Association of intestinal dysbiosis with susceptibility to multiple sclerosis: Evidence from different population studies (Review)
- Authors:
- María Eugenia Torres-Chávez
- Nora Magdalena Torres-Carrillo
- Ana Victoria Monreal-Lugo
- Sandra Garnés-Rancurello
- Selvasankar Murugesan
- Itzae Adonai Gutiérrez-Hurtado
- Jesús Raúl Beltrán-Ramírez
- Elena Sandoval-Pinto
- Norma Torres-Carrillo
-
Affiliations: Department of Microbiology and Pathology, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco 44340, Mexico, Department of Microbiology and Pathology, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco 44340, Mexico, Department of Nutrition and Health Research Center, National Institute of Public Health, Cuernavaca, Morelos 62100, Mexico, Department of Nutrition, Technological Institute of Higher Studies of Monterrey, Zapopan, Jalisco 45201, Mexico, Maternal and Child Health Program, Sidra Medicine, Doha 26999, Qatar, Department of Molecular Biology and Genomics, University Center for Health Sciences, University of Guadalajara, Guadalajara, Jalisco 44340, Mexico, Department of Information Systems, University Center of Administrative Economic Sciences, University of Guadalajara, Zapopan, Jalisco 45100, Mexico, Department of Cellular and Molecular Biology, University Center for Biological and Agricultural Sciences, University of Guadalajara, Zapopan, Jalisco 45200, Mexico - Published online on: October 12, 2023 https://doi.org/10.3892/br.2023.1675
- Article Number: 93
-
Copyright: © Torres-Chávez et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Tinahones FJ: The importance of the microbiota in obesity. Rev Esp Endocrinol Pediatr. 8 (Suppl 1):16–20. 2017. | |
Bibbò S, Dore MP, Pes GM, Delitala G and Delitala AP: Is there a role for gut microbiota in type 1 diabetes pathogenesis? Ann Med. 49:11–22. 2017.PubMed/NCBI View Article : Google Scholar | |
Kim S and Jazwinski SM: The gut microbiota and healthy aging: A mini-review. Gerontology. 64:513–520. 2018.PubMed/NCBI View Article : Google Scholar | |
Ordoñez-Rodriguez A, Roman P, Rueda-Ruzafa L, Campos-Rios A and Cardona D: Changes in gut microbiota and multiple sclerosis: A systematic review. Int J Environ Res Public Health. 20(4624)2023.PubMed/NCBI View Article : Google Scholar | |
Cornejo-Pareja I, Muñoz-Garach A, Clemente-Postigo M and Tinahones FJ: Importance of gut microbiota in obesity. Eur J Clin Nutr. 72 (Suppl 1):S26–S37. 2019.PubMed/NCBI View Article : Google Scholar | |
Passos MDCF and Moraes-Filho JP: Intestinal microbiota in digestive diseases. Arq Gastroenterol. 54:255–262. 2017.PubMed/NCBI View Article : Google Scholar | |
Mörkl S, Butler MI, Holl A, Cryan JF and Dinan TG: Probiotics and the microbiota-gut-brain axis: Focus on psychiatry. Curr Nutr Rep. 9:171–182. 2020.PubMed/NCBI View Article : Google Scholar | |
Freedman SN, Shahi SK and Mangalam AK: The ‘Gut Feeling’: Breaking down the role of gut microbiome in multiple sclerosis. Neurotherapeutics. 15:109–125. 2018.PubMed/NCBI View Article : Google Scholar | |
Altieri C, Speranza B, Corbo MR, Sinigaglia M and Bevilacqua A: Gut-Microbiota, and multiple sclerosis: Background, evidence, and perspectives. Nutrients. 15(942)2023.PubMed/NCBI View Article : Google Scholar | |
Wang HX and Wang YP: Gut microbiota-brain axis. Chin Med J (Engl). 129:2373–2380. 2016.PubMed/NCBI View Article : Google Scholar | |
De Luca F and Shoenfeld Y: The microbiome in autoimmune diseases. Clin Exp Immunol. 195:74–85. 2019.PubMed/NCBI View Article : Google Scholar | |
Forssberg H: Microbiome programming of brain development: Implications for neurodevelopmental disorders. Dev Med Child Neurol. 61:744–749. 2019.PubMed/NCBI View Article : Google Scholar | |
Sharon G, Sampson TR, Geschwind DH and Mazmanian SK: The central nervous system and the gut microbiome. Cell. 167:915–932. 2016.PubMed/NCBI View Article : Google Scholar | |
Kesika P, Suganthy N, Sivamaruthi BS and Chaiyasut C: Role of gut-brain axis, gut microbial composition, and probiotic intervention in Alzheimer's disease. Life Sci. 264(118627)2021.PubMed/NCBI View Article : Google Scholar | |
Gotkine M, Kviatcovsky D and Elinav E: Amyotrophic lateral sclerosis and intestinal microbiota-toward establishing cause and effect. Gut Microbes. 11:1833–1841. 2020.PubMed/NCBI View Article : Google Scholar | |
Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, Zhu D, Koya JB, Wei L, Li J and Chen ZS: Microbiota in health and diseases. Signal Transduct Target Ther. 7(135)2022.PubMed/NCBI View Article : Google Scholar | |
Vasudha M, Prashantkumar CS, Bellurkar M, Kaveeshwar V and Gayathri D: Probiotic potential of β-galactosidase-producing lactic acid bacteria from fermented milk and their molecular characterization. Biomed Rep. 18(23)2023.PubMed/NCBI View Article : Google Scholar | |
Markowiak P and Śliżewska K: Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients. 9(1021)2017.PubMed/NCBI View Article : Google Scholar | |
Marietta E, Mangalam AK, Taneja V and Murray JA: Intestinal dysbiosis in, and enteral bacterial therapies for, systemic autoimmune diseases. Front Immunol. 11(573079)2020.PubMed/NCBI View Article : Google Scholar | |
Cryan JF, O'Riordan KJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV, et al: The microbiota-gut-brain axis. Physiol Rev. 99:1877–2013. 2019.PubMed/NCBI View Article : Google Scholar | |
Klineova S and Lublin FD: Clinical course of multiple sclerosis. Cold Spring Harb Perspect Med. 8(a028928)2018.PubMed/NCBI View Article : Google Scholar | |
Walton C, King R, Rechtman L, Kaye W, Leray E, Marrie RA, Robertson N, La Rocca N, Uitdehaag B, van der Mei I, et al: Rising prevalence of multiple sclerosis worldwide: Insights from the Atlas of MS, third edition. Mult Scler. 26:1816–1821. 2020.PubMed/NCBI View Article : Google Scholar | |
Iacobaeus E, Arrambide G, Amato MP, Derfuss T, Vukusic S, Hemmer B, Tintore M and Brundin L: 2018 ECTRIMS Focused Workshop Group. Aggressive multiple sclerosis (1): Towards a definition of the phenotype. Mult Scler. 26(1352458520925369)2020.PubMed/NCBI View Article : Google Scholar | |
Olsson T, Barcellos LF and Alfredsson L: Interactions between genetic, lifestyle and environmental risk factors for multiple sclerosis. Nat Rev Neurol. 13:25–36. 2017.PubMed/NCBI View Article : Google Scholar | |
Cotsapas C and Mitrovic M: Genome-wide association studies of multiple sclerosis. Clin Transl Immunology. 7(e1018)2018.PubMed/NCBI View Article : Google Scholar | |
López-Gómez J, Sacristán-Enciso B, Caro-Miró MA and Querol Pascual MR: Clinically isolated syndrome: Diagnosis and risk of developing clinically definite multiple sclerosis. Neurologia (Engl Ed). S0213-4853(21)(00028-1)2021.PubMed/NCBI View Article : Google Scholar : (Epub ahead of print). | |
Thompson AJ, Baranzini SE, Geurts J, Hemmer B and Ciccarelli O: Multiple sclerosis. Lancet. 391:1622–1636. 2018.PubMed/NCBI View Article : Google Scholar | |
van der Vuurst de Vries RM, Wong YYM, Mescheriakova JY, van Pelt ED, Runia TF, Jafari N, Siepman TA, Melief MJ, Wierenga-Wolf AF, van Luijn MM, et al: High neurofilament levels are associated with clinically definite multiple sclerosis in children and adults with clinically isolated syndrome. Mult Scler. 25:958–967. 2019.PubMed/NCBI View Article : Google Scholar | |
Sorensen PS, Sellebjerg F, Hartung HP, Montalban X, Comi G and Tintoré M: The apparently milder course of multiple sclerosis: Changes in the diagnostic criteria, therapy and natural history. Brain. 143:2637–2652. 2020.PubMed/NCBI View Article : Google Scholar | |
Yuan S, Xiong Y and Larsson SC: An atlas on risk factors for multiple sclerosis: A Mendelian randomization study. J Neurol. 268:114–124. 2021.PubMed/NCBI View Article : Google Scholar | |
Ilchmann-Diounou H and Menard S: Psychological stress, intestinal barrier dysfunctions, and autoimmune disorders: An overview. Front Immunol. 11(1823)2020.PubMed/NCBI View Article : Google Scholar | |
Riccio P and Rossano R: Diet, Gut microbiota, and vitamins D + A in multiple sclerosis. Neurotherapeutics. 15:75–91. 2018.PubMed/NCBI View Article : Google Scholar | |
Scheperjans F: Can microbiota research change our understanding of neurodegenerative diseases? Neurodegener Dis Manag. 6:81–85. 2016.PubMed/NCBI View Article : Google Scholar | |
Parodi B and Kerlero de Rosbo N: The gut-brain axis in multiple sclerosis. is its dysfunction a pathological trigger or a consequence of the disease? Front Immunol. 12(718220)2021.PubMed/NCBI View Article : Google Scholar | |
Wu C, Yosef N, Thalhamer T, Zhu C, Xiao S, Kishi Y, Regev A and Kuchroo VK: Induction of Pathogenic TH17 Cells by Inducible Salt-Sensing Kinase SGK1. Nature. 496:513–517. 2013.PubMed/NCBI View Article : Google Scholar | |
Wilck N, Matus MG, Kearney SM, Olesen SW, Forslund K, Bartolomaeus H, Haase S, Mähler A, Balogh A, Markó L, et al: Salt-Responsive Gut Commensal modulates TH17 axis and disease. Nature. 551:585–589. 2017.PubMed/NCBI View Article : Google Scholar | |
Farez MF, Fiol MP, Gaitán MI, Quintana FJ and Correale J: Sodium intake is associated with increased disease activity in multiple sclerosis. J Neurol Neurosurg Psychiatry. 86:26–31. 2015.PubMed/NCBI View Article : Google Scholar | |
Chen J, Chia N, Kalari KR, Yao JZ, Novotna M, Paz Soldan MM, Luckey DH, Marietta EV, Jeraldo PR, Chen X, et al: Multiple sclerosis patients have a distinct gut microbiota compared to healthy controls. Sci Rep. 6(28484)2016.PubMed/NCBI View Article : Google Scholar | |
Moser T, Akgün K, Proschmann U, Sellner J and Ziemssen T: The role of TH17 cells in multiple sclerosis: Therapeutic implications. Autoimmun Rev. 19(102647)2020.PubMed/NCBI View Article : Google Scholar | |
Rutsch A, Kantsjö JB and Ronchi F: The gut-brain axis: How microbiota and host inflammasome influence brain physiology and pathology. Front Immunol. 11(604179)2020.PubMed/NCBI View Article : Google Scholar | |
Gentile F, Doneddu PE, Riva N, Nobile-Orazio E and Quattrini A: Diet, microbiota and brain health: Unraveling the network intersecting metabolism and neurodegeneration. Int J Mol Sci. 21(7471)2020.PubMed/NCBI View Article : Google Scholar | |
Chidambaram SB, Essa MM, Rathipriya AG, Bishir M, Ray B, Mahalakshmi AM, Tousif AH, Sakharkar MK, Kashyap RS, Friedland RP and Monaghan TM: Gut dysbiosis, defective autophagy and altered immune responses in neurodegenerative diseases: Tales of a vicious cycle. Pharmacol Ther. 231(107988)2022.PubMed/NCBI View Article : Google Scholar | |
Cosorich I, Dalla-Costa G, Sorini C, Ferrarese R, Messina MJ, Dolpady J, Radice E, Mariani A, Testoni PA, Canducci F, et al: High frequency of intestinal TH17 cells correlates with microbiota alterations and disease activity in multiple sclerosis. Sci Adv. 3(e1700492)2017.PubMed/NCBI View Article : Google Scholar | |
Vijayakumar TM, Kumar RM, Agrawal A, Dubey GP and Ilango K: Comparative inhibitory potential of selected dietary bioactive polyphenols, phytosterols on CYP3A4 and CYP2D6 with fluorometric high-throughput screening. J Food Sci Technol. 52:4537–4543. 2015.PubMed/NCBI View Article : Google Scholar | |
Tankou SK, Regev K, Healy BC, Cox LM, Tjon E, Kivisakk P, Vanande IP, Cook S, Ghandi R, Glanz B, et al: Investigation of probiotics in multiple sclerosis. Mult Scler. 24:58–63. 2018.PubMed/NCBI View Article : Google Scholar | |
Kouchaki E, Tamtaji OR, Salami M, Bahmani F, Daneshvar Kakhaki R, Akbari E, Tajabadi-Ebrahimi M, Jafari P and Asemi Z: Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin Nutr. 36:1245–1249. 2017.PubMed/NCBI View Article : Google Scholar | |
Borody T, Leis S, Campbell J, Torres M and Nowak A: Fecal Microbiota Transplantation (FMT) in Multiple Sclerosis (Ms). Am J Gast. 106 (Suppl 2)(S352)2011. | |
Engen PA, Zaferiou A, Rasmussen H, Naqib A, Green SJ, Fogg LF, Forsyth CB, Raeisi S, Hamaker B and Keshavarzian A: Single-Arm, non-randomized, time series, single-subject study of fecal microbiota transplantation in multiple sclerosis. Front Neurol. 11(978)2020.PubMed/NCBI View Article : Google Scholar | |
Rashmi BS and Gayathri D: Molecular characterization of gluten hydrolysing Bacillus sp. and their efficacy and biotherapeutic potential as probiotics using Caco-2 cell line. J Appl Microbiol. 123:759–772. 2017.PubMed/NCBI View Article : Google Scholar | |
Kumara SS, Gayathri D, Hariprasad P, Venkateswaran G and Swamy CT: In vivo AFB1 detoxification by Lactobacillus fermentum LC5/a with chlorophyll and immunopotentiating activity in albino mice. Toxicon. 187:214–222. 2020.PubMed/NCBI View Article : Google Scholar | |
Tamtaji OR, Kouchaki E, Salami M, Aghadavod E, Akbari E, Tajabadi-Ebrahimi M and Asemi Z: The effects of probiotic supplementation on gene expression related to inflammation, insulin, and lipids in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. J Am Coll Nutr. 36:660–665. 2017.PubMed/NCBI View Article : Google Scholar | |
Duscha A, Gisevius B, Hirschberg S, Yissachar N, Stangl GI, Eilers E, Dawin E, Bader V, Haase S, Kaisler J, et al: Proprionic acid shapes the multiple sclerosis disease course by an immunomodulatory mechanism. Cell. 180:1067–1080. e16. 2020.PubMed/NCBI View Article : Google Scholar | |
Wekerle H: The gut-brain connection: Triggering of brain autoimmune disease by commensal gut bacteria. Rheumatology (Oxford). 55 (suppl 2):ii68–ii75. 2016.PubMed/NCBI View Article : Google Scholar | |
Miyauchi E, Kim SW, Suda W, Kawasumi M, Onawa S, Taguchi-Atarashi N, Morita H, Taylor TD, Hattori M and Ohno H: Gut microorganisms act together to exacerbate inflammation in spinal cords. Nature. 585:102–106. 2020.PubMed/NCBI View Article : Google Scholar | |
Bernardo-Castro S, Sousa JA, Brás A, Cecília C, Rodrigues B, Almendra L, Machado C, Santo G, Silva F, Ferreira L, et al: Pathophysiology of blood-brain barrier permeability throughout the different stages of ischemic stroke and its implication on hemorrhagic transformation and recovery. Front Neurol. 11(594672)2020.PubMed/NCBI View Article : Google Scholar | |
Buscarinu MC, Romano S, Mechelli R, Pizzolato Umeton R, Ferraldeschi M, Fornasiero A, Reniè R, Cerasoli B, Morena E, Romano C, et al: Intestinal permeability in relapsing-remitting multiple sclerosis. Neurotherapeutics. 15:68–74. 2018.PubMed/NCBI View Article : Google Scholar | |
Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Tóth M, Korecka A, Bakocevic N, Ng LG, Kundu P, et al: The gut microbiota influences blood-brain barrier permeability in mice. Sci Transl Med. 6(263ra158)2014.PubMed/NCBI View Article : Google Scholar | |
Bermúdez-Morales VH, Fierros G, Lopez RL, Martínez-Nava G, Flores-Aldana M, Flores-Rivera J and Hernández-Girón C: Vitamin D receptor gene polymorphisms are associated with multiple sclerosis in Mexican adults. J Neuroimmunol. 306:20–24. 2017.PubMed/NCBI View Article : Google Scholar | |
Püntener U, Booth SG, Perry VH and Teeling JL: Long-term impact of systemic bacterial infection on the cerebral vasculature and microglia. J Neuroinflammation. 9(146)2012.PubMed/NCBI View Article : Google Scholar | |
Yang L, Jama B, Wang H, Labarta-Bajo L, Zúñiga EI and Morris GP: TCRα reporter mice reveal contribution of dual TCRα expression to T cell repertoire and function. Proc Natl Acad Sci USA. 117:32574–32583. 2020.PubMed/NCBI View Article : Google Scholar | |
Li H, Limenitakis JP, Greiff V, Yilmaz B, Schären O, Urbaniak C, Zünd M, Lawson MAE, Young ID, Rupp S, et al: Mucosal or systemic microbiota exposures shape the B cell repertoire. Nature. 584:274–278. 2020.PubMed/NCBI View Article : Google Scholar | |
Round JL and Mazmanian SK: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 107:12204–12209. 2010.PubMed/NCBI View Article : Google Scholar | |
Haghikia A, Jörg S, Duscha A, Berg J, Manzel A, Waschbisch A, Hammer A, Lee DH, May C, Wilck N, et al: Dietary fatty acids directly impact central nervous system autoimmunity via the small intestine. Immunity. 43:817–829. 2015.PubMed/NCBI View Article : Google Scholar | |
López-Taboada I, González-Pardo H and Conejo NM: Western Diet: Implications for brain function and behavior. Front Psychol. 11(564413)2020.PubMed/NCBI View Article : Google Scholar | |
Li JM, Yu R, Zhang LP, Wen SY, Wang SJ, Zhang XY, Xu Q and Kong LD: Dietary fructose-induced gut dysbiosis promotes mouse hippocampal neuroinflammation: A benefit of short-chain fatty acids. Microbiome. 7(98)2019.PubMed/NCBI View Article : Google Scholar | |
Erny D, Hrabě de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, et al: Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 18:965–977. 2015.PubMed/NCBI View Article : Google Scholar | |
Ghimire L, Paudel S, Jin L and Jeyaseelan S: The NLRP6 inflammasome in health and disease. Mucosal Immunol. 13:388–398. 2020.PubMed/NCBI View Article : Google Scholar | |
Dombrowski Y, O'Hagan T, Dittmer M, Penalva R, Mayoral SR, Bankhead P, Fleville S, Eleftheriadis G, Zhao C, Naughton M, et al: Regulatory T cells promote myelin regeneration in the central nervous system. Nat Neurosci. 20:674–680. 2017.PubMed/NCBI View Article : Google Scholar | |
Kurashina R, Denda-Nagai K, Saba K, Hisai T, Hara H and Irimura T: Intestinal lamina propria macrophages upregulate interleukin-10 mRNA in response to signals from commensal bacteria recognized by MGL1/CD301a. Glycobiology. 31:827–837. 2021.PubMed/NCBI View Article : Google Scholar | |
Chen H, Lin W, Zhang Y, Lin L, Chen J, Zeng Y, Zheng M, Zhuang Z, Du H, Chen R and Liu N: IL-10 promotes neurite outgrowth and synapse formation in cultured cortical neurons after the oxygen-glucose deprivation via JAK1/STAT3 pathway. Sci Rep. 6(30459)2016.PubMed/NCBI View Article : Google Scholar | |
Sun S, Luo L, Liang W, Yin Q, Guo J, Rush AM, Lv Z, Liang Q, Fischbach MA, Sonnenburg JL, et al: Bifidobacterium alters the gut microbiota and modulates the functional metabolism of T regulatory cells in the context of immune checkpoint blockade. Proc Natl Acad Sci USA. 117:27509–27515. 2020.PubMed/NCBI View Article : Google Scholar | |
Kang Z, Wang C, Zepp J, Wu L, Sun K, Zhao J, Chandrasekharan U, DiCorleto PE, Trapp BD, Ransohoff RM and Li X: Act1 mediates IL-17-induced EAE pathogenesis selectively in NG2+ glial cells. Nat Neurosci. 16:1401–1408. 2013.PubMed/NCBI View Article : Google Scholar | |
Averina OV, Zorkina YA, Yunes RA, Kovtun AS, Ushakova VM, Morozova AY, Kostyuk GP, Danilenko VN and Chekhonin VP: Bacterial metabolites of human gut microbiota correlating with depression. Int J Mol Sci. 21(9234)2020.PubMed/NCBI View Article : Google Scholar | |
Cui Y, Miao K, Niyaphorn S and Qu X: Production of gamma-aminobutyric acid from lactic acid bacteria: A systematic review. Int J Mol Sci. 21(995)2020.PubMed/NCBI View Article : Google Scholar | |
Anderson G, Rodriguez M and Reiter RJ: Multiple sclerosis: Melatonin, orexin, and ceramide interact with platelet activation coagulation factors and gut-microbiome-derived butyrate in the circadian dysregulation of mitochondria in glia and immune cells. Int J Mol Sci. 20(5500)2019.PubMed/NCBI View Article : Google Scholar | |
Malinova TS, Dijkstra CD and de Vries HE: Serotonin: A mediator of the gut-brain axis in multiple sclerosis. Mult Scler. 24:1144–1150. 2018.PubMed/NCBI View Article : Google Scholar | |
Strandwitz P: Neurotransmitter modulation by the gut microbiota. Brain Res. 1693(Pt B):128–133. 2018.PubMed/NCBI View Article : Google Scholar | |
Bonaz B, Bazin T and Pellissier S: The vagus nerve at the interface of the microbiota-gut-brain axis. Front Neurosci. 12(49)2018.PubMed/NCBI View Article : Google Scholar | |
Wu T, Rayner CK, Young RL and Horowitz M: Gut motility and enteroendocrine secretion. Curr Opin Pharmacol. 13:928–934. 2013.PubMed/NCBI View Article : Google Scholar | |
Hirschberg S, Gisevius B, Duscha A and Haghikia A: Implications of diet and the gut microbiome in neuroinflammatory and neurodegenerative diseases. Int J Mol Sci. 20(3109)2019.PubMed/NCBI View Article : Google Scholar | |
Jhangi S, Gandhi R, Glanz B, Cook S, Nejad P, Ward D, Li N, Gerber G, Bry L and Weiner H: Increased Archaea species and changes with therapy in gut microbiome of multiple sclerosis subjects (S24.001). Neurology. 82 (Suppl 10)(S24.001)2014. | |
Dopkins N, Nagarkatti PS and Nagarkatti M: The role of gut microbiome and associated metabolome in the regulation of neuroinflammation in multiple sclerosis and its implications in attenuating chronic inflammation in other inflammatory and autoimmune disorders. Immunology. 154:178–185. 2018.PubMed/NCBI View Article : Google Scholar | |
Ribeiro MF, Santos AA, Afonso MB, Rodrigues PM, Sa Santos S, Castro RE, Rodrigues CMP and Solá S: Diet-dependent gut microbiota impacts on adult neurogenesis through mitochondrial stress modulation. Brain Commun. 2(fcaa165)2020.PubMed/NCBI View Article : Google Scholar | |
Schepici G, Silvestro S, Bramanti P and Mazzon E: The gut microbiota in multiple sclerosis: An overview of clinical trials. Cell Transplant. 28:1507–1527. 2019.PubMed/NCBI View Article : Google Scholar | |
González-Sanmiguel J, Schuh CMAP, Muñoz-Montesino C, Contreras-Kallens P, Aguayo LG and Aguayo S: Complex interaction between resident microbiota and misfolded proteins: Role in neuroinflammation and neurodegeneration. Cells. 9(2476)2020.PubMed/NCBI View Article : Google Scholar | |
Castillo X, Castro-Obregón S, Gutiérrez-Becker B, Gutiérrez-Ospina G, Karalis N, Khalil AA, Lopez-Noguerola JS, Rodríguez LL, Martínez-Martínez E, Perez-Cruz C, et al: Re-thinking the etiological framework of neurodegeneration. Front Neurosci. 13(728)2019.PubMed/NCBI View Article : Google Scholar | |
Fan Y and Zhang J: Dietary modulation of intestinal microbiota: Future opportunities in experimental autoimmune encephalomyelitis and multiple sclerosis. Front Microbiol. 10(740)2019.PubMed/NCBI View Article : Google Scholar | |
Camara-Lemarroy CR, Metz L, Meddings JB, Sharkey KA and Wee Yong V: The intestinal barrier in multiple sclerosis: Implications for pathophysiology and therapeutics. Brain. 141:1900–1916. 2018.PubMed/NCBI View Article : Google Scholar | |
Shahi SK, Freedman SN and Mangalam AK: Gut microbiome in multiple sclerosis: The players involved and the roles they play. Gut Microbes. 8:607–615. 2017.PubMed/NCBI View Article : Google Scholar | |
Mirza A, Forbes JD, Zhu F, Bernstein CN, Van Domselaar G, Graham M, Waubant E and Tremlett H: The multiple sclerosis gut microbiota: A systematic review. Mult Scler Relat Disord. 37(101427)2020.PubMed/NCBI View Article : Google Scholar | |
Chu F, Shi M, Lang Y, Shen D, Jin T, Zhu J and Cui L: Gut microbiota in multiple sclerosis and experimental autoimmune encephalomyelitis: Current applications and future perspectives. Mediators Inflamm. 2018(8168717)2018.PubMed/NCBI View Article : Google Scholar | |
Miyake S, Kim S, Suda W, Oshima K, Nakamura M, Matsuoka T, Chihara N, Tomita A, Sato W, Kim SW, et al: 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(e0137429)2015.PubMed/NCBI View Article : Google Scholar | |
Madonini ER: Probiotics and allergies: Myth or reality? Eur Ann Allergy Clin Immunol. 46:196–200. 2014.PubMed/NCBI | |
Mcfarland LV and Dublin S: Meta-analysis of probiotics for the treatment of irritable bowel syndrome. World J Gastroenterol. 14:2650–2661. 2008.PubMed/NCBI View Article : Google Scholar | |
Saggioro A: Probiotics in the treatment of irritable bowel syndrome. J Clin Gastroenterol. 38 (6 Suppl):S104–S106. 2004.PubMed/NCBI View Article : Google Scholar | |
Kim HJ, Camilleri M, McKinzie S, Lempke MB, Burton DD, Thomforde GM and Zinsmeister AR: A randomized controlled trial of a probiotic, VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther. 17:895–904. 2003.PubMed/NCBI View Article : Google Scholar | |
Abenavoli L, Scarpellini E, Colica C, Boccuto L, Salehi B, Sharifi-Rad J, Aiello V, Romano B, De Lorenzo A, Izzo AA and Capasso R: Gut microbiota and obesity: A role for probiotics. Nutrient. 11(2690)2019.PubMed/NCBI View Article : Google Scholar | |
Wang X, Liang Z, Wang S, Ma D, Zhu M and Feng J: Role of gut microbiota in multiple sclerosis and potential therapeutic implications. Curr Neuropharmacol. 20:1413–1426. 2022.PubMed/NCBI View Article : Google Scholar |