Mammalian gut microbiome and brain development: A comprehensive review

Aitbali, Y, Ba-M'hamed, S, Elhidar, N, Nafis, A, Soraa, N & Bennis, M 2018, Glyphosate based-herbicide exposure affects gut microbiota, anxiety and depression-like behaviors in mice. Neurotoxicology and Teratology, 67: 44-49.

Al-Asmakh, M, Anuar, F, Zadjali, F, Rafter, J & Pettersson, S 2012, Gut microbial communities modulating brain development and function. Gut Microbes, 3: 366-373.

Alenina, N & Klempin, F 2015, The role of serotonin in adult hippocampal neurogenesis. Behavioural brain research, 277: 49-57.

Allam-Ndoul, B, Castonguay-Paradis, S & Veilleux, A 2020, Gut microbiota and intestinal trans-epithelial permeability. International Journal of Molecular Sciences, 21: 6402.

Almeida, RG & Lyons, DA 2017, On myelinated axon plasticity and neuronal circuit formation and function. Journal of Neuroscience, 37: 10023-10034.

Banks, WA 2016, From blood–brain barrier to blood–brain interface: new opportunities for CNS drug delivery. Nature Reviews Drug Discovery, 15: 275-292.

Basiji, K, Sendani, AA, Ghavami, SB, Farmani, M, Kazemifard, N, Sadeghi, A, Lotfali, E & Aghdaei, HA 2023, The critical role of gut-brain axis microbiome in mental disorders. Metabolic Brain Disease, 38: 2547-2561.

Bottes, S, Jaeger, BN, Pilz, GA, Jörg, DJ, Cole, JD, Kruse, M, Harris,  Korobeynyk, VI, Mallona, I & Helmchen, F 2021, Long-term self-renewing stem cells in the adult mouse hippocampus identified by intravital imaging. Nature Neuroscience, 24: 225-233.

Braniste, V, Al-Asmakh, M, Kowal, C, Anuar, F, Abbaspour, A, Tóth, M, Korecka, A, Bakocevic, N, Ng, LG & Kundu, P 2014, The gut microbiota influences blood-brain barrier permeability in mice. Science Translational Medicine, 6: 263ra158-263ra158.

Bravo, J A, Forsythe, P, Chew, MV, Escaravage, E, Savignac, HM, Dinan, TG, Bienenstock, J & Cryan, JF 2011, Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proceedings of the National Academy of Sciences, 108: 16050-16055.

Chen S, Luo S, Yan C 2021, Gut Microbiota Implications for Health and Welfare in Farm Animals: A Review.

Animals (Basel) 12: 93.

Clarke, G, Grenham, S, Scully, ., Fitzgerald, P, Moloney, R, Shanahan, F, Dinan, T & Cryan, J 2013, The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Molecular Psychiatry, 18: 666-673.

Collins, J, Borojevic, R, Verdu, E, Huizinga, J & Ratcliffe, E 2014, Intestinal microbiota influence the early postnatal development of the enteric nervous system. Neurogastroenterology & Motility, 26: 98-107.

Daneman, R 2012, The blood–brain barrier in health and disease. Annals of Neurology, 72: 648-672.

Dominguez Bello, M 2019, Effects of C‐section on the human microbiota. American Journal of Human Biology, 31.

Dunphy-Doherty, F, O'Mahony, SM, Peterson, VL, O'Sullivan, O, Crispie, F, Cotter, PD, Wigmore, P, King, MV, Cryan, JF & Fone, KC 2018, Post-weaning social isolation of rats leads to long-term disruption of the gut microbiota-immune-brain axis. Brain, Behavior, and Immunity, 68: 261-273.

Erny, D, Hrabě de Angelis, AL, Jaitin, D, Wieghofer, P, Staszewski, O, David, E, Keren-Shaul, H, Mahlakoiv, T, Jakobshagen, K & Buch, T 2015, Host microbiota constantly control maturation and function of microglia in the CNS. Nature Neuroscience, 18: 965-977.

Farré-Maduell, E & Casals-Pascual, C 2019, The origins of gut microbiome research in Europe: From Escherich to Nissle. Human Microbiome Journal, 14: 100065.

Feng, W, Ao, H, Peng, C & Yan, D 2019, Gut microbiota, a new frontier to understand traditional Chinese medicines. Pharmacological Research, 142: 176-191.

Gacias, M, Gaspari, S, Santos, PMG, Tamburini, S, Andrade, M, Zhang, F, Shen, N, Tolstikov, V, Kiebish, MA, & Dupree, JL 2016, Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. Elife, 5: e13442.

Gershon, MD & Margolis, KG 2021, The gut, its microbiome, and the brain: connections and communications. The Journal of Clinical Investigation, 131.

Glover, V, O'Donnell, KJ, O'Connor, TG & Fisher, J 2018, Prenatal maternal stress, fetal programming, and mechanisms underlying later psychopathology-A global perspective. Development and Psychopathology, 30: 843-854.

Griffith, JC & Morgan, XC 2019, Invited commentary: improving the accessibility of human microbiome project data through integration with R/Bioconductor. American Journal of Epidemiology, 188: 1027-1030.

Hayes, W & Sahu, S 2020, The Human Microbiome: History and Future: Microbiome. Journal of Pharmacy & Pharmaceutical Sciences, 23: 406-411.

Hemmati, M, Mashayekhi, F, Firouzi, F, Ashori, M & Mashayekhi, H 2014, Effects of electromagnetic fields on reelin and Dab1 expression in the developing cerebral cortex. Neurological Sciences, 35: 1243-1247.

Hill, JH, Franzosa, EA, Huttenhower, C & Guillemin, K 2016, A conserved bacterial protein induces pancreatic beta cell expansion during zebrafish development. Elife, 5: e20145.

Hoban, AE, Stilling, RM, Ryan, FJ, Shanahan, F, Dinan, TG, Claesson, MJ, Clarke, G & Cryan, J 2016, Regulation of prefrontal cortex myelination by the microbiota. Translational Psychiatry, 6: e774-e774.

Humann, J, Mann, B, Gao, G, Moresco, P, Ramahi, J, Loh, LN, Farr, A, Hu, Y, Durick-Eder, K & Fillon, SA 2016, Bacterial peptidoglycan traverses the placenta to induce fetal neuroproliferation and aberrant postnatal behavior. Cell Host & Microbe, 19: 388-399.

Kambe, J, Usuda, K, Inoue, R, Hirayama, K, Ito, M, Suenaga, K, Masukado, S, Liu, H, Miyata, S & Li, C 2024, Hydrogen peroxide in breast milk is crucial for gut microbiota formation and myelin development in neonatal mice. Gut Microbes, 16: 2359729.

Kaul, D, Habbel, P, Derkow, K, Krüger, C, Franzoni, E, Wulczyn, FG, Bereswill, S, Nitsch, R, Schott, E & Veh, R 2012, Expression of Toll-like receptors in the developing brain. PLoS One, 7: e37767.

Kempermann, G 2019, Environmental enrichment, new neurons and the neurobiology of individuality. Nature Reviews Neuroscience, 20: 235-245.

Keogh, CE, Kim, DH, Pusceddu, MM, Knotts, TA, Rabasa, G, Sladek, JA, Hsieh, MT, Honeycutt, M, Brust-Mascher, I & Barboza, M 2021, Myelin as a regulator of development of the microbiota-gut-brain axis. Brain, Behavior, and Immunity, 91: 437-450.

Keramat Amirkolaie, A 2015, Effects of prebiotic Immunogen on growth performance, intestinal bacteria colonization, and survival rate in Rutilus kutum fry. Caspian Journal of Environmental Sciences, 13: 99-108.

Liu, C, Yang, SY, Wang, L & Zhou, F 2022, The gut microbiome: implications for neurogenesis and neurological diseases. Neural Regeneration Research, 17: 53-58.

Lynch, CM, Cowan, CS, Bastiaanssen, TF, Moloney, GM, Theune, N, van de Wouw, M, Zanuy, EF, Ventura-Silva, AP, Codagnone, MG & Villalobos-Manríquez, F 2023, Critical windows of early-life microbiota disruption on behaviour, neuroimmune function, and neurodevelopment. Brain, Behavior, and Immunity, 108: 309-327.

Mashayekhi, F, Draper, CE, Bannister, CM, Pourghasem, M, Owen‐Lynch, PJ & Miyan, JA 2002, Deficient cortical development in the hydrocephalic Texas (H‐Tx) rat: A role for CSF. Brain, 125: 1859-1874.

Mashayekhi, F, Hadiyan, SP & Salehi, Z 2015, Administration of leukemia inhibitory factor increases Opalin and myelin oligodendrocyte glycoprotein expression in the cerebral cortex in a cuprizone-induced model of demyelination. Folia Neuropathologica, 53: 147-152.

Mashayekhi, F & Salehi, Z 2024, The impact of gut microbiota in human health and disease: A comprehensive review. International Journal of Molecular and Clinical Microbiology, 14: 1970-1980.

Mayer EA, Knight R, Mazmanian SK, Cryan JF, Tillisch K 2014, Gut microbes and the brain: paradigm shift in neuroscience. Journal of Neuroscience, 34: 15490-6.

Matcovitch-Natan, O, Winter, DR, Giladi, A, Vargas Aguilar, S, Spinrad, A, Sarrazin, S, Ben-Yehuda, H, David, E, Zelada González, F & Perrin, P 2016, Microglia development follows a stepwise program to regulate brain homeostasis. Science, 353: aad8670.

McFall-Ngai, MJ 2014, The importance of microbes in animal development: lessons from the squid-vibrio symbiosis. Annual Review of Microbiology, 68: 177-194.

Michel, L & Prat, A 2016, One more role for the gut: microbiota and blood brain barrier. Annals of Translational Medicine, 4.

Möhle, L, Mattei, D, Heimesaat, MM, Bereswill, S, Fischer, A, Alutis, M, French, T, Hambardzumyan, D, Matzinger, P & Dunay, IR 2016, Ly6Chi monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Reports, 15: 1945-1956.

Morais, LH, Schreiber IV, HL & Mazmanian, SK 2021, The gut microbiota–brain axis in behaviour and brain disorders. Nature Reviews Microbiology, 19: 241-255.

Nasseri, S, Hajrasouliha, S, Vaseghi, S & Ghorbani Yekta, B 2024, Interaction effect of crocin and citalopram on memory and locomotor activity in rats: An insight into BDNF and synaptophysin levels in the hippocampus. Naunyn-Schmiedeberg's Archives of Pharmacology, pp. 1-10.

Needham, B 2024, Exposed wires: A microbial metabolite influences myelination in the brain. Science, 385: 37-37.

Ntranos, A & Casaccia, P 2018, The microbiome–gut–behavior axis: crosstalk between the gut microbiome and oligodendrocytes modulates behavioral responses. Neurotherapeutics, 15: 31-35.

Owen‐Lynch, PJ, Draper, CE, Mashayekhi, F, Bannister, CM & Miyan, JA 2003, Defective cell cycle control underlies abnormal cortical development in the hydrocephalic Texas rat. Brain, 126: 623-631.

Pessa-Morikawa, T, Husso, A, Kärkkäinen, O, Koistinen, V, Hanhineva, K, Iivanainen, A & Niku, M 2022, Maternal microbiota-derived metabolic profile in fetal murine intestine, brain and placenta. BMC Microbiology, 22: 46.

Powell, N, Walker, MM & Talley, NJ 2017, The mucosal immune system: master regulator of bidirectional gut–brain communications. Nature Reviews Gastroenterology & Hepatology, 14: 143-159.

Ratsika, A, Pereira, JSC, Lynch, CM, Clarke, G & Cryan, JF 2023, Microbiota-immune-brain interactions: A lifespan perspective. Current Opinion in Neurobiology, 78: 102652.

Salehi, Z & Mashayekhi, F 2009, Brain-derived neurotrophic factor concentrations in the cerebrospinal fluid of patients with Parkinson’s disease. Journal of Clinical Neuroscience, 16: 90-93.

Salvo, E, Stokes, P, Keogh, CE, Brust-Mascher, I, Hennessey, C, Knotts, TA. Sladek, JA, Rude, KM, Swedek, M & Rabasa, G 2020, A murine model of pediatric inflammatory bowel disease causes microbiota-gut-brain axis deficits in adulthood. American Journal of Physiology-Gastrointestinal and Liver Physiology, 319: G361-G374.

Sarubbo, F, Cavallucci, V & Pani, G 2022, The influence of gut microbiota on neurogenesis: evidence and hopes. Cells, 11: 382.

Sender, R, Fuchs, S & Milo, R 2016, Revised estimates for the number of human and bacteria cells in the body. PLoS biology, 14: e1002533.

Sharon, G, Sampson, TR, Geschwind, DH & Mazmanian, SK 2016, The central nervous system and the gut microbiome. Cell, 167: 915-932.

Shin, JH, Bozadjieva-Kramer, N, Shao, Y, Lyons-Abbott, S, Rupp, AC, Sandoval, DA & Seeley, RJ 2022, The gut peptide Reg3g links the small intestine microbiome to the regulation of energy balance, glucose levels, and gut function. Cell Metabolism, 34: 1765-1778. e1766.

Sonnenburg, JL & Bäckhed, F 2016, Diet–microbiota interactions as moderators of human metabolism. Nature, 535: 56-64.

Stilling, R. M, Ryan, FJ, Hoban, AE, Shanahan, F, Clarke, G, Claesson, MJ, Dinan, TG & Cryan, JF 2015, Microbes & neurodevelopment–Absence of microbiota during early life increases activity-related transcriptional pathways in the amygdala. Brain, Behavior, and Immunity, 50: 209-220.

Tiwari, RK, Moin, A, Rizvi, SMD, Shahid, SMA & Bajpai, P 2021, Modulating neuroinflammation in neurodegeneration-related dementia: Can microglial toll-like receptors pull the plug? Metabolic Brain Disease, 36: 829-847.

Van de Wouw, M, Boehme, M, Lyte, JM., Wiley, N, Strain, C, O'Sullivan, O, Clarke, G, Stanton, C, Dinan, TG & Cryan, JF 2018, Short‐chain fatty acids: microbial metabolites that alleviate stress‐induced brain–gut axis alterations. The Journal of Physiology, 596: 4923-4944.

Wang, H, Hou, X, Li, B, Yang, Y, Li, Q & Si, Y 2021, Study on active components of cuscuta chinensis promoting neural stem cells proliferation: bioassay-guided fractionation. Molecules, 26: 6634.

Wang, Y, Zheng, AN, Yang, H, Wang, Q, Dai, B, Wang, JJ, Wan, Yt, Liu, Z & Liu, SY 2024, Olfactory Three-Needle Electroacupuncture Improved Synaptic Plasticity and Gut Microbiota of SAMP8 Mice by Stimulating Olfactory Nerve. Chinese Journal of Integrative Medicine, 30: 729-741.

Watts, PC, Mappes, T, Tukalenko, E, Mousseau, TA, Boratyński, Z, Møller, AP & Lavrinienko, A 2022, Interpretation of gut microbiota data in the ‘eye of the beholder: A commentary and re‐evaluation of data from ‘Impacts of radiation exposure on the bacterial and fungal microbiome of small mammals in the Chernobyl Exclusion Zone’. Journal of Animal Ecology, 91: 1535-1545.

Willemsen, Y, Ou, Y, Belzer, C, Vásquez, AA, Smidt, H, Beijers, R & de Weerth, C 2024, A longitudinal study of the gut microbiota during the first three years of life: Links with problem behavior and executive functions at preschool age. Development and Psychopathology, pp. 36:2032-2048.

Williams, S, Chen, L, Savignac, HM, Tzortzis, G, Anthony, DC & Burnet, PW 2016, Neonatal prebiotic (BGOS) supplementation increases the levels of synaptophysin, Glu N 2 A‐subunits and BDNF proteins in the adult rat hippocampus. Synapse, 70: 121-124.

Williamson, JM & Lyons, DA 2018, Myelin dynamics throughout life: an ever-changing landscape? Frontiers in cellular neuroscience, 12: 424.

Yarandi, SS, Kulkarni, S, Saha, M, Sylvia, KE, Sears, CL, & Pasricha, PJ 2020, Intestinal bacteria maintain adult enteric nervous system and nitrergic neurons via toll-like receptor 2-induced neurogenesis in mice. Gastroenterology, 159: 200-213. e208.

Zhang, C, Xue, P, Zhang, H, Tan, C, Zhao, S, Li, X, Sun, L, Zheng, H, Wang, J & Zhang, B 2022, Gut brain interaction theory reveals gut microbiota mediated neurogenesis and traditional Chinese medicine research strategies. Frontiers in Cellular and Infection Microbiology, 12: 1072341.