Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Volume 26, 2023 - Issue 11
1,256
Views
3
CrossRef citations to date
0
Altmetric
Research Article

The microbiome-gut-brain axis in nutritional neuroscience

ORCID Icon, , & ORCID Icon

References

  • Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med. 2016 Dec 15;375(24):2369–79. doi:10.1056/NEJMra1600266.
  • Morais LH, Schreiber HL, Mazmanian SK. The gut microbiota–brain axis in behaviour and brain disorders. Nat Rev Microbiol. 2021;19(4):241–55. doi:10.1038/s41579-020-00460-0.
  • Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 2016;14(8):e1002533. doi:10.1371/journal.pbio.1002533.
  • Boscaini S, Leigh S-J, Lavelle A, García-Cabrerizo R, Lipuma T, Clarke G, et al. Microbiota and body weight control: weight watchers within? Mol Metab. 2021;57:101427–101427. doi:10.1016/j.molmet.2021.101427.
  • Schellekens H, Torres-Fuentes C, van de Wouw M, Long-Smith CM, Mitchell A, Strain C, et al. Bifidobacterium longum counters the effects of obesity: partial successful translation from rodent to human. EBioMedicine. 2021 Jan;63:103176. doi:10.1016/j.ebiom.2020.103176.
  • Torres-Fuentes C, Schellekens H, Dinan TG, Cryan JF, et al. The microbiota-gut-brain axis in obesity. Lancet Gastroenterol Hepatol. 2017 Oct;2(10):747–56. doi:10.1016/s2468-1253(17)30147-4.
  • Korpela K, Kallio S, Salonen A, Hero M, Kukkonen AK, Miettinen PJ, et al. Gut microbiota develop towards an adult profile in a sex-specific manner during puberty. Sci Rep. 2021 Dec 2;11(1):23297. doi:10.1038/s41598-021-02375-z.
  • Codagnone MG, Spichak S, O'Mahony SM, O’Mahony SM, O’Leary OF, Clarke G, et al. Programming bugs: microbiota and the developmental origins of brain health and disease. Biol Psychiatry. 2019 Jan 15;85(2):150–63. doi:10.1016/j.biopsych.2018.06.014.
  • Cowan CSM, Dinan TG, Cryan JF. Annual research review: critical windows – the microbiota-gut-brain axis in neurocognitive development. J Child Psychol Psychiatry. 2020 Mar;61(3):353–71. doi:10.1111/jcpp.13156.
  • Daliry A, Pereira E. Role of maternal microbiota and nutrition in early-life neurodevelopmental disorders. Nutrients. 2021 Oct 9;13(10):3533. doi:10.3390/nu13103533.
  • Forssberg H. Microbiome programming of brain development: implications for neurodevelopmental disorders. Dev Med Child Neurol. 2019;61(7):744–9. doi:10.1111/dmcn.14208.
  • Cruz-Pereira JS, Rea K, Nolan YM, O'Leary OF, Dinan TG, Cryan JF. Depression's unholy TRinity: dysregulated stress, immunity, and the microbiome. Annu Rev Psychol. 2020;71(1):49–78. doi:10.1146/annurev-psych-122216-011613.
  • Forssten SD, Ouwehand AC, Griffin SM, Patterson E, et al. One giant leap from mouse to man: the microbiota–gut–brain axis in mood disorders and translational challenges moving towards human clinical trials. Nutrients. 2022;14(3):568. doi:10.3390/nu14030568.
  • Manchia M, Fontana A, Panebianco C, Paribello P, Arzedi C, Cossu E, et al. Involvement of Gut microbiota in schizophrenia and treatment resistance to antipsychotics. Biomedicines. 2021 Jul 23;9(8):875. doi:10.3390/biomedicines9080875.
  • Boehme M, Guzzetta KE, Bastiaanssen TFS, van de Wouw M, Moloney GM, Gual-Grau A, et al. Microbiota from young mice counteracts selective age-associated behavioral deficits. Nat Aging. 2021;1(8):666–76. doi:10.1038/s43587-021-00093-9.
  • Dinan TG, Cryan JF. Gut instincts: microbiota as a key regulator of brain development, ageing and neurodegeneration. J Physiol. 2017;595(2):489–503. doi:10.1113/JP273106.
  • Ghosh TS, Shanahan F, O’Toole PW. The gut microbiome as a modulator of healthy ageing. Nat Rev Gastroenterol Hepatol. 2022. doi:10.1038/s41575-022-00605-x.
  • Li Y, Ning L, Yin Y, Wang R, Zhang Z, Hao L, et al. Age-related shifts in gut microbiota contribute to cognitive decline in aged rats. Aging (Albany NY). 2020 May 1;12(9):7801–17. doi:10.18632/aging.103093.
  • O'Connor R, Moloney GM, Fulling C, O’Connor R, O’Riordan KJ, Fitzgerald P, et al. Maternal antibiotic administration during a critical developmental window has enduring neurobehavioural effects in offspring mice. Behav Brain Res. 2021 Apr 23;404:113156. doi:10.1016/j.bbr.2021.113156.
  • O'Connor R, van De Wouw M, Moloney GM, O’Connor R, Ventura-Silva AP, O’Riordan K, et al. Strain differences in behaviour and immunity in aged mice: relevance to autism. Behav Brain Res. 2021 Feb 5;399:113020. doi:10.1016/j.bbr.2020.113020.
  • Wu ML, Yang XQ, Xue L, Duan W, Du J-R. Age-related cognitive decline is associated with microbiota-gut-brain axis disorders and neuroinflammation in mice. Behav Brain Res. 2021 Mar 26;402:113125. doi:10.1016/j.bbr.2021.113125.
  • Kemp KM, Colson J, Lorenz RG, Maynard CL, Pollock JS. Early life stress in mice alters gut microbiota independent of maternal microbiota inheritance. American journal of physiology-regulatory. Integr Compar Physiol. 2021;320(5):R663–R674. doi:10.1152/ajpregu.00072.2020.
  • van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C, O'Sullivan O, et al. Short-chain fatty acids: microbial metabolites that alleviate stress-induced brain-gut axis alterations. J Physiol. 2018;596(20):4923–44. doi:10.1113/JP276431.
  • García-Cabrerizo R, Carbia C, ÓRiordan KJ, Schellekens H, Cryan JF. Microbiota-gut-brain axis as a regulator of reward processes. J Neurochem. 2021 Jun;157(5):1495–524. doi:10.1111/jnc.15284.
  • Torres-Fuentes C, Golubeva AV, Zhdanov AV, Torres-Fuentes C, Wallace S, Arboleya S, et al. Short-chain fatty acids and microbiota metabolites attenuate ghrelin receptor signaling. FASEB J. 2019;33(12):13546–59. doi:10.1096/fj.201901433R.
  • Chen Y, Xu J, Chen Y. Regulation of neurotransmitters by the gut microbiota and effects on cognition in neurological disorders. Nutrients. 2021;13(6):2099. doi:10.3390/nu13062099.
  • Berding K, Vlckova K, Marx W, Schellekens H, Stanton C, Clarke G, et al. Diet and the microbiota-gut-brain axis: sowing the seeds of good mental health. Adv Nutr. 2021 Jul 30;12(4):1239–85. doi:10.1093/advances/nmaa181.
  • Spichak S, Bastiaanssen TFS, Berding K, Vlckova K, Clarke G, Dinan TG, Cryan JF. Mining microbes for mental health: determining the role of microbial metabolic pathways in human brain health and disease. Neurosci Biobehav Rev. 2021 Jun;125:698–761. doi:10.1016/j.neubiorev.2021.02.044.
  • Gentile F, Doneddu PE, Riva N, Nobile-Orazio E, Quattrini A. Diet, microbiota and brain health: unraveling the network intersecting metabolism and neurodegeneration. Int J Mol Sci. 2020;21(20):7471. doi:10.3390/ijms21207471.
  • O'Mahony SM, Clarke G, Borre YE, O’Mahony SM, Dinan TG, Cryan JF. Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res. 2015 Jan 15;277:32–48. doi:10.1016/j.bbr.2014.07.027.
  • Delgado I, Cussotto S, Anesi A, Dexpert S, Aubert A, Aouizerate B, et al. Association between the indole pathway of tryptophan metabolism and subclinical depressive symptoms in obesity: a preliminary study. Int J Obes (Lond). 2022 Jan 10;46(4):885–8. doi:10.1038/s41366-021-01049-0.
  • Golubeva AV, Joyce SA, Moloney G, Burokas A, Sherwin E, Arboleya S, et al. Microbiota-related changes in bile acid & tryptophan metabolism are associated with gastrointestinal dysfunction in a mouse model of autism. EBioMedicine. 2017 Oct;24:166–78. doi:10.1016/j.ebiom.2017.09.020.
  • Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem. 2003 Mar 28;278(13):11312–9. doi:10.1074/jbc.M211609200.
  • Cohen LJ, Esterhazy D, Kim S-H, Lemetre C, Aguilar RR, Gordon EA, et al. Commensal bacteria make GPCR ligands that mimic human signalling molecules. Nature. 2017;549(7670):48–53.
  • Lozupone M, D'Urso F, Piccininni C, Montagna ML, Sardone R, Resta E, et al. The relationship between epigenetics and microbiota in neuropsychiatric diseases. Epigenomics. 2020;12(17):1559–68. doi:10.2217/epi-2020-0053.
  • Sharma M, Li Y, Stoll ML, Tollefsbol TO. The epigenetic connection between the gut microbiome in obesity and diabetes. Front Genet. 2020;10:1329–. doi:10.3389/fgene.2019.01329.
  • Woo V, Alenghat T. Epigenetic regulation by gut microbiota. Gut Microbes. 2022;14(1):2022407. doi:10.1080/19490976.2021.2022407.
  • Berding K, Cryan JF. Microbiota-targeted interventions for mental health. Curr Opin Psychiatry. 2022 Jan 1;35(1):3–9. doi:10.1097/yco.0000000000000758.
  • Borge TC, Aase H, Brantsæter AL, Biele G. The importance of maternal diet quality during pregnancy on cognitive and behavioural outcomes in children: a systematic review and meta-analysis. BMJ Open. 2017 Sep 24;7(9):e016777. doi:10.1136/bmjopen-2017-016777.
  • Codagnone MG, Stanton C, O'Mahony SM, O’Mahony SM, Dinan TG, Cryan JF. Microbiota and neurodevelopmental trajectories: role of maternal and early-life nutrition. Ann Nutr Metab. 2019;74(Suppl 2):16–27. doi:10.1159/000499144.
  • Lynn MA, Eden G, Ryan FJ, Bensalem J, Wang X, Blake SJ, et al. The composition of the gut microbiota following early-life antibiotic exposure affects host health and longevity in later life. Cell Rep. 2021 Aug 24;36(8):109564. doi:10.1016/j.celrep.2021.109564.
  • Vich Vila A, Collij V, Sanna S, Sinha T, Imhann F, Bourgonje AR, et al. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat Commun. 2020;11(1):362. doi:10.1038/s41467-019-14177-z.
  • Schverer M, Donoso F, Mitchell A, Rea K, Fitzgerald P, Sen P, et al. Dietary milk phospholipids attenuate chronic stress-induced changes in behavior and endocrine responses across the lifespan. Mol Nutr Food Res. 2021 Dec 1;66(3):e2100665. doi:10.1002/mnfr.202100665.
  • Koletzko B, Brands B, Grote V, Kirchberg FF, Prell C, Rzehak P, et al. Long-Term health impact of early nutrition: the power of programming. Ann Nutr Metab. 2017;70(3):161–9. doi:10.1159/000477781.
  • Liu Z, Subbaraj A, Fraser K, Jia H, Chen W, Day L, et al. Human milk and infant formula differentially alters the microbiota composition and functional gene relative abundance in the small and large intestines in weanling rats. Eur J Nutr. 2020 Aug;59(5):2131–43. doi:10.1007/s00394-019-02062-w.
  • Mennella JA, Li Y, Bittinger K, Friedman ES, Zhao C, Wu GD, Trabulsi JC. The macronutrient composition of infant formula produces differences in gut microbiota maturation that associate with weight gain velocity and weight status. Nutrients. 2022 Mar 15;14(6):1241. doi:10.3390/nu14061241.
  • Oluwagbemigun K, O'Donovan AN, Berding K, Lyons K, Alexy U, Schmid M, et al. Long-term dietary intake from infancy to late adolescence is associated with gut microbiota composition in young adulthood. Am J Clin Nutr. 2021;113(3):647–56. doi:10.1093/ajcn/nqaa340.
  • Kim G, Bae J, Kim MJ, et al. Delayed establishment of gut microbiota in infants delivered by cesarean section [original research]. Front Microbiol. 2020;11; doi:10.3389/fmicb.2020.02099.English.
  • Ma J, Li Z, Zhang W, Mei H, Zhuo N, Wang H, et al. Comparison of gut microbiota in exclusively breast-fed and formula-fed babies: a study of 91 term infants. Sci Rep. 2020 Sep 25;10(1):15792. doi:10.1038/s41598-020-72635-x.
  • Frank NM, Lynch KF, Uusitalo U, Yang J, Lönnrot M, Virtanen SM, et al. The relationship between breastfeeding and reported respiratory and gastrointestinal infection rates in young children. BMC Pediatr. 2019;19(1):339. doi:10.1186/s12887-019-1693-2.
  • Ratsika A, Codagnone MC, O'Mahony S, O’Mahony S, Stanton C, Cryan JF. Priming for life: early life nutrition and the microbiota-gut-brain axis. Nutrients. 2021;13(2):423. doi:10.3390/nu13020423.
  • Girdhar K, Soto M, Huang Q, Orliaguet L, Cederquist C, Sundaresh B, et al. Gut microbiota regulate pancreatic growth, exocrine function and gut hormones. Diabetes. 2022;71(5):945–60. doi:10.2337/db21-0382.
  • Scheepers LE, Penders J, Mbakwa CA, Thijs C, Mommers M, Arts ICW. The intestinal microbiota composition and weight development in children: the KOALA birth cohort study. Int J Obes (Lond). 2015 Jan;39(1):16–25. doi:10.1038/ijo.2014.178.
  • Mubanga M, Lundholm C, D'Onofrio BM, D’Onofrio BM, Stratmann M, Hedman A, Almqvist C. Association of early life exposure to antibiotics with risk of atopic dermatitis in Sweden. JAMA Netw Open. 2021 Apr 1;4(4):e215245. doi:10.1001/jamanetworkopen.2021.5245.
  • Örtqvist AK, Lundholm C, Halfvarson J, Ludvigsson JF, Almqvist C. Fetal and early life antibiotics exposure and very early onset inflammatory bowel disease: a population-based study. Gut. 2019 Feb;68(2):218–25. doi:10.1136/gutjnl-2017-314352.
  • Alsegiani AS, Shah ZA. The influence of gut microbiota alteration on age-related neuroinflammation and cognitive decline. Neural Regen Res. 2022;17(11):2407–2412.
  • Unger MM, Spiegel J, Dillmann KU, Grundmann D, Philippeit H, Bürmann J, et al. Short chain fatty acids and gut microbiota differ between patients with Parkinson's disease and age-matched controls. Parkinsonism Relat Disord. 2016 Nov;32:66–72. doi:10.1016/j.parkreldis.2016.08.019.
  • Minter MR, Hinterleitner R, Meisel M, Zhang C, Leone V, Zhang X, et al. Antibiotic-induced perturbations in microbial diversity during post-natal development alters amyloid pathology in an aged APP(SWE)/PS1(ΔE9) murine model of Alzheimer's disease. Sci Rep. 2017 Sep 5;7(1):10411. doi:10.1038/s41598-017-11047-w.
  • Preiningerova JL, Jiraskova Zakostelska Z, Srinivasan A, Ticha V, Kovarova I, Kleinova P, et al. Multiple sclerosis and microbiome. Biomolecules. 2022 Mar 11;12(3):433. doi:10.3390/biom12030433.
  • Zhu F, Ju Y, Wang W, Guo R, Ma Q, Sun Q, et al. Metagenome-wide association of gut microbiome features for schizophrenia. Nat Commun. 2020;11(1):1612. doi:10.1038/s41467-020-15457-9.
  • Mosaferi B, Jand Y, Salari A-A. Gut microbiota depletion from early adolescence alters anxiety and depression-related behaviours in male mice with Alzheimer-like disease. Sci Rep. 2021;11(1):22941. doi:10.1038/s41598-021-02231-0.
  • Slykerman RF, Kang J, Van Zyl N, Barthow C, Wickens K, Stanley T, et al. Effect of early probiotic supplementation on childhood cognition, behaviour and mood a randomised, placebo-controlled trial. Acta Paediatr. 2018 Dec;107(12):2172–8. doi:10.1111/apa.14590.
  • Halverson T, Alagiakrishnan K. Gut microbes in neurocognitive and mental health disorders. Ann Med. 2020;52(8):423–43. doi:10.1080/07853890.2020.1808239.
  • Fouquier J, Huizar NM, Donnelly J, Moreno Huizar N, Glickman C, Kang D-W, et al. The gut microbiome in autism: study-site effects and longitudinal analysis of behavior change. mSystems. 2021;6(2):e00848–20.
  • Yap CX, Henders AK, Alvares GA, Wood DLA, Krause L, Tyson GW, et al. Autism-related dietary preferences mediate autism-gut microbiome associations. Cell. 2021;184(24):5916–31. doi:10.1016/j.cell.2021.10.015.
  • Alcock J, Maley CC, Aktipis CA. Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms. Bioessays. 2014 Oct;36(10):940–9. doi:10.1002/bies.201400071.
  • de Wouters d’Oplinter A, Rastelli M, Van Hul M, Delzenne NM, Cani PD, Everard A. Gut microbes participate in food preference alterations during obesity. Gut Microbes. 2021;13(1):1959242. doi:10.1080/19490976.2021.1959242.
  • Fetissov SO. Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour. Nat Rev Endocrinol. 2017 Jan;13(1):11–25. doi:10.1038/nrendo.2016.150.
  • Han H, Yi B, Zhong R, Wang M, Zhang S, Ma J, et al. From gut microbiota to host appetite: gut microbiota-derived metabolites as key regulators. Microbiome. 2021 Jul 20;9(1):162. doi:10.1186/s40168-021-01093-y.
  • Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012 Oct;13(10):701–12. doi:10.1038/nrn3346.
  • Sherwin E, Bordenstein SR, Quinn JL, Dinan TG, Cryan JF. Microbiota and the social brain. Science. 2019;366(6465):eaar2016. doi:10.1126/science.aar2016.
  • Asnicar F, Berry SE, Valdes AM, Nguyen LH, Piccinno G, Drew DA, et al. Microbiome connections with host metabolism and habitual diet from 1,098 deeply phenotyped individuals. Nat Med. 2021;27(2):321–32. doi:10.1038/s41591-020-01183-8.
  • Bolte LA, Vich Vila A, Imhann F, Collij V, Gacesa R, Peters V, et al. Long-term dietary patterns are associated with pro-inflammatory and anti-inflammatory features of the gut microbiome. Gut. 2021;70(7):1287–98. doi:10.1136/gutjnl-2020-322670.
  • Shikany JM, Demmer RT, Johnson AJ, Fino NF, Meyer K, Ensrud KE, et al. Association of dietary patterns with the gut microbiota in older, community-dwelling men. Am J Clin Nutr. 2019;110(4):1003–14. doi:10.1093/ajcn/nqz174.
  • Wastyk HC, Fragiadakis GK, Perelman D, Dahan D, Merrill BD, Yu FB, et al. Gut-microbiota-targeted diets modulate human immune status. Cell. 2021;184(16):4137–53. doi:10.1016/j.cell.2021.06.019.
  • Cotillard A, Cartier-Meheust A, Litwin NS, Chaumont S, Saccareau M, Lejzerowicz F, et al. A posteriori dietary patterns better explain variations of the gut microbiome than individual markers in the American gut project. Am J Clin Nutr. 2021;115(2):432–43. doi:10.1093/ajcn/nqab332.
  • Schverer M, O'Mahony SM, O’Riordan KJ, Donoso F, Roy BL, Stanton C, et al. Dietary phospholipids: role in cognitive processes across the lifespan. Neurosci Biobehav Rev. 2020;111:183–93. doi:10.1016/j.neubiorev.2020.01.012.
  • Macpherson AJ, de Agüero MG, Ganal-Vonarburg SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017 Aug;17(8):508–17. doi:10.1038/nri.2017.58.
  • Armet AM, Deehan EC, O'Sullivan AF, O’Sullivan AF, Mota JF, Field CJ, et al. Rethinking healthy eating in light of the gut microbiome. Cell Host Microbe. 2022 Jun 8;30(6):764–85. doi:10.1016/j.chom.2022.04.016.
  • Bhattarai S, Janaswamy S. The nexus of gut microbiota, diet, and health. Funct Food Sci. 2022;2(2). doi:10.31989/ffs.v2i2.885
  • Uzbay T. Germ-free animal experiments in the gut microbiota studies. Curr Opin Pharmacol. 2019 Dec;49:6–10. doi:10.1016/j.coph.2019.03.016.
  • Forgie AJ, Drall KM, Bourque SL, Field CJ, Kozyrskyj AL, Willing BP. The impact of maternal and early life malnutrition on health: a diet-microbe perspective. BMC Med. 2020;18(1):135. doi:10.1186/s12916-020-01584-z.
  • Sarkar A, Yoo JY, Valeria Ozorio Dutra S, Morgan KH, Groer M. The association between early-life gut microbiota and long-term health and diseases. J Clin Med. 2021;10(3):459. doi:10.3390/jcm10030459.
  • Kang SS, Kurti A, Fair DA, Fryer JD. Dietary intervention rescues maternal obesity induced behavior deficits and neuroinflammation in offspring. J Neuroinflammation. 2014 Sep 12;11:156. doi:10.1186/s12974-014-0156-9.
  • Mitchell AJ, Dunn GA, Sullivan EL. The influence of maternal metabolic state and nutrition on offspring neurobehavioral development: A focus on preclinical models. Biol Psychiatry: Cognit Neurosci Neuroimag. 2021. doi:10.1016/j.bpsc.2021.11.014.
  • McDonnell L, Gilkes A, Ashworth M, Rowland V, Harries TH, Armstrong D, White P. Association between antibiotics and gut microbiome dysbiosis in children: systematic review and meta-analysis. Gut Microbes. 2021 Jan-Dec;13(1):1–18. doi:10.1080/19490976.2020.1870402.
  • Ramirez J, Guarner F, Bustos Fernandez L, Maruy A, Sdepanian VL, Cohen H. Antibiotics as major disruptors of Gut microbiota. Front Cell Infect Microbiol. 2020;10:572912. doi:10.3389/fcimb.2020.572912.
  • Vuong HE, Yano JM, Fung TC, Hsiao EY. The microbiome and host behavior. Annu Rev Neurosci. 2017;40(1):21–49. doi:10.1146/annurev-neuro-072116-031347.
  • Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013. doi:10.1152/physrev.00018.2018.
  • Guirro M, Costa A, Gual-Grau A, Herrero P, Torrell H, Canela N, Arola L. Effects from diet-induced gut microbiota dysbiosis and obesity can be ameliorated by fecal microbiota transplantation: A multiomics approach. PLoS One. 2019;14(9):e0218143.
  • Weingarden AR, Vaughn BP. Intestinal microbiota, fecal microbiota transplantation, and inflammatory bowel disease. Gut Microbes. 2017 May 4;8(3):238–52.
  • Parker A, Romano S, Ansorge R, Aboelnour A, Le Gall G, Savva GM, et al. Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain. Microbiome. 2022;10(1):68. doi:10.1186/s40168-022-01243-w.
  • Berer K, Gerdes LA, Cekanaviciute E, Jia X, Xiao L, Xia Z, et al. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc Natl Acad Sci USA. 2017;114(40):10719–24. doi:10.1073/pnas.1711233114.
  • Kang D-W, Adams JB, Gregory AC, Borody T, Chittick L, Fasano A, et al. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: an open-label study. Microbiome. 2017;5(1):10. doi:10.1186/s40168-016-0225-7.
  • Kelly JR, Borre Y, O' Brien C, Patterson E, El Aidy S, Deane J, et al. Transferring the blues: depression-associated gut microbiota induces neurobehavioural changes in the rat. J Psychiatr Res. 2016 Nov;82:109–18. doi:10.1016/j.jpsychires.2016.07.019.
  • Sun J, Xu J, Ling Y, Wang F, Gong T, Yang C, et al. Fecal microbiota transplantation alleviated Alzheimer’s disease-like pathogenesis in APP/PS1 transgenic mice. Transl Psychiatry. 2019;9(1):189. doi:10.1038/s41398-019-0525-3.
  • Sun MF, Zhu YL, Zhou ZL, Jia X-B, Xu Y-D, Yang Q, et al. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson's disease mice: gut microbiota, glial reaction and TLR4/TNF-α signaling pathway. Brain Behav Immun. 2018 May;70:48–60. doi:10.1016/j.bbi.2018.02.005.
  • Zhu F, Guo R, Wang W, Ju Y, Ma Q, Sun Q, et al. Transplantation of microbiota from drug-free patients with schizophrenia causes schizophrenia-like abnormal behaviors and dysregulated kynurenine metabolism in mice. Mol Psychiatry. 2020 Nov;25(11):2905–18. doi:10.1038/s41380-019-0475-4.
  • Vendrik KEW, Ooijevaar RE, de Jong PRC, Laman JD, van Oosten BW, van Hilten JJ, et al. Fecal microbiota transplantation in neurological disorders. Front Cell Infect Microbiol. 2020;10:98. doi:10.3389/fcimb.2020.00098.
  • Xu HM, Huang HL, Zhou YL, Zhao H-L, Shou D-W, Liu Y-D, Nie Y-Q. Fecal microbiota transplantation: A new therapeutic attempt from the gut to the brain. Gastroenterol Res Pract. 2021;2021:1–20. doi:10.1155/2021/6699268.
  • Kang D-W, Adams JB, Coleman DM, Pollard EL, Maldonado J, McDonough-Means S, et al. Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota. Sci Rep. 2019;9(1):5821. doi:10.1038/s41598-019-42183-0.
  • Martin S, Battistini C, Sun J. A gut feeling in amyotrophic lateral sclerosis: microbiome of mice and men [review]. Front Cell Infect Microbiol. 2022;12; doi:10.3389/fcimb.2022.839526.English.
  • Gheorghe CE, Ritz NL, Martin JA, Wardill HR, Cryan JF, Clarke G. Investigating causality with fecal microbiota transplantation in rodents: applications, recommendations and pitfalls. Gut Microbes. 2021;13(1):1941711. doi:10.1080/19490976.2021.1941711.
  • Blacher E, Bashiardes S, Shapiro H, Rothschild D, Mor U, Dori-Bachash M, et al. Potential roles of gut microbiome and metabolites in modulating ALS in mice. Nature. 2019 Aug;572(7770):474–80. doi:10.1038/s41586-019-1443-5.
  • Fang P, Kazmi SA, Jameson KG, Hsiao EY. The microbiome as a modifier of neurodegenerative disease risk. Cell Host Microbe. 2020 Aug 12;28(2):201–22. doi:10.1016/j.chom.2020.06.008.
  • Hsiao Elaine Y, Sara W M, Hsien S, McBride SW, Sharon G, Hyde ER, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155(7):1451–63. doi:10.1016/j.cell.2013.11.024.
  • Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell. 2016;165(7):1762–75. doi:10.1016/j.cell.2016.06.001.
  • Depommier C, Everard A, Druart C, Plovier H, Van Hul M, Vieira-Silva S, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med. 2019 Jul;25(7):1096–103. doi:10.1038/s41591-019-0495-2.
  • Zhou Q, Zhang Y, Wang X, Yang R, Zhu X, Chen C, et al. Gut bacteria Akkermansia is associated with reduced risk of obesity: evidence from the American gut Project. Nutr Metab (Lond). 2020;17(1):90. doi:10.1186/s12986-020-00516-1.
  • Ding Y, Bu F, Chen T, Shi G, Yuan X, Feng Z, et al. A next-generation probiotic: Akkermansia muciniphila ameliorates chronic stress-induced depressive-like behavior in mice by regulating gut microbiota and metabolites. Appl Microbiol Biotechnol. 2021 Nov;105(21-22):8411–26.
  • Marx W, Lane M, Hockey M, Aslam H, Berk M, Walder K, et al. Diet and depression: exploring the biological mechanisms of action. Mol Psychiatry. 2021;26(1):134–50. doi:10.1038/s41380-020-00925-x.
  • Nikolova VL, Hall MRB, Hall LJ, Cleare AJ, Stone JM, Young AH. Perturbations in gut microbiota composition in psychiatric disorders: A review and meta-analysis. JAMA Psychiatry. 2021;78(12):1343–54. doi:10.1001/jamapsychiatry.2021.2573.
  • Jacka FN, O'Neil A, Opie R, O’Neil A, Itsiopoulos C, Cotton S, et al. A randomised controlled trial of dietary improvement for adults with major depression (the ‘SMILES’ trial). BMC Med. 2017;15(1):23–23. doi:10.1186/s12916-017-0791-y.
  • Ghosh TS, Rampelli S, Jeffery IB, Santoro A, Neto M, Capri M, et al. Mediterranean diet intervention alters the gut microbiome in older people reducing frailty and improving health status: the NU-AGE 1-year dietary intervention across five European countries. Gut. 2020;69(7):1218–28. doi:10.1136/gutjnl-2019-319654.
  • Dong TS, Mayer EA, Osadchiy V, Chang C, Katzka W, Lagishetty V, et al. A distinct brain-gut-microbiome profile exists for females with obesity and food addiction. Obesity (Silver Spring, Md). 2020 Aug;28(8):1477–86.
  • Marx W, Scholey A, Firth J, D’Cunha NM, Lane M, Hockey M, et al. Prebiotics, probiotics, fermented foods and cognitive outcomes: A meta-analysis of randomized controlled trials. Neurosci Biobehav Rev. 2020;118:472–84.
  • Hiel S, Gianfrancesco MA, Rodriguez J, Portheault D, Leyrolle Q, Bindels LB, et al. Link between gut microbiota and health outcomes in inulin -treated obese patients: lessons from the Food4Gut multicenter randomized placebo-controlled trial. Clin Nutr. 2020;39(12):3618–28. doi:10.1016/j.clnu.2020.04.005.
  • Stewart Campbell A, Needham BD, Meyer CR, Tan J, Conrad M, Preston GM, et al. Safety and target engagement of an oral small-molecule sequestrant in adolescents with autism spectrum disorder: an open-label phase 1b/2a trial. Nat Med. 2022 Mar;28(3):528–34. doi:10.1038/s41591-022-01683-9.
  • Berding K, Long-Smith CM, Carbia C, Bastiaanssen TFS, van de Wouw M, Wiley N, et al. A specific dietary fibre supplementation improves cognitive performance-an exploratory randomised, placebo-controlled, crossover study. Psychopharmacology (Berl). 2021 Jan;238(1):149–63. doi:10.1007/s00213-020-05665-y.
  • Dalile B, Vervliet B, Bergonzelli G, Verbeke K, Van Oudenhove L. Colon-delivered short-chain fatty acids attenuate the cortisol response to psychosocial stress in healthy men: a randomized, placebo-controlled trial. Neuropsychopharmacology. 2020 Dec;45(13):2257–66. doi:10.1038/s41386-020-0732-x.
  • Allen AP, Hutch W, Borre YE, Kennedy PJ, Temko A, Boylan G, et al. Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl Psychiatry. 2016;6(11):e939–e939. doi:10.1038/tp.2016.191.
  • Wang H, Braun C, Murphy EF, Enck P. Bifidobacterium longum 1714™ strain modulates brain activity of healthy volunteers during social stress. Am J Gastroenterol. 2019 Jul;114(7):1152–62. doi:10.14309/ajg.0000000000000203.
  • Jacka FN, Kremer PJ, Leslie ER, Berk M, Patton GC, Toumbourou JW, Williams JW. Associations between diet quality and depressed mood in adolescents: results from the Australian Healthy Neighbourhoods Study. Aust N Z J Psychiatry. 2010 May;44(5):435–42. doi:10.3109/00048670903571598.
  • Darch HT, Collins MK, O’Riordan KJ, Cryan JF. Microbial memories: sex-dependent impact of the gut microbiome on hippocampal plasticity. Eur J Neurosci. 2021;54(4):5235–44. doi:10.1111/ejn.15119.
  • Luczynski P, McVey Neufeld KA, Oriach CS, Clarke G, Dinan TG, Cryan JF. Growing up in a bubble: using germ-free animals to assess the influence of the gut microbiota on brain and behavior. Int J Neuropsychopharmacol. 2016 Aug;19(8):pyw020. doi:10.1093/ijnp/pyw020.
  • Legan TB, Lavoie B, Mawe GM. Direct and indirect mechanisms by which the gut microbiota influence host serotonin systems. Neurogastroenterol Motil. 2022 Mar 5: e14346. doi:10.1111/nmo.14346.
  • Duranti S, Ruiz L, Lugli GA, Tames H, Milani C, Mancabelli L, et al. Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA. Sci Rep. 2020 Aug 24;10(1):14112. doi:10.1038/s41598-020-70986-z.
  • Caso JR, MacDowell KS, González-Pinto A, García S, de Diego-Adeliño J, Carceller-Sindreu M, et al. Gut microbiota, innate immune pathways, and inflammatory control mechanisms in patients with major depressive disorder. Transl Psychiatry. 2021;11(1):645. doi:10.1038/s41398-021-01755-3.
  • Tang AT, Choi JP, Kotzin JJ, Yang Y, Hong CC, Hobson N, et al. Endothelial TLR4 and the microbiome drive cerebral cavernous malformations. Nature. 2017 May 18;545(7654):305–10. doi:10.1038/nature22075.
  • O'Riordan KJ, Collins MK, Moloney GM, Knox EG, Aburto MR, Fülling C, et al. Short chain fatty acids: microbial metabolites for gut-brain axis signalling. Mol Cell Endocrinol. 2022 Jan 20;546:111572. doi:10.1016/j.mce.2022.111572.
  • Yang W, Cong Y. Gut microbiota-derived metabolites in the regulation of host immune responses and immune-related inflammatory diseases. Cell Mol Immunol. 2021 Apr;18(4):866–77. doi:10.1038/s41423-021-00661-4.
  • Ntranos A, Park H-J, Wentling M, Tolstikov V, Amatruda M, Inbar B, et al. Bacterial neurotoxic metabolites in multiple sclerosis cerebrospinal fluid and plasma. Brain. 2021;145(2):569–83. doi:10.1093/brain/awab320.
  • Park J, Kim CH. Regulation of common neurological disorders by gut microbial metabolites. Exp Mol Med. 2021;53(12):1821–33. doi:10.1038/s12276-021-00703-x.
  • Shimizu H, Masujima Y, Ushiroda C, Mizushima R, Taira S, Ohue-Kitano R, Kimura I. Dietary short-chain fatty acid intake improves the hepatic metabolic condition via FFAR3. Sci Rep. 2019;9(1):16574. doi:10.1038/s41598-019-53242-x.
  • He J, Zhang P, Shen L, Niu L, Tan Y, Chen L, et al. Short-Chain fatty acids and their association with signalling pathways in inflammation, glucose and lipid metabolism. Int J Mol Sci. 2020;21(17):6356. doi:10.3390/ijms21176356.
  • Leeuwendaal NK, Cryan JF, Schellekens H. Gut peptides and the microbiome: focus on ghrelin. Curr Opin Endocrinol Diabetes Obes. 2021 Apr 1;28(2):243–52. doi:10.1097/med.0000000000000616.
  • O'Sullivan E, Barrett E, Grenham S, Fitzgerald P, Stanton C, Ross R, et al. BDNF expression in the hippocampus of maternally separated rats: does Bifidobacterium breve 6330 alter BDNF levels? Benef Microbes. 2011 Sep;2(3):199–207. doi:10.3920/bm2011.0015.
  • Distrutti E, O'Reilly JA, McDonald C, O’Reilly J-A, Cipriani S, Renga B, et al. Modulation of intestinal microbiota by the probiotic VSL#3 resets brain gene expression and ameliorates the age-related deficit in LTP. PLoS One. 2014;9(9):e106503. doi:10.1371/journal.pone.0106503.
  • Agus A, Clément K, Sokol H. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut. 2021;70(6):1174–82. doi:10.1136/gutjnl-2020-323071.
  • Krautkramer KA, Fan J, Bäckhed F. Gut microbial metabolites as multi-kingdom intermediates. Nat Rev Microbiol. 2021;19(2):77–94. doi:10.1038/s41579-020-0438-4.
  • O’Donnell MP, Fox BW, Chao P-H, Schroeder FC, Sengupta P. A neurotransmitter produced by gut bacteria modulates host sensory behaviour. Nature. 2020;583(7816):415–20. doi:10.1038/s41586-020-2395-5.
  • Needham BD, Funabashi M, Adame MD, Wang Z, Boktor JC, Haney J, et al. A gut-derived metabolite alters brain activity and anxiety behaviour in mice. Nature. 2022 Feb;602(7898):647–53. doi:10.1038/s41586-022-04396-8.
  • Logsdon AF, Erickson MA, Rhea EM, Salameh TS, Banks WA. Gut reactions: how the blood-brain barrier connects the microbiome and the brain. Exp Biol Med (Maywood). 2018 Jan;243(2):159–65. doi:10.1177/1535370217743766.
  • Coureuil M, Lécuyer H, Bourdoulous S, Nassif X. A journey into the brain: insight into how bacterial pathogens cross blood-brain barriers. Nat Rev Microbiol. 2017 Mar;15(3):149–59. doi:10.1038/nrmicro.2016.178.
  • Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 2014;6(263):263ra158–263ra158. doi:10.1126/scitranslmed.3009759.
  • Kelly CR, Yen EF, Grinspan AM, Kahn SA, Atreja A, Lewis JD, et al. Fecal microbiota transplantation is highly effective in real-world practice: initial results from the FMT National Registry. Gastroenterology. 2021 Jan;160(1):183–92. doi:10.1053/j.gastro.2020.09.038.
  • Cryan JF, Mazmanian SK. Microbiota-brain axis: context and causality. Science. 2022 May 27;376(6596):938–9. doi:10.1126/science.abo4442.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.