Gut-brain axis and immunoneuroendocrine modulation in neurological and psychiatric disorders: A systematic review

Authors

DOI:

https://doi.org/10.33448/rsd-v10i4.14185

Keywords:

Gastrointestinal Microbiome; Active Immune Response; Mental Disorders; Neurosecretory Systems; Nervous system diseases.

Abstract

The present study aimed to explore the influence of the gut-brain axis on neuroendocrine and immunological modulation in neurological and psychiatric disorders. This systematic review followed the Preferred Reporting Items for Systematic Reviews and Meta-analyzes (PRISMA) guidelines, and searches were conducted in the electronic databases PubMed and SciELO using combinations of descriptors “Gastrointestinal Microbiome”, “Neurosecretory Systems”, “Immune Response”, “Nervous System Diseases” e “Mental Disorders”. From the 144 studies generated by crossing the descriptors, 32 of them were excluded because they were duplicated in the databases, 13 because they were not related to the objectives of the review, and another 29 because they were not on eligibility criteria. Therefore, 70 studies were included in the present review. Communication between the GI tract and the CNS occurs via the neuronal, endocrine, and immunological pathways through a) the production of neurotransmitters, b) the tryptophan metabolism, c) the modulation of the immunological activity in the CNS and the SNE, d) production of short chain fatty acids, e) the production of intestinal hormones, and f) the production of branched chain amino acids.

References

Ait-Belgnaoui, A., Durand, H., Cartier, C., Chaumaz, G., Eutamene, H., & Theodorou, V. (2012). Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology, 37(11), 1885-1895. 10.1016/j.psyneuen.2012.03.024

Akbaraly, T. N., Brunner, E. J., Ferrie, J. E., Marmot, M. G., Kivimaki, M., & Singh-Manoux A. (2009). Dietary pattern and depressive symptoms in middle age. Br J Psychiatry, 195(5), 408-413. 10.1192/bjp.bp.108.058925

Asano, Y., Hiramoto, T., Nishino, R., Aiba, Y., Kimura, T., Yoshihara, K., & Sudo, N. (2012). Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol - Gastrointest Liver Physiol, 303(11), G1288-G1295). 10.1152/ajpgi.00341.2012

Barouei, J., Moussavi, M., & Hodgson, D. M. (2012). Effect of maternal probiotic intervention on HPA Axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One, 7(10), e46051. 10.1371/journal.pone.0046051

Barrett, E., Ross, R. P., O’Toole, P. W., Fitzgerald, G. F, & Stanton C. (2012). γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol, 113(2), 411-417. 10.1111/j.1365-2672.2012.05344.x

Blachier, F., Mariotti, F., Huneau, J. F., & Tomé, D. (2007). Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids, 33(4), 547-562. 10.1007/s00726-006-0477-9

Belkaid, Y., & Hand, T. W. (2014) Role of the microbiota in immunity and inflammation. Cell, 157(1), 121-157. 10.1016/j.cell.2014.03.011

Berer, K., Gerdes, L. A., Cekanaviciute E., Jia, X., Xiao, L., Xia, Z., & Wekerle, H. (2017). Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. Proc Natl Acad Sci U S A, 114(40), 10719-10724. 10.1073/pnas.1711233114

Boem, F., & Amedei, A. (2019). Healthy axis: Towards an integrated view of the gut-brain health. World J Gastroenterol, 25(19), 3838-3841. 10.3748/wjg.v25.i29.3838

Bohórquez, D. V., Shahid, R. A., Erdmann, A., Kreger, A. M., Wang, Y., Calakos, N., & Liddle, R. A. (2015). Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J Clin Invest, 125(2), 782-786. 10.1172/JCI78361

Bourassa, M. W., Alim, I., Bultman, S. J., & Ratan, R. R. (2016). Butyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health? Neurosci Lett, 626, 56-63. 10.1016/j.neulet.2016.02.009

Bravo, J. A., Forsythe P., Chew, M. V., Escaravage, E., Savignac, H. M., Dinan, T. G., & Cryan, J. F. (2011). 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, 108(38), 16050-16055. 10.1073/pnas.1102999108

Brosnan, J. T., & Brosnan, M. E. (2006). Branched-chain amino acids: Enzyme and substrate regulation. Journal of Nutrition, 136(1), 207S-211S. 10.1093/jn/136.1.207s

Chen, J., Chia, N., Kalari, K. R., Yao, J. Z., Novotna, M., Soldan, M. M. P., Luckey, D. H., & Mangalam, A, K. (2016). Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep, 6, 28484. 10.1038/srep28484

Cho, I., & Blaser, M. J. (2012). The human microbiome: At the interface of health and disease. Nat Rev Genet, 13, 260-270. 10.1038/nrg3182

Clarke, G., Grenham, S., Scully, P., Fitzgerald, P., Moloney, R. D., Shanahan, F., & Cryan, J. F. (2013). The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol Psychiatry, 18, 666-673. 10.1038/mp.2012.77

Cryan, J. F., & O’Mahony, S. M. (2011). The microbiome-gut-brain axis: From bowel to behavior. Neurogastroenterol Motil, 23(3), 187-192. 10.1111/j.1365-2982.2010.01664.x

Cummings, J., Rombeau, J., & Sakata, T. (2004). Physiological and Clinical Aspects of Short-Chain Fatty Acids. Cambridge University Press. Editor: John H. Cummings.

Dai, Z. L., Wu, G., & Zhu, W. Y. (2011). Amino acid metabolism in intestinal bacteria: Links between gut ecology and host health. Front Biosci, 16, 1768-1786. 10.2741/3820

Davey, K. J., Cotter, P. D., O’Sullivan, O., Crispie, F., Dinan, T. G., Cryan, J. F., & O'Mahony. (2013). Antipsychotics and the gut microbiome: Olanzapine-induced metabolic dysfunction is attenuated by antibiotic administration in the rat. Transl Psychiatry, 3, e309. 10.1038/tp.2013.83

De Angelis, M., Francavilla, R., Piccolo, M., De Giacomo, A., & Gobbetti, M. (2015). Autism spectrum disorders and intestinal microbiota. Gut Microbes, 6(3), 207-213. 10.1080/19490976.2015.1035855

DeCastro, M., Nankova, B. B., Shah, P., Patel, P., Mally, P. V., Mishra, R., & La Gamma, E. F. (2005). Short chain fatty acids regulate tyrosine hydroxylase gene expression through a cAMP-dependent signaling pathway. Mol Brain Res, 142(1), 28-38. 10.1016/j.molbrainres.2005.09.002

De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., & Lionetti, P. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A, 107(33), 14692-14696. 10.1073/pnas.1005963107

Desbonnet, L., Garrett, L., Clarke, G., Bienenstock, J., & Dinan, T. G. (2008). The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res, 43(2), 164-174. 10.1016/j.jpsychires.2008.03.009

Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010). Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience, 170(4), 1179-1188. 10.1016/j.neuroscience.2010.08.005

Dickerson, F., Adamos, M., Katsafanas, E., Khushalani, S., Origoni, A., Savage, C., & Yolken, R. (2017). The association between immune markers and recent suicide attempts in patients with serious mental illness: A pilot study. Psychiatry Res, 255, 8-12. 10.1016/j.psychres.2017.05.005

Dickerson, F., Adamos, M., Katsafanas, E., Khushalani, S., Origoni, A., Savage, C., & Yolken, R. H. (2018). Adjunctive probiotic microorganisms to prevent rehospitalization in patients with acute mania: A randomized controlled trial. Bipolar Disord, 20(7), 614-621. 10.1111/bdi.12652

Dinan, T. G., Stanton, C., & Cryan, J. F. (2013). Psychobiotics: A novel class of psychotropic. Biol Psychiatry, 74(10), 720-726. 10.1016/j.biopsych.2013.05.001

Ding, H. T., Taur ,Y., & Walkup, J. T. (2016). Gut Microbiota and Autism: Key Concepts and Findings. J Autism Dev Disord, 47, 480-489. 10.1007/s10803-016-2960-9

Duerkop, B. A., Vaishnava, S., & Hooper, L. V. (2009). Immune Responses to the Microbiota at the Intestinal Mucosal Surface. Immunity, 31(3), 368-376. 10.1016/j.immuni.2009.08.009

Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J. (2011). NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell, 145(5), 745-757. 10.1016/j.cell.2011.04.022

Erny, D., De Angelis, A. L. H., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., & Prinz, M. (2015). Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci, 18, 965-977. 10.1038/nn.4030

Evans, S. J., Bassis, C. M., Hein, R., Assari, S., Flowers, S. A., Kelly, M. B., & Mclnnis, M. G. (2017). The gut microbiome composition associates with bipolar disorder and illness severity. J Psychiatr Res, 87, 23-29. 10.1016/j.jpsychires.2016.12.007

Fattorusso, A., Di Genova, L., Dell’isola, G. B., Mencaroni, E., & Esposito, S. (2019). Autism spectrum disorders and the gut microbiota. Nutrients, 11(3), 521. 10.3390/nu11030521

Fernstrom, J. D. (2005). Branched-chain amino acids and brain function. Journal of Nutrition, 135(6), 1539S-1546S. 10.1093/jn/135.6.1539s

Gómez-Eguílaz, M., Ramón-Trapero, J. L., Pérez-Martínez, L., & Blanco, J. R. The beneficial effect of probiotics as a supplementary treatment in drug-resistant epilepsy: A pilot study. Benef Microbes, 9(6), 875-881. 10.3920/BM2018.0018

Hasegawa, S., Goto, S., Tsuji, H., Okuno, T., Asahara, T., Nomoto, K., & Hirayama, M. (2015). Intestinal dysbiosis and lowered serum lipopolysaccharide-binding protein in Parkinson’s disease. PLoS One, 10(11), e0142164). 10.1371/journal.pone.0142164

He, Z., Cui, B. T., Zhang, T., Li, P., Long, C.-Y., Ji, G.-Z., & Zhang, F.-M. (2017). Fecal microbiota transplantation cured epilepsy in a case with Crohn’s Disease: The first report. World J Gastroenterol, 23(19), 3565-3568. 10.3748/wjg.v23.i19.3565

Hsiao, E. Y., McBride, S. W., Hsien, S., Sharon, G., Hyde, E. R., McCue, T., & Mazmanian, S. K. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155(7), 1451-1463. 10.1016/j.cell.2013.11.024

Huuskonen, J., Suuronen, T., Nuutinen, T., Kyrylenko, S., & Salminen, A. (2004). Regulation of microglial inflammatory response by sodium butyrate and short-chain fatty acids. Br J Pharmacol, 141(5), 874-880. 10.1038/sj.bjp.0705682

Inoue, R., Sakaue, Y., Sawai, C., Sawai, T., Ozeki, M., Romero-Pérez, G. A., & Tsukahara, T. (2016). A preliminary investigation on the relationship between gut microbiota and gene expressions in peripheral mononuclear cells of infants with autism spectrum disorders. Biosci Biotechnol Biochem, 80(12). 10.1080/09168451.2016.1222267

Jangi, S., Gandhi, R., Cox, L. M., Li, N., Glehn, F. V., Yan, R., & Patel, B. (2016). Alterations of the human gut microbiome in multiple sclerosis. Nat Commun, 7(12015). 10.1038/ncomms12015

Jordal, P. B., Dueholm, M. S., Larsen, P., Petersen, S. V., Enghild, J. J., Christiansen, G., Hojurup, P., & Otzen, D. E. (2009). Widespread abundance of functional bacterial amyloid in mycolata and other gram-positive bacteria. Appl Environ Microbiol, 75(12), 4101-4110. 10.1128/AEM.02107-08

Kekuda, R., Manoharan, P., Baseler, W., & Sundaram, U. (2013). Monocarboxylate 4 mediated butyrate transport in a rat intestinal epithelial cell line. Dig Dis Sci, 58, 660-667. 10.1007/s10620-012-2407-x

Keshavarzian, A., Green, S. J., Engen, P. A., Voigt, R. M., Naqib, A., Forsyth, C. B., & Shannon, K. M. (2015). Colonic bacterial composition in Parkinson’s disease. Mov Disord, 30(10), 1351-1360. 10.1002/mds.26307

Kidd, M., Gustafsson, B. I., Drozdov, I., & Modlin, I. M. (2009). IL1β- and LPS-induced serotonin secretion is increased in EC cells derived from Crohn’s disease. Neurogastroenterol Motil, 21(4), 439-450. 10.1111/j.1365-2982.2008.01210.x

Landgrave-Gómez, J., Mercado-Gómez, O., & Guevara-Guzmán, R. (2015). Epigenetic mechanisms in neurological and neurodegenerative diseases. Front Cell Neurosci, 9(58), 1-11. 10.3389/fncel.2015.00058

La Rosa, F., Saresella, M., Marventano, I., Piancone, F., Ripamonte, E., Al-Daghri, N., Bazzini, C., & Clerici, M. (2019). Stavudine Reduces NLRP3 Inflammasome Activation and Modulates Amyloid-β Autophagy. J Alzheimers Dis, 72(2), 401-412. 10.3233/JAD-181259

Larraufie, P., Doré, J., Lapaque, N., & Blottière, H. M. (2017). TLR ligands and butyrate increase Pyy expression through two distinct but inter-regulated pathways. Cell Microbiol, 19(2), e12648. 10.1111/cmi.12648

Larsen, P., Nielsen, J. L., Otzen, D., & Nielsen, P. H. (2008). Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge. Appl Environ Microbiol. 10.1128/AEM.02274-07

Leblhuber, F., Steiner, K., Schuetz, B., Fuchs, D., & Gostner, J. M. (2018). Probiotic supplementation in patients with Alzheimer’s dementia - An explorative intervention study. Curr Alzheimer Res, 15(12), 1106-1113. 10.2174/1389200219666180813144834

Li ,Q., Han, Y., Dy, A. B. C., Hager-Man, R. J., & Hager-man, R. J. (2017). The gut microbiota and autism spectrum disorders. Front Cell Neurosci, 11(120), 1-14. 10.3389/fncel.2017.00120

Liu, X., Cao, S., & Zhang, X. (2015). Modulation of Gut Microbiota-Brain Axis by Probiotics, Prebiotics, and Diet. J Agric Food Chem, 63(36), 7885-7895. 10.1021/acs.jafc.5b02404

Macfarlane, G. T., & Macfarlane, S. (2012). Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int, 95(1), 50-60. 10.5740/jaoacint.SGE_Macfarlane

Maes, M., Kubera, M., & Leunis, J. C. (2008). The gut-brain barrier in major depression: intestinal mucosal dysfunction with an increased translocation of LPS from gram negative enterobacteria (leaky gut) plays a role in the inflammatory pathophysiology of depression. Neuro Endocrinol Lett, 29(1), 117-124.

Mawe, G. M., & Hoffman, J. M. (2013). Serotonin signalling in the gut-functions, dysfunctions and therapeutic targets. Nat Rev Gastroenterol Hepatol, 10, 473-486. 10.1038/nrgastro.2013.105

Matsumoto, M., Kibe, R., Ooga, T., Aiba, Y., Sakawi, E., Koga, Y., & Benno, Y. (2013). Cerebral low-molecular metabolites influenced by intestinal microbiota: A pilot study. Front Syst Neurosci, 7(9), 1-19. 10.3389/fnsys.2013.00009

Messaoudi, M., Lalonde, R., Violle, N. Javelot, H., Desor, D., Nejdi, A., & Cazaubiel, J.-M. (2011). Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr, 105(5), 755-764. 10.1017/S0007114510004319

Miyake, S., Kim, S., Suda, W., Oshima, K., Nakamura, M., Matsuoka, T., Chihara, N., & Yamamura, T. (2015). Dysbiosis in the gut microbiota of patients with multiple sclerosis, with a striking depletion of species belonging to clostridia XIVa and IV clusters. PLoS One, 10(9), e0137429. 10.1371/journal.pone.0137429

Morowitz, M. J., Carlisle E. M., & Alverdy, J. C. (2011). Contributions of intestinal bacteria to nutrition and metabolism in the critically ill. Surg Clin North Am, 91(4), 771-785. 10.1016/j.suc.2011.05.001

Mouihate, A., Galic, M. A., Ellis, S. L., Spencer, S. J., Tsutsui S., & Pittman, Q. J. (2010). Early life activation of Toll-like Receptor 4 reprograms neural anti-inflammatory pathways. J Neurosci, 30(23), 7975-7983. 10.1523/JNEUROSCI.6078-09.2010

Nankova, B. B., Agarwal, R., MacFabe, D. F, & La Gamma E. F. (2014). Enteric bacterial metabolites propionic and butyric acid modulate gene expression, including CREB-dependent catecholaminergic neurotransmission, in PC12 cells - Possible relevance to autism spectrum disorders. PLoS One, 9(8), e103740. 10.1371/journal.pone.0103740

Navarro, F., Liu, Y., & Rhoads, J. M. (2016). Can probiotics benefit children with autism spectrum disorders? World J Gastroenterol, 22(46), 10093-10102. 10.3748/wjg.v22.i46.10093

Nguyen, T. T., Kosciolek, T., Maldonado, Y., Daly, R. E., Martin, A. S., McDonald, D., & Jeste, D. V. (2019). Differences in gut microbiome composition between persons with chronic schizophrenia and healthy comparison subjects. Schizophr Res, 204, 23-29. 10.1016/j.schres.2018.09.014

Nishino, R., Mikami, K., Takahashi, H., Tomonaga, S., Furuse, M., Hiramoto, T., & Sudo, N. (2013). Commensal microbiota modulate murine behaviors in a strictly contamination-free environment confirmed by culture-based methods. Neurogastroenterol Motil, 25(6), 521-e371. 10.1111/nmo.12110

Ohland, C. L., Kish, L., Bell, H., Thiesen, A., Hotte, N., Pankiv, E., & Madsen, K. L. (2013). Effects of Lactobacillus helveticus on murine behavior are dependent on diet and genotype and correlate with alterations in the gut microbiome. Psychoneuroendocrinology, 38(9), 1738-1747. 10.1016/j.psyneuen.2013.02.008

Okubo, R., Koga, M., Katsumata, N., Odamaki, T., Matsuyama, S., Oka, M., & Matsuoka, Y. Y. (2019). Effect of Bifidobacterium breve A-1 on anxiety and depressive symptoms in schizophrenia: A proof-of-concept study. J Affect Disord, 245, 377-385. 10.1016/j.jad.2018.11.011

Pierantozzi, M., Pietroiusti, A., Brusa, L., Galati, S., & Stefani, A., Lunardi,...Galante, A. (2006). Helicobacter pylori eradication and L-dopa absorption in patients with PD and motor fluctuations. Neurology, 66(12), 1824-1829. 10.1212/01.wnl.0000221672.01272.ba

Peng, A., Qiu, X., Lai, W., Li, W., Zhang, L., Zhu, X., & Chen, L. 2018. Altered composition of the gut microbiome in patients with drug-resistant epilepsy. Epilepsy Res, 147, 102-107. 10.1016/j.eplepsyres.2018.09.013

Pereira, A. S. et al. (2018). Metodologia da pesquisa científica. UFSM. https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica.pdf?sequence=1.

PRISMA (2015). Principais itens para relatar Revisões sistemáticas e Meta-análises: A recomendação PRISMA. Epidemiologia e Serviços de Saúde, 24(2), 335-342. Recuperado em 30 de março de 2021, de http://scielo.iec.gov.br/scielo.php?script=sci_arttext&pid=S1679-49742015000200017&lng=pt&tlng=pt.

Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., & Wang, J. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59-65. 10.1038/nature08821

Scheperjans, F., Aho, V., Pereira, P. A. B., Koskinen, K., Paulin, L., Pekkonen, E., & Auvinen, P. (2015). Gut microbiota are related to Parkinson’s disease and clinical phenotype. Mov Disord, 30(3), 350-358. 10.1002/mds.26069

Srikantha, P., & Hasan Mohajeri M. (2019). The possible role of the microbiota-gut-brain-axis in autism spectrum disorder. Int J Mol Sci, 20(9), 2115. 10.3390/ijms20092115

Stilling, R. M., van de Wouw, M., Clarke, G., Stanton, C., Dinan, T. G., & Cryan, J. F. (2016). The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis? Neurochem Int, 99, 99-110. 10.1016/j.neuint.2016.06.011

Tankou, S. K., Regev, K., Healy, B. C., Cox, L. M., Tjon, E., Kivisakk, P., & Weiner, H. L. (2018). Investigation of probiotics in multiple sclerosis. Mult Scler, 24(1), 58-63. 10.1177/1352458517737390

Tamtaji, O. R., Heidari-soureshjani, R., Mirhosseini, N., Kouchaki, E., Bahmani, F., Aghadavod, E., & Asemi, Z. (2019b). Probiotic and selenium co-supplementation, and the effects on clinical, metabolic and genetic status in Alzheimer’s disease: A randomized, double-blind, controlled trial. Clin Nutr, 38(6), 2569-2575. 10.1016/j.clnu.2018.11.034

Tamtaji, O. R., Taghizadeh, M., Kakhaki, R. D., Kouchaki, E., Bahmani, F., Borzabadi, S., & Asemi, Z. (2019a). Clinical and metabolic response to probiotic administration in people with Parkinson’s disease: A randomized, double-blind, placebo-controlled trial. Clin Nutr, 38(3), 1031-1035. 10.1016/j.clnu.2018.05.018

Tomova, A., Husarova, V., Lakatosova, S., Lakatosova, S., Bakos, J., Vlkova, B., & Ostatnikova, D. (2015). Gastrointestinal microbiota in children with autism in Slovakia. Physiol Behav, 138, 179-187. 10.1016/j.physbeh.2014.10.033

Turnbaugh, P. J., Bäckhed, F., Fulton, L., & Gordon, J. I. (2008). Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe, 3(4), 213-223. 10.1016/j.chom.2008.02.015

Uher, R. (2014). Gene-environment interactions in severe mental illness. Front Psychiatry, 5(48), 1-9. 10.3389/fpsyt.2014.00048

Valladares, R., Bojilova, L., Potts, A. H., Cameron, E., Gardner, C., Lorca, G., & Gonzalez, C. F. (2013). Lactobacillus johnsonii inhibits indoleamine 2,3-dioxygenase and alters tryptophan metabolite levels in BioBreeding rats. FASEB J, 27(4), 1711-1720. 10.1096/fj.12-223339

Valverde, J. R., & Mellado, R. P. (2013). Analysis of metagenomic data containing high biodiversity levels. PLoS One, 8(3), e58118. 10.1371/journal.pone.0058118

Vetulani, J. (2013). Early maternal separation: A rodent model of depression and a prevailing human condition. Pharmacol Reports, 65(6). 10.1016/S1734-1140(13)71505-6

Vijay N, & Morris M. (2014). Role of monocarboxylate transporters in drug delivery to the brain. Curr Pharm Des, 20(10), 1487-1498. 10.2174/13816128113199990462

Vigo, D. V., Kestel, D., Pendakur, K., Thornicroft, G., & Atun R. (2019). Disease burden and government spending on mental, neurological, and substance use disorders, and self-harm: cross-sectional, ecological study of health system response in the Americas. Lancet Public Heal, 4(2), e89-e96. 10.1016/S2468-2667(18)30203-2

Yang, Z., Huang, S., Zou, D., Dong, D., He, X., Liu, N., & Huang, L. (2016). Metabolic shifts and structural changes in the gut microbiota upon branched-chain amino acid supplementation in middle-aged mice. Amino Acids, 48, 2731-2745. 10.1007/s00726-016-2308-y

Yano, J. M., Yu, K., Donaldson, G. P., & Shastri, G. G. (2015). Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell, 161(2), 264-276. 10.1016/j.cell.2015.02.047

Downloads

Published

10/04/2021

How to Cite

LAMI, K. F.; OLIVEIRA, V. F. de; BATISTA, K. Z. S. Gut-brain axis and immunoneuroendocrine modulation in neurological and psychiatric disorders: A systematic review. Research, Society and Development, [S. l.], v. 10, n. 4, p. e28110414185, 2021. DOI: 10.33448/rsd-v10i4.14185. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/14185. Acesso em: 3 dec. 2024.

Issue

Section

Review Article