow K, Shaw LM, Hoessler YC, Zetterberg H, Trojanowski JQ. Total and phosphorylated tau protein as biological markers of Alzheimer’s disease. Exp Gerontol. 2010;45(1):30. doi:10.1016/j.exger.2009.10.010.
  • Hamano T, Enomoto S, Shirafuji N, Ikawa M, Yamamura O, Yen S-H, Nakamoto Y. Autophagy and tau protein. Int J Mol Sci. 2021;22(14):7475. doi:10.3390/ijms22147475.
  • Jiang S, Bhaskar K. Degradation and transmission of tau by autophagic-endolysosomal networks and potential therapeutic targets for tauopathy. Front Mol Neurosci. 2020 [accessed 2024 Jan 3];13. doi:10.3389/fnmol.2020.586731.
  • Nguyen TLA, Vieira-Silva S, Liston A, Raes J. How informative is the mouse for human gut microbiota research? Dis Model Mech. 2015;8(1):1–16. doi:10.1242/dmm.017400.
  • Perlman RL. Mouse models of human disease: an evolutionary perspective. Evol Med Public Health. 2016;2016:170–176. doi:10.1093/emph/eow014.
  • Song HW, Foreman KL, Gastfriend BD, Kuo JS, Palecek SP, Shusta EV. Transcriptomic comparison of human and mouse brain microvessels. Sci Rep. 2020;10(1):12358. doi:10.1038/s41598-020-69096-7.
  • Cai L, Xia X, Gu Y, Hu L, Li C, Ma X, Yin J. Opposite effects of low-carbohydrate high-fat diet on metabolism in humans and mice. Lipids Health Dis. 2023;22(1):191. doi:10.1186/s12944-023-01956-3.
  • Barrington WT, Wulfridge P, Wells AE, Rojas CM, Howe SY, Perry A, Hua K, Pellizzon MA, Hansen KD, Voy BH. Improving metabolic health through precision dietetics in mice. Genetics. 2018;208(1):399–417. doi:10.1534/genetics.117.300536.
  • Kadyan S, Park G, Singh P, Arjmandi B, Nagpal R. Prebiotic mechanisms of resistant starches from dietary beans and pulses on gut microbiome and metabolic health in a humanized murine model of aging. Front Nutr. 2023;10:1106463. doi:10.3389/fnut.2023.1106463.
  • Munley JA, Kelly LS, Park G, Gillies GS, Pons EE, Kannan KB, Whitley EM, Bible LE, Efron PA, Nagpal R. Multicompartmental traumatic injury induces sex-specific alterations in the gut microbiome. J Trauma Acute Care Surg. 2023;95(1):30–38. doi:10.1097/TA.0000000000003939.
  • Kadyan S, Park G, Wang B, Singh P, Arjmandi B, Nagpal R. Resistant starches from dietary pulses modulate the gut metabolome in association with microbiome in a humanized murine model of ageing. Sci Rep. 2023;13(1):10566. doi:10.1038/s41598-023-37036-w.
  • Gratton J, Phetcharaburanin J, Mullish BH, Williams HR, Thursz M, Nicholson JK, Holmes E, Marchesi JR, Li JV. Optimized sample handling strategy for metabolic profiling of human feces. Anal Chem. 2016;88(9):4661–4668. doi:10.1021/acs.analchem.5b04159.
  • Wang B, Maldonado-Devincci AM, Jiang L. Evaluating line-broadening factors on a reference spectrum as a bucketing method for NMR based metabolomics. Anal Biochem. 2020;606:113872. doi:10.1016/j.ab.2020.113872.
  • Crawley JN. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev. 1985;9(1):37–44. doi:10.1016/0149-7634(85)90030-2.
  • Barker GRI, Bird F, Alexander V, Warburton EC. Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci. 2007;27(11):2948–2957. doi:10.1523/JNEUROSCI.5289-06.2007.
  • d’Isa R, Comi G, Leocani L. Apparatus design and behavioural testing protocol for the evaluation of spatial working memory in mice through the spontaneous alternation T-maze. Sci Rep. 2021;11(1):21177. doi:10.1038/s41598-021-00402-7.
  • Hoffman E, Winder SJ. A modified wire hanging apparatus for small animal muscle function testing. PloS Curr. 2016;8:ecurrents.md.1e2bec4e78697b7b0ff80ea25a1d38be. doi:10.1371/currents.md.1e2bec4e78697b7b0ff80ea25a1d38be.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
  • Katoh K. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–3066. doi:10.1093/nar/gkf436.
  • Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MG. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020;38(6):685–688. doi:10.1038/s41587-020-0548-6.
  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):1–18. doi:10.1186/gb-2011-12-6-r60.
  • Fernandes AD, Reid JN, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome. 2014;2(1):1–13. doi:10.1186/2049-2618-2-15.