The microbiota–gut–brain axis and neurodevelopmental disorders

Qinwen Wang , Qianyue Yang , Xingyin Liu

Protein Cell ›› 2023, Vol. 14 ›› Issue (10) : 762 -775.

PDF (1447KB)
Protein Cell ›› 2023, Vol. 14 ›› Issue (10) : 762 -775. DOI: 10.1093/procel/pwad026
REVIEW
REVIEW

The microbiota–gut–brain axis and neurodevelopmental disorders

Author information +
History +
PDF (1447KB)

Abstract

The gut microbiota has been found to interact with the brain through the microbiota–gut–brain axis, regulating various physiological processes. In recent years, the impacts of the gut microbiota on neurodevelopment through this axis have been increasingly appreciated. The gut microbiota is commonly considered to regulate neurodevelopment through three pathways, the immune pathway, the neuronal pathway, and the endocrine/systemic pathway, with overlaps and crosstalks in between. Accumulating studies have identified the role of the microbiota–gut–brain axis in neurodevelopmental disorders including autism spectrum disorder, attention deficit hyperactivity disorder, and Rett Syndrome. Numerous researchers have examined the physiological and pathophysiological mechanisms influenced by the gut microbiota in neurodevelopmental disorders (NDDs). This review aims to provide a comprehensive overview of advancements in research pertaining to the microbiota-gut-brain axis in NDDs. Furthermore, we analyzed both the current state of research progress and discuss future perspectives in this field.

Keywords

neurodevelopmental disorders / gut microbiome / microbiota / gut / brain axis

Cite this article

Download citation ▾
Qinwen Wang, Qianyue Yang, Xingyin Liu. The microbiota–gut–brain axis and neurodevelopmental disorders. Protein Cell, 2023, 14(10): 762-775 DOI:10.1093/procel/pwad026

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Aarts E, Ederveen THA, Naaijen J et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS One 2017a;12:e0183509.

[2]

Aarts E, Ederveen THA, Naaijen J et al. Gut microbiome in ADHD and its relation to neural reward anticipation. PLoS One 2017b;12:e0183509.

[3]

Agirman G, Hsiao EY. SnapShot: the microbiota-gut-brain axis. Cell 2021;184:2524–2524.e1.

[4]

Agustí A, García-Pardo MP, López-Almela I et al. Interplay between the gut-brain axis, obesity and cognitive function. Front Neurosci 2018;12:155.

[5]

Alemi F, Poole DP, Chiu J et al. The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology 2013;144:145–154.

[6]

American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th edn. Washington D.C.: American Psychiatric Association, 2013.

[7]

Arentsen T, Qian Y, Gkotzis S et al. The bacterial peptidoglycan-sensing molecule Pglyrp2 modulates brain development and behavior. Mol Psychiatry 2017;22:257–266.

[8]

Ashwood P, Krakowiak P, Hertz-Picciotto I et al. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav Immun 2011;25:40–45.

[9]

Bellono NW, Bayrer JR, Leitch DB et al. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 2017;170:185–198.e16.

[10]

Bercik P, Denou E, Collins J et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology 2011;141:599–609.e1.

[11]

Berer K, Mues M, Koutrolos M et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011;479:538–541.

[12]

Bhattarai Y, Williams BB, Battaglioli EJ et al. Gut microbiota-produced tryptamine activates an epithelial G-protein-coupled receptor to increase colonic secretion. Cell Host Microbe 2018;23:775–785.e5.

[13]

Biagi E, Candela M, Centanni M et al. Gut microbiome in down syndrome. PLoS One 2014;9:e112023.

[14]

Bohórquez DV, Shahid RA, Erdmann A et al. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J Clin Invest 2015;125:782–786.

[15]

Bonaz B, Bazin T, Pellissier S. Bhattarai. Front Neurosci 2018;12:49.

[16]

Bonnefil V, Dietz K, Amatruda M et al. Region-specific myelin differences define behavioral consequences of chronic social defeat stress in mice. Elife 2019;8:e40855.

[17]

Borghi E, Borgo F, Severgnini M et al. Rett syndrome: a focus on gut microbiota. Int J Mol Sci 2017;18:344–344.

[18]

Borgmann D, Ciglieri E, Biglari N et al. Gut-brain communication by distinct sensory neurons differently controls feeding and glucose metabolism. Cell Metab 2021;33:1466–1482.e7.

[19]

Borgo F, Severgnini M, Savini M et al. Rett syndrome: a focus on gut microbiota. IJMS 2017;18:344.

[20]

Bravo JA, Forsythe P, Chew MV et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011a;108:16050–16055.

[21]

Bravo JA, Forsythe P, Chew MV et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011b;108:16050–16055.

[22]

Brescia P, Rescigno M. The gut vascular barrier: a new player in the gut–liver–brain axis. Trends Mol Med 2021;27:844–855.

[23]

Brown GC, Neher JJ. Microglial phagocytosis of live neurons. Nat Rev Neurosci 2014;15:209–216.

[24]

Browning KN, Travagli RA. Central nervous system control of gastro-intestinal motility and secretion and modulation of gastrointestinal functions. In: Terjung R (ed.), Comprehensive Physiology, 1st edn. Wiley, 2014, 1339–1368.

[25]

Bruckner JJ, Stednitz SJ, Grice MZ et al. The microbiota promotes social behavior by modulating microglial remodeling of forebrain neurons. PLoS Biol 2022;20:e3001838.

[26]

Buchanan KL, Rupprecht LE, Kaelberer MM et al. The preference for sugar over sweetener depends on a gut sensor cell. Nat Neurosci 2022;25:191–200.

[27]

Buffington SA, Di Prisco GV, Auchtung TA et al. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell 2016;165:1762–1775.

[28]

Buffington SA, Dooling SW, Sgritta M et al. Dissecting the contribution of host genetics and the microbiome in complex behaviors. Cell 2021;184:1740–1756.e16.

[29]

Burnham PM, Hendrixson DR. Campylobacter jejuni: collective components promoting a successful enteric lifestyle. Nat Rev Microbiol 2018;16:551–565.

[30]

Chambers AP, Sandoval DA, Seeley RJ. Integration of satiety signals by the central nervous system. Curr Biol 2013;23:R379–R388.

[31]

Chang L, Wei Y, Hashimoto K. Brain–gut–microbiota axis in depression: a historical overview and future directions. Brain Res Bull 2022;182:44–56.

[32]

Chang PV, Hao L, Offermanns S et al. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA 2014;111:2247–2252.

[33]

Checa-Ros A, Jeréz-Calero A, Molina-Carballo A et al. Current evidence on the role of the gut microbiome in ADHD pathophysiology and therapeutic implications. Nutrients 2021;13:249.

[34]

Chen G, Ran X, Li B et al. Sodium butyrate inhibits inflammation and maintains epithelium barrier integrity in a TNBS-induced inflammatory bowel disease mice model. EBioMedicine 2018;30:317–325.

[35]

Chen K, Luan X, Liu Q et al. Drosophila Histone Demethylase KDM5 Regulates Social Behavior through Immune Control and Gut Microbiota Maintenance. Cell Host & Microbe 2019;25(4):537–552.e8.

[36]

Choi GB, Yim YS, Wong H et al. The maternal interleukin-17a path-way in mice promotes autism-like phenotypes in offspring. Science 2016;351:933–939.

[37]

Chugani DC, Muzik O, Behen M et al. Developmental changes in brain serotonin synthesis capacity in autistic and nonautistic children. Ann Neurol 1999;45:287–295.

[38]

Corrêa-Oliveira R, Fachi JL, Vieira A et al. Regulation of immune cell function by short-chain fatty acids. Clin Trans Immunol 2016;5:e73.

[39]

Cryan JF, O’Riordan KJ, Cowan CSM et al. The microbiota-gut-brain axis. Physiol Rev 2019;99:1877–2013.

[40]

Cunningham CL, Martinez-Cerdeno V, Noctor SC. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J Neurosci 2013;33:4216–4233.

[41]

Cussotto S, Sandhu KV, Dinan TG et al. The neuroendocrinology of the microbiota-gut-brain axis: a behavioural perspective. Front Neuroendocrinol 2018;51:80–101.

[42]

Dalile B, Van Oudenhove L, Vervliet B et al. The role of short-chain fatty acids in microbiota–gut–brain communication. Nat Rev Gastroenterol Hepatol 2019;16:461–478.

[43]

Davenport ER, Sanders JG, Song SJ et al. The human microbiome in evolution. BMC Biol 2017;15:127.

[44]

Dayanithi G, Cazalis M, Nordmann JJ. Relaxin affects the release of oxytocin and vasopressin from the neurohypophysis. Nature 1987;325:813–816.

[45]

de Theije CGM, Wopereis H, Ramadan M et al. Altered gut microbiota and activity in a murine model of autism spectrum disorders. Brain Behav Immun 2014;37:197–206.

[46]

Dervola KS, Roberg BA, Wøien G et al. Marine omega-3 polyunsaturated fatty acids induce sex-specific changes in reinforcer- controlled behaviour and neurotransmitter metabolism in a spontaneously hypertensive rat model of ADHD. Behav Brain Funct 2012;8:56.

[47]

Dinan TG, Cryan JF. Brain–gut–microbiota axis — mood, metabolism and behaviour. Nat Rev Gastroenterol Hepatol 2017;14:69–70.

[48]

Dölen G, Darvishzadeh A, Huang KW et al. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 2013;501:179–184.

[49]

Donovan MH, Tecott LH. Serotonin and the regulation of mammalian energy balance. Front Neurosci 2013;7:36–36.

[50]

Enticott PG, Rinehart NJ, Tonge BJ et al. A preliminary transcranial magnetic stimulation study of cortical inhibition and excitability in high-functioning autism and Asperger disorder: TMS in Austism and Asperger Disorder. Develop Med Child Neurol 2010;52:e179–e183.

[51]

Erny D, Dokalis N, Mezö C et al. Microbiota-derived acetate enables the metabolic fitness of the brain innate immune system during health and disease. Cell Metab 2021;33:2260–2276.e7.

[52]

Erny D, Hrabě de Angelis AL, Prinz M. Communicating systems in the body: how microbiota and microglia cooperate. Immunology 2017;150:7–15.

[53]

Fasano A. All disease begins in the (leaky) gut: role of zonulin-mediated gut permeability in the pathogenesis of some chronic inflammatory diseases. F1000Res 2020;9:69.

[54]

Fattorusso A, Di Genova L, Dell’Isola G et al. Autism spectrum disorders and the gut microbiota. Nutrients 2019;11:521.

[55]

Fineberg SK, Ross DA. Oxytocin and the social brain. Biol Psychiatry 2017;81:e19–e21.

[56]

Fitzpatrick Z, Frazer G, Ferro A et al. Gut-educated IgA plasma cells defend the meningeal venous sinuses. Nature 2020;587:472–476.

[57]

Francis AP, Dominguez-Bello MG. Early-life microbiota perturbations and behavioral effects. Trends Microbiol 2019;27:567–569.

[58]

Fung TC, Olson CA, Hsiao EY. Interactions between the microbiota, immune and nervous systems in health and disease. Nat Neurosci 2017;20:145–155.

[59]

Gao J, Zou J, Yang L et al. Alteration of peripheral cortisol and autism spectrum disorder: a meta-analysis. Front Psychiatry 2022a;13:928188.

[60]

Gao X, Su X, Han X et al. Unsaturated fatty acids in mental disorders: an umbrella review of meta-analyses. Adv Nutr 2022b;13:2217–2236.

[61]

Garlanda C, Dinarello CA, Mantovani A. The Interleukin-1 family: back to the future. Immunity 2013;39:1003–1018.

[62]

George Kerry R, Patra JK, Gouda S et al. Benefaction of probiotics for human health: a review. J Food Drug Anal 2018;26:927–939.

[63]

Gilbert JA, Krajmalnik-Brown R, Porazinska DL et al. Toward effective probiotics for autism and other neurodevelopmental disorders. Cell 2013;155:1446–1448.

[64]

Goehler LE, Gaykema RPA, Opitz N et al. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 2005;19:334–344.

[65]

Gonzalez-Santana A, Diaz Heijtz R. Bacterial peptidoglycans from microbiota in neurodevelopment and behavior. Trends Mol Med 2020;26:729–743.

[66]

Gray H, Standring S, Anhand N (eds). Gray’s anatomy: the anatomical basis of clinical practice, 42nd edn, Amsterdam: Elsevier, 2021.

[67]

Gribble FM, Reimann F. Enteroendocrine cells: chemosensors in the intestinal epithelium. Annu Rev Physiol 2016;78:277–299.

[68]

Grimaldi R, Gibson GR, Vulevic J et al. A prebiotic intervention study in children with autism spectrum disorders (ASDs). Microbiome 2018;6:133.

[69]

Han VX, Patel S, Jones HF et al. Maternal immune activation and neuroinflammation in human neurodevelopmental disorders. Nat Rev Neurol 2021;17:564–579.

[70]

Hang S, Paik D, Yao L et al. Bile acid metabolites control TH17 and Treg cell differentiation. Nature 2019;576:143–148.

[71]

Hanley HG, Stahl SM, Freedman DX. Hyperserotonemia and amine metabolites in autistic and retarded children. Arch Gen Psychiatry 1977;34:521–531.

[72]

Harry GJ. Microglia during development and aging. Pharmacol Ther 2013;139:313–326.

[73]

Hartsough LA, Park M, Kotlajich MV et al. Optogenetic control of gut bacterial metabolism to promote longevity. Elife 2020;9:e56849.

[74]

Heinrichs M, von Dawans B, Domes G. Oxytocin, vasopressin, and human social behavior. Front Neuroendocrinol 2009;30:548–557.

[75]

Hisle-Gorman E, Susi A, Stokes T et al. Prenatal, perinatal, and neonatal risk factors of autism spectrum disorder. Pediatr Res 2018;84:190–198.

[76]

Hoban AE, Stilling RM, Ryan FJ et al. Regulation of prefrontal cortex myelination by the microbiota. Transl Psychiatry 2016;6:e774.

[77]

Hoogenraad CC, Riol-Blanco L. Interleukin-17: a social cytokine. Cell 2020;181:517–519.

[78]

Hsiao EY, McBride SW, Hsien S et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 2013;155:1451–1463.

[79]

Hsueh B, Chen R, Jo Y et al. Cardiogenic control of affective behavioural state. Nature 2023.

[80]

Hughes AN, Appel B. Microglia phagocytose myelin sheaths to modify developmental myelination. Nat Neurosci 2020;23:1055–1066.

[81]

Ichiki T, Wang T, Kennedy A et al. Sensory representation and detection mechanisms of gut osmolality change. Nature 2022;602:468–474.

[82]

Isolauri E, Kalliomaki M, Laitinen K et al. Modulation of the maturing gut barrier and microbiota: a novel target in allergic disease. CPD 2008;14:1368–1375.

[83]

Jiang H, Zhou Y, Zhou G et al. Gut microbiota profiles in treatment-naïve children with attention deficit hyperactivity disorder. Behav Brain Res 2018;347:408–413.

[84]

Jolanta Wasilewska J, Klukowski M. Gastrointestinal symptoms and autism spectrum disorder: links and risks – a possible new overlap syndrome. PHMT 2015;153.

[85]

Kaelberer MM, Buchanan KL, Klein ME et al. A gut-brain neural circuit for nutrient sensory transduction. Science 2018;361:eaat5236.

[86]

Kaelberer MM, Rupprecht LE, Liu WW et al. Neuropod cells: the emerging biology of gut-brain sensory transduction. Annu Rev Neurosci 2020;43:337–353.

[87]

Kalenik A, Kardaś K, Rahnama A et al. Gut microbiota and probiotic therapy in ADHD: a review of current knowledge. Prog Neuropsychopharmacol Biol Psychiatry 2021;110:110277.

[88]

Kang D-W, Adams JB, Coleman DM et al. Long-term benefit of Microbiota Transfer Therapy on autism symptoms and gut microbiota. Sci Rep 2019;9:5821.

[89]

Kidd M, Gustafsson BI, Drozdov I et al. IL1β- and LPS-induced serotonin secretion is increased in EC cells derived from Crohn’s disease. Neurogastroenterol Motil 2009;21:439–450.

[90]

Kim M, Heo G, Kim S-Y. Neural signalling of gut mechanosensation in ingestive and digestive processes. Nat Rev Neurosci 2022;23:135–156.

[91]

Kim S, Kim H, Yim YS et al. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature 2017;549:528–532.

[92]

Kong X-J, Liu J, Li J et al. Probiotics and oxytocin nasal spray as neuro- social-behavioral interventions for patients with autism spectrum disorders: a pilot randomized controlled trial protocol. Pilot Feasibility Stud 2020;6:20.

[93]

Krieger J-P, Asker M, van der Velden P et al. Neural pathway for gut feelings: vagal interoceptive feedback from the gastrointestinal tract is a critical modulator of anxiety-like behavior. Biol Psychiatry 2022;92:709–721.

[94]

Lai Z, Shan W, Li J et al. Appropriate exercise level attenuates gut dysbiosis and valeric acid increase to improve neuroplasticity and cognitive function after surgery in mice. Mol Psychiatry 2021;26:7167–7187.

[95]

Lavelle A, Sokol H. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 2020;17:223–237.

[96]

Leader G, Abberton C, Cunningham S et al. Gastrointestinal symptoms in autism spectrum disorder: a systematic review. Nutrients 2022;14:1471.

[97]

Lh M, Hl S, Sk M. The gut microbiota-brain axis in behaviour and brain disorders. Nat Rev Microbiol 2021;19.

[98]

Li D, Sun T, Tong Y et al. Gut-microbiome-expressed 3β-hydroxysteroid dehydrogenase degrades estradiol and is linked to depression in premenopausal females. Cell Metab 2023;S1550413123000530.

[99]

Li M, Tan H-E, Lu Z et al. Gut–brain circuits for fat preference. Nature 2022a;610:722–730.

[100]

Li N, Chen H, Cheng Y et al. Fecal microbiota transplantation relieves gastrointestinal and autism symptoms by improving the gut microbiota in an open-label study. Front Cell Infect Microbiol 2021;11:759435.

[101]

Li X, Wang C, Zhu J et al. Sodium butyrate ameliorates oxidative stress-induced intestinal epithelium barrier injury and mitochondrial damage through AMPK-Mitophagy Pathway. Oxid Med Cell Longevity 2022b;2022:1–23.

[102]

Li Y, Sun H, Huang Y et al. Gut metagenomic characteristics of ADHD reveal low Bacteroides ovatus-associated host cognitive impairment. Gut Microbes 2022c;14:2125747.

[103]

Liu F, Li J, Wu F et al. Altered composition and function of intestinal microbiota in autism spectrum disorders: a systematic review. Transl Psychiatry 2019;9:43.

[104]

Liu L, Wang H, Chen X et al. Gut microbiota and its metabolites in depression: from pathogenesis to treatment. EBioMedicine 2023;90:104527.

[105]

Lou M, Cao A, Jin C et al. Deviated and early unsustainable stunted development of gut microbiota in children with autism spectrum disorder. Gut 2021.

[106]

Lu J, Fan X, Lu L et al. Limosilactobacillus reuteri normalizes blood–brain barrier dysfunction and neurodevelopment deficits associated with prenatal exposure to lipopolysaccharide. Gut Microbes 2023;15:2178800.

[107]

Lukens JR, Eyo UB. Microglia and neurodevelopmental disorders. Annu Rev Neurosci 2022;45:425–445.

[108]

Lyte M, Varcoe J J, Bailey M T. Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation. Physiology & Behavior 2002;65(1):63–68.

[109]

Malik A, Brudvig JM, Gadsden BJ et al. Campylobacter jejuni induces autoimmune peripheral neuropathy via Sialoadhesin and Interleukin-4 axes. Gut Microbes 2022;14:2064706.

[110]

Maniscalco JW, Rinaman L. Vagal interoceptive modulation of motivated behavior. Physiology 2018;33:151–167.

[111]

Margolis KG, Cryan JF, Mayer EA. The microbiota-gut-brain axis: from motility to mood. Gastroenterology 2021;160:1486–1501.

[112]

Marklund U. Diversity, development and immunoregulation of enteric neurons. Nat Rev Gastroenterol Hepatol 2022;19:85–86.

[113]

Maslowski KM, Vieira AT, Ng A et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009;461:1282–1286.

[114]

Matcovitch-Natan O, Winter DR, Giladi A et al. Microglia development follows a stepwise program to regulate brain homeostasis. Science 2016;353:aad8670.

[115]

Mercado-Perez A, Beyder A. Gut feelings: mechanosensing in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 2022;19:283–296.

[116]

Mirabella F, Desiato G, Mancinelli S et al. Prenatal interleukin 6 elevation increases glutamatergic synapse density and disrupts hippocampal connectivity in offspring. Immunity 2021;54:2611–2631.e8.

[117]

Morais LH, Schreiber HL, Mazmanian SK. The gut microbiota–brain axis in behaviour and brain disorders. Nat Rev Microbiol 2021;19:241–255.

[118]

Mossad O, Batut B, Yilmaz B et al. Gut microbiota drives age-related oxidative stress and mitochondrial damage in microglia via the metabolite N6-carboxymethyllysine. Nat Neurosci 2022;25:295–305.

[119]

Müller TD, Finan B, Bloom SR et al. Glucagon-like peptide 1 (GLP-1). Mol Metab 2019;30:72–130.

[120]

Murakami Y, Imamura Y, Saito K et al. Altered kynurenine pathway metabolites in a mouse model of human attention-deficit hyperactivity/autism spectrum disorders: a potential new biological diagnostic marker. Sci Rep 2019;9:13182.

[121]

Needham BD, Adame MD, Serena G et al. Plasma and fecal metabolite profiles in autism spectrum disorder. Biol Psychiatry 2021;89:451–462.

[122]

Needham BD, Funabashi M, Adame MD et al. A gut-derived metabolite alters brain activity and anxiety behaviour in mice. Nature 2022;602:647–653.

[123]

Neier K, Grant TE, Palmer RL et al. Sex disparate gut microbiome and metabolome perturbations precede disease progression in a mouse model of Rett syndrome. Commun Biol 2021;4:1408.

[124]

Nemes-Baran AD, White DR, DeSilva TM. Fractalkine-dependent microglial pruning of viable oligodendrocyte progenitor cells regulates myelination. Cell Rep 2020;32:108047.

[125]

Neufeld KM, Kang N, Bienenstock J et al. Reduced anxiety-like behavior and central neurochemical change in germ-free mice: behavior in germ-free mice. Neurogastroenterol Motil 2011;23:255–e119.

[126]

Neumann ID, Slattery DA. Oxytocin in general anxiety and social fear: a translational approach. Biol Psychiatry 2016;79:213–221.

[127]

Ng SC, Kamm MA, Yeoh YK et al. Scientific frontiers in faecal microbiota transplantation: joint document of Asia-Pacific Association of Gastroenterology (APAGE) and Asia-Pacific Society for Digestive Endoscopy (APSDE). Gut 2020;69:83–91.

[128]

O’Dwyer DN, Dickson RP, Moore BB. The lung microbiome, immunity, and the pathogenesis of chronic lung disease. J Immunol 2016;196:4839–4847.

[129]

Pan S, Mayoral SR, Choi HS et al. Preservation of a remote fear memory requires new myelin formation. Nat Neurosci 2020;23:487–499.

[130]

Pandiyan P, Bhaskaran N, Zou M et al. Microbiome dependent regulation of tregs and Th17 cells in mucosa. Front Immunol 2019;10:426.

[131]

Paolicelli RC, Bolasco G, Pagani F et al. Synaptic pruning by microglia is necessary for normal brain development. Science 2011;333:1456–1458.

[132]

Parrott JM, Redus L, O’Connor JC. Kynurenine metabolic balance is disrupted in the hippocampus following peripheral lipopolysaccharide challenge. J Neuroinflammation 2016;13:124.

[133]

Pärtty A, Kalliomäki M, Wacklin P et al. A possible link between early probiotic intervention and the risk of neuropsychiatric disorders later in childhood: a randomized trial. Pediatr Res 2015;77:823–828.

[134]

Pellegrini C, Antonioli L, Colucci R et al. Interplay among gut microbiota, intestinal mucosal barrier and enteric neuro-immune system: a common path to neurodegenerative diseases? Acta Neuropathol 2018;136:345–361.

[135]

Poling HM, Wu D, Brown N et al. Mechanically induced development and maturation of human intestinal organoids in vivo. Nat Biomed Eng 2018;2:429–442.

[136]

Prehn-Kristensen A, Zimmermann A, Tittmann L et al. Reduced microbiome alpha diversity in young patients with ADHD. PLoS One 2018a;13:e0200728.

[137]

Prehn-Kristensen A, Zimmermann A, Tittmann L et al. Reduced microbiome alpha diversity in young patients with ADHD. PLoS One 2018b;13:e0200728.

[138]

Pronovost GN, Hsiao EY. Perinatal interactions between the microbiome, immunity, and neurodevelopment. Immunity 2019;50:18–36.

[139]

Puricelli C, Rolla R, Gigliotti L et al. The gut-brain-immune axis in autism spectrum disorders: a state-of-art report. Front Psychiatry 2022;12:755171.

[140]

Quintana FJ, Sherr DH. Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol Rev 2013;65:1148–1161.

[141]

Rao M, Gershon MD. The bowel and beyond: the enteric nervous system in neurological disorders. Nat Rev Gastroenterol Hepatol 2016;13:517–528.

[142]

Reigstad CS, Salmonson CE, Iii JFR et al. Gut microbes promote colonic serotonin production through an effect of short-chain fatty acids on enterochromaffin cells. FASEB J 2015;29:1395–1403.

[143]

Rodier PM. Vulnerable periods and processes during central nervous system development. Environ Health Perspect 1994;102:121–124.

[144]

Rodrigues HG, Takeo Sato F, Curi R et al. Fatty acids as modulators of neutrophil recruitment, function and survival. Eur J Pharmacol 2016;785:50–58.

[145]

Rothhammer V, Borucki DM, Tjon EC et al. Microglial control of astrocytes in response to microbial metabolites. Nature 2018;557:724–728.

[146]

Rothhammer V, Mascanfroni ID, Bunse L et al. Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor. Nat Med 2016;22:586–597.

[147]

Sanmarco LM, Wheeler MA, Gutiérrez-Vázquez C et al. Gut-licensed IFNγ+ NK cells drive LAMP1+TRAIL+ anti-inflammatory astrocytes. Nature 2021;590:473–479.

[148]

Satterstrom FK, Kosmicki JA, Wang J et al; Autism Sequencing Consortium. Large-scale exome sequencing study implicates both developmental and functional changes in the neurobiology of autism. Cell 2020;180:568–584.e23.

[149]

Sayal K, Prasad V, Daley D et al. ADHD in children and young people: prevalence, care pathways, and service provision. Lancet Psychiatry 2018;5:175–186.

[150]

Schafer DP, Lehrman EK, Kautzman AG et al. Microglia sculpt post-natal neural circuits in an activity and complement-dependent manner. Neuron 2012;74:691–705.

[151]

Schnell A, Huang L, Singer M et al. Stem-like intestinal Th17 cells give rise to pathogenic effector T cells during autoimmunity. Cell 2021;184:6281–6298.e23.

[152]

Sgritta M, Dooling SW, Buffington SA et al. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 2019a;101:246–259.e6.

[153]

Sgritta M, Dooling SW, Buffington SA et al. Mechanisms underlying microbial-mediated changes in social behavior in mouse models of autism spectrum disorder. Neuron 2019b;101:246–259.e6.

[154]

Sharon G, Cruz NJ, Kang D-W et al. Human gut microbiota from autism spectrum disorder promote behavioral symptoms in mice. Cell 2019;177:1600–1618.e17.

[155]

Shin Yim Y, Park A, Berrios J et al. Reversing behavioural abnormalities in mice exposed to maternal inflammation. Nature 2017;549:482–487.

[156]

Shoubridge AP, Choo JM, Martin AM et al. The gut microbiome and mental health: advances in research and emerging priorities. Mol Psychiatry 2022;27:1908–1919.

[157]

Skott E, Yang LL, Stiernborg M et al. Effects of a synbiotic on symptoms, and daily functioning in attention deficit hyperactivity disorder – a double-blind randomized controlled trial. Brain Behav Immun 2020;89:9–19.

[158]

Steinert RE, Feinle-Bisset C, Asarian L et al. Ghrelin, CCK, GLP-1, and PYY(3–36): secretory controls and physiological roles in eating and glycemia in health, obesity, and after RYGB. Physiol Rev 2017;97:411–463.

[159]

Stephens MAC, Wand G. Stress and the HPA axis. Alcohol Res 2012;34:468–483.

[160]

Stevens AJ, Purcell RV, Darling KA et al. Human gut microbiome changes during a 10 week Randomised Control Trial for micronutrient supplementation in children with attention deficit hyperactivity disorder. Sci Rep 2019;9:10128.

[161]

Strati F, Cavalieri D, Albanese D et al. Altered gut microbiota in Rett syndrome. Microbiome 2016;4:41.

[162]

Taché Y, Vale W, Rivier J et al. Brain regulation of gastric secretion: influence of neuropeptides. Proc Natl Acad Sci USA 1980;77:5515–5519.

[163]

Tengeler AC, Dam SA, Wiesmann M et al. Gut microbiota from persons with attention-deficit/hyperactivity disorder affects the brain in mice. Microbiome 2020;8:44.

[164]

Theoharides TC, Asadi S, Patel AB. Focal brain inflammation and autism. J Neuroinflammation 2013;10:815.

[165]

Trost B, Thiruvahindrapuram B, Chan AJS et al. Genomic architecture of autism from comprehensive whole-genome sequence annotation. Cell 2022;185:4409–4427.e18.

[166]

Uesaka T, Young HM, Pachnis V et al. Development of the intrinsic and extrinsic innervation of the gut. Dev Biol 2016;417:158–167.

[167]

Veerakumar A, Yung AR, Liu Y et al. Molecularly defined circuits for cardiovascular and cardiopulmonary control. Nature 2022;606:739–746.

[168]

Vickers NJ. Animal communication: When I’m Calling You, Will You Answer Too? Curr Biol 2017;27:R713–R715.

[169]

Vuong HE, Yano JM, Fung TC et al. The microbiome and host behavior. Annu Rev Neurosci 2017;40:21–49.

[170]

Wan Y, Zuo T, Xu Z et al. Underdevelopment of the gut microbiota and bacteria species as non-invasive markers of prediction in children with autism spectrum disorder. Gut 2022;71:910–918.

[171]

Wang L-J, Yang C-Y, Chou W-J et al. Gut microbiota and dietary patterns in children with attention-deficit/hyperactivity disorder. Eur Child Adolesc Psychiatry 2020;29:287–297.

[172]

Williams EK, Chang RB, Strochlic DE et al. Sensory neurons that detect stretch and nutrients in the digestive system. Cell 2016;166:209–221.

[173]

Willsey HR, Willsey AJ, Wang B et al. Genomics, convergent neuroscience and progress in understanding autism spectrum disorder. Nat Rev Neurosci 2022;23:323–341.

[174]

Wong JMW, de Souza R, Kendall CWC et al. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 2006;40:235–243.

[175]

Woo V, Alenghat T. Epigenetic regulation by gut microbiota. Gut Microbes 2022.

[176]

Wu W-L, Adame MD, Liou C-W et al. Microbiota regulate social behaviour via stress response neurons in the brain. Nature 2021;595:409–414.

[177]

Ya C X, Henders A K, Alvares G A et al. Interactions between the lipidome and genetic and environmental factors in autism. Nature Medicine 2023;29(4):936–949.

[178]

Yan Y, Jiang W, Spinetti T et al. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity 2013;38:1154–1163.

[179]

Yano JM, Yu K, Donaldson GP et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell 2015;161:264–276.

[180]

Yap CX, Henders AK, Alvares GA et al. 1.3 Autism-related dietary preferences mediate autism-gut microbiome associations. Cell 2021;184:5916–5931.e17.

[181]

Yavitt FM, Kirkpatrick BE, Blatchley MR et al. In situ modulation of intestinal organoid epithelial curvature through photoinduced viscoelasticity directs crypt morphogenesis. Sci Adv 2023;9:eadd5668.

[182]

Yu Y, Zhang B, Ji P et al. Changes to gut amino acid transporters and microbiome associated with increased E/I ratio in Chd8+/− mouse model of ASD-like behavior. Nat Commun 2022;13:1151.

[183]

Yuan B, Wang M, Wu X et al. Identification of de novo mutations in the Chinese Autism Spectrum Disorder cohort via whole-exome sequencing unveils brain regions implicated in autism. Neurosci Bull 2023.

[184]

Zengeler KE, Lukens JR. Innate immunity at the crossroads of healthy brain maturation and neurodevelopmental disorders. Nat Rev Immunol 2021;21:454–468.

[185]

Zheng L, Kelly CJ, Battista KD et al. Microbial-derived butyrate promotes epithelial barrier function through IL-10 receptor–dependent repression of Claudin-2. J Immunol 2017;199:2976–2984.

[186]

Zheng Y, Bek MK, Prince NZ et al. The role of bacterial-derived aromatic amino acids metabolites relevant in autism spectrum disorders: a comprehensive review. Front Neurosci 2021;15:738220.

RIGHTS & PERMISSIONS

The Author(s) 2023. Published by Oxford University Press on behalf of Higher Education Press.

AI Summary AI Mindmap
PDF (1447KB)

695

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/