Gut-Brain Axis in the Early Postnatal Years of Life: A Developmental Perspective

Overview

Journal Front Integr Neurosci

Date 2020 Aug 28

PMID 32848651

Citations 38

Authors

Ankita Jena

Carlos A Montoya

Jane A Mullaney

Ryan N Dilger

Wayne Young

Warren C McNabb

Nicole C Roy

Affiliations

Soon will be listed here.

Abstract

Emerging evidence suggests that alterations in the development of the gastrointestinal (GI) tract during the early postnatal period can influence brain development and vice-versa. It is increasingly recognized that communication between the GI tract and brain is mainly driven by neural, endocrine, immune, and metabolic mediators, collectively called the gut-brain axis (GBA). Changes in the GBA mediators occur in response to the developmental changes in the body during this period. This review provides an overview of major developmental events in the GI tract and brain in the early postnatal period and their parallel developmental trajectories under physiological conditions. Current knowledge of GBA mediators in context to brain function and behavioral outcomes and their synthesis and metabolism (site, timing, etc.) is discussed. This review also presents hypotheses on the role of the GBA mediators in response to the parallel development of the GI tract and brain in infants.

Citing Articles

Necrotizing Enterocolitis and Neurodevelopmental Impairments: Microbiome, Gut, and Brain Entanglements.

Sha C, Jin Z, Ku S, Kogosov A, Yu S, Bergese S Biomolecules. 2024; 14(10).

PMID: 39456187 PMC: 11505939. DOI: 10.3390/biom14101254.

A pilot case-control study on the fecal microbiota of pediatric functional abdominal pain-not otherwise specified and the role of early life stress.

Otaru N, Pugin B, Pluss S, Hojsak I, Braegger C, Lacroix C Microbiome Res Rep. 2024; 3(3):32.

PMID: 39421253 PMC: 11485736. DOI: 10.20517/mrr.2023.75.

Maternal and infant microbiome and birth anthropometry.

Padiyar S, Nandakumar V, Kollikonda S, Karnati S, Sangwan N, Aly H iScience. 2024; 27(10):110312.

PMID: 39386758 PMC: 11462025. DOI: 10.1016/j.isci.2024.110312.

The gut microbiome in children with mood, anxiety, and neurodevelopmental disorders: An umbrella review.

Romano K, Shah A, Schumacher A, Zasowski C, Zhang T, Bradley-Ridout G Gut Microbiome (Camb). 2024; 4:e18.

PMID: 39295902 PMC: 11406386. DOI: 10.1017/gmb.2023.16.

Antibiotic use and risk of autism spectrum disorder and attention-deficit/hyperactivity disorder: a population-based cohort study.

Yang K, Yen T, Lin F, Hsu C, Wang C Child Adolesc Psychiatry Ment Health. 2024; 18(1):82.

PMID: 38992772 PMC: 11241894. DOI: 10.1186/s13034-024-00774-4.

References

Freestone P, Williams P, Haigh R, Maggs A, Neal C, Lyte M . Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock. 2002; 18(5):465-70. DOI: 10.1097/00024382-200211000-00014. View

Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky S, Anderson J, Jung S . The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci. 2008; 11(7):752-3. PMC: 2765052. DOI: 10.1038/nn.2139. View

Raybould H . Mechanisms of CCK signaling from gut to brain. Curr Opin Pharmacol. 2007; 7(6):570-4. PMC: 2692370. DOI: 10.1016/j.coph.2007.09.006. View

Zhang H, Malo C, Boyle C, Buddington R . Diet influences development of the pig (Sus scrofa) intestine during the first 6 hours after birth. J Nutr. 1998; 128(8):1302-10. DOI: 10.1093/jn/128.8.1302. View

Smith M, Yatsunenko T, Manary M, Trehan I, Mkakosya R, Cheng J . Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013; 339(6119):548-54. PMC: 3667500. DOI: 10.1126/science.1229000. View

Zheng X, Xie G, Zhao A, Zhao L, Yao C, Chiu N . The footprints of gut microbial-mammalian co-metabolism. J Proteome Res. 2011; 10(12):5512-22. DOI: 10.1021/pr2007945. View

Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T, Tajima S . A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun. 2016; 7:11939. PMC: 4931012. DOI: 10.1038/ncomms11939. View

Cusick S, Georgieff M . The Role of Nutrition in Brain Development: The Golden Opportunity of the "First 1000 Days". J Pediatr. 2016; 175:16-21. PMC: 4981537. DOI: 10.1016/j.jpeds.2016.05.013. View

Bravo J, Forsythe P, Chew M, Escaravage E, Savignac H, Dinan T . Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011; 108(38):16050-5. PMC: 3179073. DOI: 10.1073/pnas.1102999108. View

10.

Lyall A, Shi F, Geng X, Woolson S, Li G, Wang L . Dynamic Development of Regional Cortical Thickness and Surface Area in Early Childhood. Cereb Cortex. 2014; 25(8):2204-12. PMC: 4506327. DOI: 10.1093/cercor/bhu027. View

11.

Mahanonda R, Sa-Ard-Iam N, Montreekachon P, Pimkhaokham A, Yongvanichit K, Fukuda M . IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol. 2007; 178(2):1151-7. DOI: 10.4049/jimmunol.178.2.1151. View

12.

de Weerth C . Do bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis. Neurosci Biobehav Rev. 2017; 83:458-471. DOI: 10.1016/j.neubiorev.2017.09.016. View

13.

Wu Y, Dissing-Olesen L, MacVicar B, Stevens B . Microglia: Dynamic Mediators of Synapse Development and Plasticity. Trends Immunol. 2015; 36(10):605-613. PMC: 4841266. DOI: 10.1016/j.it.2015.08.008. View

14.

Le Floch N, Otten W, Merlot E . Tryptophan metabolism, from nutrition to potential therapeutic applications. Amino Acids. 2010; 41(5):1195-205. DOI: 10.1007/s00726-010-0752-7. View

15.

Shi Y, Guo H, Chen J, Sun G, Ren R, Guo M . Initial meconium microbiome in Chinese neonates delivered naturally or by cesarean section. Sci Rep. 2018; 8(1):3255. PMC: 5818670. DOI: 10.1038/s41598-018-21657-7. View

16.

Shaftel S, Kyrkanides S, Olschowka J, Miller J, Johnson R, OBanion M . Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J Clin Invest. 2007; 117(6):1595-604. PMC: 1878531. DOI: 10.1172/JCI31450. View

17.

Yamamoto J, Ihara K, Nakayama H, Hikino S, Satoh K, Kubo N . Characteristic expression of aryl hydrocarbon receptor repressor gene in human tissues: organ-specific distribution and variable induction patterns in mononuclear cells. Life Sci. 2003; 74(8):1039-49. DOI: 10.1016/j.lfs.2003.07.022. View

18.

Wikoff W, Anfora A, Liu J, Schultz P, Lesley S, Peters E . Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A. 2009; 106(10):3698-703. PMC: 2656143. DOI: 10.1073/pnas.0812874106. View

19.

Batterham R, Ffytche D, Rosenthal J, Zelaya F, Barker G, Withers D . PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature. 2007; 450(7166):106-9. DOI: 10.1038/nature06212. View

20.

Bergstrom A, Skov T, Bahl M, Roager H, Christensen L, Ejlerskov K . Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol. 2014; 80(9):2889-900. PMC: 3993305. DOI: 10.1128/AEM.00342-14. View