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Research Paper

A novel Mediterranean diet-inspired supplement ameliorates cognitive, microbial, and metabolic deficits in a mouse model of low-grade inflammation

, , , , , , , , , , & ORCID Icon show all
Article: 2363011 | Received 10 Jan 2024, Accepted 29 May 2024, Published online: 04 Jun 2024

References

  • Sikalidis AK, Kelleher AH, Kristo AS. Mediterranean Diet. Encyclopedia. 2021;1(2):371–19. doi:10.3390/encyclopedia1020031.
  • Gardener H, Caunca MR. Mediterranean Diet in Preventing Neurodegenerative Diseases. Curr Nutr Rep. 2018;7(1):10–20. doi:10.1007/s13668-018-0222-5.
  • Radd-Vagenas S, Duffy SL, Naismith SL, Brew BJ, Flood VM, Fiatarone Singh MA. Effect of the Mediterranean diet on cognition and brain morphology and function: a systematic review of randomized controlled trials. Am J Clin Nutr. 2018;107(3):389–404. doi:10.1093/ajcn/nqx070.
  • Sánchez-Villegas A, Galbete C, Martinez-González MA, Martinez JA, Razquin C, Salas-Salvadó J, Estruch R, Buil-Cosiales P, Martí A. The effect of the Mediterranean diet on plasma brain-derived neurotrophic factor (BDNF) levels: the PREDIMED-NAVARRA randomized trial. Nutr Neurosci. 2011;14(5):195–201. doi:10.1179/1476830511Y.0000000011.
  • Franco GA, Interdonato L, Cordaro M, Cuzzocrea S, Di Paola R. Bioactive compounds of the Mediterranean diet as nutritional support to fight neurodegenerative disease. Int J Mol Sci. 2023;24(8):24. doi:10.3390/ijms24087318.
  • De Marchi F, Vignaroli F, Mazzini L, Comi C, Tondo G. New insights into the relationship between nutrition and neuroinflammation in Alzheimer’s disease: Preventive and therapeutic perspectives. CNS Neurol Disord Drug Targets. 2023;23(5):614–627. doi:10.2174/1871527322666230608110201.
  • Mathur R, Ahmid Z, Ashor AW, Shannon O, Stephan BCM, Siervo M. Effects of dietary-based weight loss interventions on biomarkers of endothelial function: a systematic review and meta-analysis. Eur J Clin Nutr. 2023;77(10):927–940. doi:10.1038/s41430-023-01307-6.
  • Shannon OM, Ranson JM, Gregory S, Macpherson H, Milte C, Lentjes M, Mulligan A, McEvoy C, Griffiths A, Matu J. et al. Mediterranean diet adherence is associated with lower dementia risk, independent of genetic predisposition: findings from the UK biobank prospective cohort study. BMC Med. 2023;21(1):81. doi:10.1186/s12916-023-02772-3.
  • Kimble R, Gouinguenet P, Ashor A, Stewart C, Deighton K, Matu J, Griffiths A, Malcomson FC, Joel A, Houghton D. et al. Effects of a Mediterranean diet on the gut microbiota and microbial metabolites: A systematic review of randomized controlled trials and observational studies. Crit Rev Food Sci Nutr. 2022;63(27):8698–8719. doi:10.1080/10408398.2022.2057416.
  • Papadaki A, Wood L, Sebire SJ, Jago R. Adherence to the Mediterranean diet among employees in South West England: Formative research to inform a web-based, work-place nutrition intervention. Prev Med Rep. 2015;2:223–228. doi:10.1016/j.pmedr.2015.03.009.
  • Nair A, Jacob S. A simple practice guide for dose conversion between animals and human. J Basic Clin Pharm. 2016;7(2):27. doi:10.4103/0976-0105.177703.
  • Saavedra D, Añé-Kourí AL, Barzilai N, Caruso C, Cho KH, Fontana L, Franceschi C, Frasca D, Ledón N, Niedernhofer LJ. et al. Aging and chronic inflammation: highlights from a multidisciplinary workshop. Immun Ageing. 2023;20(1):25. doi:10.1186/s12979-023-00352-w.
  • Hoyles L, Pontifex MG, Rodriguez-Ramiro I, Anis-Alavi MA, Jelane KS, Snelling T, Solito E, Fonseca S, Carvalho AL, Carding SR. et al. Regulation of blood–brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide. Microbiome. 2021;9(1):235. doi:10.1186/s40168-021-01181-z.
  • Pontifex MG, Connell E, Le Gall G, Pourtau L, Gaudout D, Angeloni C, Zallocco L, Ronci M, Giusti L, Müller M. et al. Saffron extract (Safr’inside™) improves anxiety related behaviour in a mouse model of low-grade inflammation through the modulation of the microbiota and gut derived metabolites. Food Funct. 2022;13(23):12219–12233. doi:10.1039/D2FO02739A.
  • Di Paolo M, Corsi F, Cerri C, Bisti S, Piano I, Gargini C. A window to the brain: The Retina to monitor the progression and efficacy of saffron repron® Pre-Treatment in an LPS model of neuroinflammation and memory impairment. Pharmaceuticals (Basel). 2023;16(9):1307. doi:10.3390/ph16091307.
  • Zheng YR, Tufvesson-Alm M, Trepci A, Imbeault S, Li XQ, Schwieler L, Engberg G, Erhardt S. Dual administration of lipopolysaccharide induces behavioural changes in rats relevant to psychotic disorders. Acta Neuropsychiatr. 2023; 1–13. doi:10.1017/neu.2023.40.
  • Khodaei S, Wang DS, Ariza A, Syed RM, Orser BA. The impact of inflammation and general anesthesia on memory and executive function in mice. Anesth Analg. 2023;136(5):999–1011. doi:10.1213/ANE.0000000000006221.
  • Schaeffer JD, Newell C, Spann C, Siemens G, Liegey Dougall A. Inflammation, depression, and anxiety related to recognition memory in young adults. J Gen Psychol. 2023;150(1):1–25. doi:10.1080/00221309.2021.1893638.
  • Xie W, Kumar S, Kakon SH, Haque R, Petri WA, Nelson CA. Chronic inflammation is associated with neural responses to faces in bangladeshi children. Neuroimage. 2019;202:116110. doi:10.1016/j.neuroimage.2019.116110.
  • Goldstein FC, Loring DW, Thomas T, Saleh S, Hajjar I. Recognition memory performance as a cognitive marker of prodromal alzheimer’s disease. J Alzheimer’s Dis. 2019;72(2):507–514. doi:10.3233/JAD-190468.
  • Divella R, Marino G, Infusino S, Lanotte L, Gadaleta-Caldarola G, Gadaleta-Caldarola G. The Mediterranean Lifestyle to Contrast Low-Grade Inflammation Behavior in Cancer. Nutrients. 2023;15(7):15. doi:10.3390/nu15071667.
  • Rivera Rodríguez R, Jj J. Terpenes: Modulating anti-inflammatory signaling in inflammatory bowel disease. Pharmacol. Ther. 2023;248:108456. doi:10.1016/j.pharmthera.2023.108456.
  • Devranis P, Vassilopoulou Ε, Tsironis V, Sotiriadis PM, Chourdakis M, Aivaliotis M, Tsolaki M. Mediterranean diet, ketogenic diet or MIND diet for aging populations with cognitive decline: a systematic review. Life (Basel). 2023;13(1):173. doi:10.3390/life13010173.
  • Arjmand G, Abbas-Zadeh M, Eftekhari MH. Effect of MIND diet intervention on cognitive performance and brain structure in healthy obese women: a randomized controlled trial. Sci Rep. 2022;12(1):2871. doi:10.1038/s41598-021-04258-9.
  • Mattei J, Bigornia SJ, Sotos-Prieto M, Scott T, Gao X, Tucker KL. The Mediterranean diet and 2-year change in cognitive function by status of type 2 diabetes and glycemic control. Diabetes Care. 2019;42(8):1372–1379. doi:10.2337/dc19-0130.
  • Pollicino F, Veronese N, Dominguez LJ, Barbagallo M. Mediterranean diet and mitochondria: new findings. Exp Gerontol. 2023;176:112165. doi:10.1016/j.exger.2023.112165.
  • Armand-Ugon M, Ansoleaga B, Berjaoui S, Ferrer I. Reduced mitochondrial activity is early and steady in the entorhinal cortex but it is mainly unmodified in the frontal cortex in alzheimer’s disease. Curr Alzheimer Res. 2017;14(12):1327–1334. doi:10.2174/1567205014666170505095921.
  • Garcia-Esparcia P, Koneti A, Rodríguez-Oroz MC, Gago B, Del Rio JA, Ferrer I. Mitochondrial activity in the frontal cortex area 8 and angular gyrus in Parkinsons disease and Parkinsons disease with dementia. Brain Pathol. 2018;28(1):43–57. doi:10.1111/bpa.12474.
  • Li J, Zhang Y, Lu T, Liang R, Wu Z, Liu M, Qin L, Chen H, Yan X, Deng S. et al. Identification of diagnostic genes for both Alzheimer’s disease and metabolic syndrome by the machine learning algorithm. Front Immunol. 2022;13:1037318. doi:10.3389/fimmu.2022.1037318.
  • Monti E, Mancini A, Marras E, Gariboldi MB. Targeting Mitochondrial ROS production to reverse the epithelial-mesenchymal transition in breast cancer cells. Curr Issues Mol Biol. 2022;44(11):5277–5293. doi:10.3390/cimb44110359.
  • Xu X, Liu Y, Luan J, Liu R, Wang Y, Liu Y, Xu A, Zhou B, Han F, Shang W. et al. Effect of downregulated citrate synthase on oxidative phosphorylation signaling pathway in HEI-OC1 cells. Proteome Sci. 2022;20(1):14. doi:10.1186/s12953-022-00196-0.
  • Chang J, Jung HJ, Jeong SH, Kim HK, Han J, Kwon HJ. A mutation in the mitochondrial protein UQCRB promotes angiogenesis through the generation of mitochondrial reactive oxygen species. Biochem Biophys Res Commun. 2014;455(3–4):290–297. doi:10.1016/j.bbrc.2014.11.005.
  • Yu Z, Zhang Y, Liu N, Yuan J, Lin L, Zhuge Q, Xiao J, Wang X. Roles of neuroglobin binding to mitochondrial complex III subunit cytochrome c1 in oxygen-glucose deprivation-induced neurotoxicity in primary neurons. Mol Neurobiol. 2016;53(5):3249–3257. doi:10.1007/s12035-015-9273-4.
  • Zheng J, Xu M, Walker V, Yuan J, Korologou-Linden R, Robinson J, Huang P, Burgess S, Au Yeung SL, Luo S. et al. Evaluating the efficacy and mechanism of metformin targets on reducing Alzheimer’s disease risk in the general population: a Mendelian randomisation study. Diabetologia. 2022;65(10):1664–1675. doi:10.1007/s00125-022-05743-0.
  • Chen R, Yi Y, Xiao W, Zhong B, Shu Y, Zhang L, Zeng Y. Label-free liquid chromatography–mass spectrometry proteomic analysis of urinary identification in diabetic vascular dementia in a Han Chinese population. Front Aging Neurosci. 2021;13:619945. doi:10.3389/fnagi.2021.619945.
  • Yu H, Wang D, Zou L, Zhang Z, Xu H, Zhu F, Ren X, Xu B, Yuan J, Liu J. et al. Proteomic alterations of brain subcellular organelles caused by low-dose copper exposure: implication for Alzheimer’s disease. Arch Toxicol. 2018;92(4):1363–1382. doi:10.1007/s00204-018-2163-6.
  • Qi YJ, Lu YR, Shi LG, Demmers JAA, Bezstarosti K, Rijkers E, Balesar R, Swaab D, Bao A-M. Distinct proteomic profiles in prefrontal subareas of elderly major depressive disorder and bipolar disorder patients. Transl Psychiatry. 2022;12(1):275. doi:10.1038/s41398-022-02040-7.
  • Henningsen K, Palmfeldt J, Christiansen S, Baiges I, Bak S, Jensen ON, Gregersen N, Wiborg O. Candidate hippocampal biomarkers of susceptibility and resilience to stress in a rat model of depression. Molecular & Cellular Proteomics: MCP. 2012;11(7):M111.016428. doi:10.1074/mcp.M111.016428.
  • Wei K, Wei Y, Wang Y, Wei X. Amelioration effects and regulatory mechanisms of different tea active ingredients on DSS-Induced colitis. J Agric Food Chem. 2023;71(44):16604–16617. doi:10.1021/acs.jafc.3c04524.
  • Lei W, Cheng Y, Gao J, Liu X, Shao L, Kong Q, Zheng N, Ling Z, Hu W. Akkermansia muciniphila in neuropsychiatric disorders: friend or foe? Front Cell Infect Microbiol. 2023;13:1224155. doi:10.3389/fcimb.2023.1224155.
  • Huang F, Marungruang N, Martinsson I, Camprubí Ferrer L, Nguyen TD, Gondo TF, Karlsson EN, Deierborg T, Öste R, Heyman-Lindén L. et al. A mixture of Nordic berries improves cognitive function, metabolic function and alters the gut microbiota in C57Bl/6J male mice. Front Nutr. 2023;10:1257472. doi:10.3389/fnut.2023.1257472.
  • 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.
  • Higarza SG, Arboleya S, Arias JL, Gueimonde M, Arias N. Akkermansia muciniphila and environmental enrichment reverse cognitive impairment associated with high-fat high-cholesterol consumption in rats. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2021.1880240.
  • Yan J, Sheng L, Li H. Akkermansia muciniphila: is it the holy grail for ameliorating metabolic diseases? Gut Microbes. 2021;13(1). doi:10.1080/19490976.2021.1984104.
  • Ullah R, Ali G, Baseer A, Irum Khan S, Akram M, Khan S, Ahmad N, Farooq U, Kanwal Nawaz N, Shaheen S. et al. Tannic acid inhibits lipopolysaccharide-induced cognitive impairment in adult mice by targeting multiple pathological features. Int Immunopharmacol. 2022;110:108970. doi:10.1016/j.intimp.2022.108970.
  • Lee Y, Ju X, Cui J, Zhang T, Hong B, Kim YH, Ko Y, Park J, Choi CH, Heo JY. et al. Mitochondrial dysfunction precedes hippocampal IL-1β transcription and cognitive impairments after low-dose lipopolysaccharide injection in aged mice. Heliyon. 2024;10(7):e28974. doi:10.1016/j.heliyon.2024.e28974.
  • Liang Y, Kang X, Zhang H, Xu H, Wu X. Knockdown and inhibition of hippocampal GPR17 attenuates lipopolysaccharide-induced cognitive impairment in mice. J Neuroinflammation. 2023;20(1):271. doi:10.1186/s12974-023-02958-9.
  • Wu Y, Yuan Q, Ma Y, Zhou X, Wang G, Wang S, Li S, Shi J, Wang D. Dietary intervention with the gut microbial metabolite urolithin a attenuates lipopolysaccharide-induced neuroinflamm and cognitive deficits via the Sirt1/acetyl-NF-κB signaling pathway. Mol Nutr Food Res. 2023;67(13):e2200401. doi:10.1002/mnfr.202200401.
  • Zeini S, Davoodian N, Kazemi H, Shareghi Brojeni M, Ghani E, Arab Firouzjaei M, Atashabparvar A. Resveratrol prevents cognitive impairment and hippocampal inflammatory response induced by lipopolysaccharide in a mouse model of chronic neuroinflammation. Physiol Behav. 2024;278:114508. doi:10.1016/j.physbeh.2024.114508.
  • Öz M, Erdal H. A TNF-α inhibitor abolishes sepsis-induced cognitive impairment in mice by modulating acetylcholine and nitric oxide homeostasis, BDNF release, and neuroinflammation. Behav Brain Res. 2024;466:114995. doi:10.1016/j.bbr.2024.114995.
  • Muhammad T, Ikram M, Ullah R, Rehman SU, Kim MO. Hesperetin, a citrus flavonoid, attenuates LPS-Induced neuroinflammation, apoptosis and memory impairments by modulating TLR4/NF-κB signaling. Nutrients. 2019;11(3):11. doi:10.3390/nu11030648.
  • Qiu F, Liu Y, Liu Y, Zhao Z, Zhou L, Chen P, Du Y, Wang Y, Sun H, Zeng C. et al. CD137L inhibition ameliorates hippocampal neuroinflammation and behavioral deficits in a mouse model of sepsis-associated encephalopathy. Neuromolecular Med. 2023;25(4):616–631. doi:10.1007/s12017-023-08764-z.
  • Jiang C, Caskurlu A, Ganesh T, Dingledine R. Inhibition of the prostaglandin EP2 receptor prevents long-term cognitive impairment in a model of systemic inflammation. Brain Behav Immun Health. 2020;8:100132. doi:10.1016/j.bbih.2020.100132.
  • Liu L, Kelly MG, Yang XR, Fernandez TG, Wierzbicki EL, Skrobach A, Doré S. Nrf2 deficiency exacerbates cognitive impairment and reactive microgliosis in a lipopolysaccharide-induced neuroinflammatory mouse model. Cell Mol Neurobiol. 2020;40(7):1185–1197. doi:10.1007/s10571-020-00807-4.
  • Huang WY, Liu KH, Lin S, Chen TY, Tseng CY, Chen HY, Wu HM, Hsu KS. NADPH oxidase 2 as a potential therapeutic target for protection against cognitive deficits following systemic inflammation in mice. Brain Behav Immun. 2020;84:242–252. doi:10.1016/j.bbi.2019.12.006.
  • Connell E, Le Gall G, Pontifex MG, Sami S, Cryan JF, Clarke G, Müller M, Vauzour D. Microbial-derived metabolites as a risk factor of age-related cognitive decline and dementia. Mol Neurodegener. 2022;17(1):43. doi:10.1186/s13024-022-00548-6.
  • Davis C, Bryan J, Hodgson J, Murphy K. Definition of the Mediterranean diet; a literature review. Nutrients. 2015;7(11):9139–9153. doi:10.3390/nu7115459.
  • Boutron I, Percie du Sert N, Hurst V, Ahluwalia A, Alam S, Avey MT, Browne WJ, Clark A, Cuthill IC, Dirnagl U. et al. The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLOS Biol. 2020;18(7):18. doi:10.1371/journal.pbio.3000410.
  • Laukens D, Brinkman BM, Raes J, De Vos M, Vandenabeele P, Normark BH. Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol Rev. 2016;40(1):117–132. doi:10.1093/femsre/fuv036.
  • Hoyles L, Pontifex MG, Rodriguez-Ramiro I, Anis-Alavi MA, Jelane KS, Snelling T, Solito E, Fonseca S, Carvalho AL, Carding SR. et al. Regulation of blood–brain barrier integrity by microbiome-associated methylamines and cognition by trimethylamine N-oxide. Microbiome. 2021;9(1). doi:10.1186/s40168-021-01181-z.
  • Denninger JK, Smith BM, Kirby ED. Novel object recognition and object location behavioral testing in mice on a budget. J Vis Exp. 2018;(141). doi:10.3791/58593-v.
  • Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261–5267. doi:10.1128/AEM.00062-07.
  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41(D1):D590–D6. doi:10.1093/nar/gks1219.
  • Tran TTT, Corsini S, Kellingray L, Hegarty C, Le Gall G, Narbad A, Müller M, Tejera N, O’Toole PW, Minihane A-M. et al. APOE genotype influences the gut microbiome structure and function in humans and mice: relevance for Alzheimer’s disease pathophysiology. FASEB J. 2019;33(7):8221–8231. doi:10.1096/fj.201900071R.
  • Pirone A, Ciregia F, Lazzarini G, Miragliotta V, Ronci M, Zuccarini M, Zallocco L, Beghelli D, Mazzoni MR, Lucacchini A. et al. Proteomic profiling reveals specific molecular hallmarks of the pig claustrum. Mol Neurobiol. 2023;60(8):4336–4358. doi:10.1007/s12035-023-03347-2.
  • Barbalace MC, Zallocco L, Beghelli D, Ronci M, Scortichini S, Digiacomo M, Macchia M, Mazzoni MR, Fiorini D, Lucacchini A. et al. Antioxidant and neuroprotective activity of extra virgin olive oil extracts obtained from quercetano cultivar trees grown in different areas of the Tuscany region (Italy). Antioxidants. 2021;10(3):10. doi:10.3390/antiox10030421.
  • Giusti L, Angeloni C, Barbalace M, Lacerenza S, Ciregia F, Ronci M, Urbani A, Manera C, Digiacomo M, Macchia M. et al. A proteomic approach to uncover neuroprotective mechanisms of oleocanthal against oxidative stress. Int J Mol Sci. 2018;19(8):2329. doi:10.3390/ijms19082329.
  • Lanas A, Tacconelli S, Contursi A, Piazuelo E, Bruno A, Ronci M, Marcone S, Dovizio M, Sopeña F, Falcone L. et al. Biomarkers of response to low-dose aspirin in familial adenomatous polyposis patients. Cancers. 2023;15(9):15. doi:10.3390/cancers15092457.
  • Xin L, Qiao R, Chen X, Tran H, Pan S, Rabinoviz S, Bian H, He X, Morse B, Shan B. et al. A streamlined platform for analyzing tera-scale DDA and DIA mass spectrometry data enables highly sensitive immunopeptidomics. Nat Commun. 2022;13(1). doi:10.1038/s41467-022-30867-7.
  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–D13. doi:10.1093/nar/gky1131.
  • Xie F, Wang J, Zhang B. RefFinder: a web-based tool for comprehensively analyzing and identifying reference genes. Funct Integr Genomics. 2023;23(2):23. doi:10.1007/s10142-023-01055-7.
  • Pang Z, Chong J, Zhou G, de Lima Morais DA, Chang L, Barrette M, Gauthier C, Jacques P-É, Li S, Xia J. et al. MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021;49(W1):W388–W96. doi:10.1093/nar/gkab382.
  • Ni Y, Yu G, Chen H, Deng Y, Wells PM, Steves CJ, Ju F, Fu J. M2IA: a web server for microbiome and metabolome integrative analysis. Bioinformatics. 2020;36(11):3493–3498. doi:10.1093/bioinformatics/btaa188.
  • Dhariwal A, Chong J, Habib S, King IL, Agellon LB, Xia J. MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 2017;45(W1):W180–w8. doi:10.1093/nar/gkx295.
  • You Y, Liang D, Wei R, Li M, Li Y, Wang J, Wang X, Zheng X, Jia W, Chen T. et al. Evaluation of metabolite-microbe correlation detection methods. Anal Biochem. 2019;567:106–111. doi:10.1016/j.ab.2018.12.008.