Probiotics in Treatment of Viral Respiratory Infections and Neuroinflammatory Disorders

Roghayeh Shahbazi, Hamed Yasavoli-Sharahi, Nawal Alsadi, Nafissa Ismail, Chantal Matar, Roghayeh Shahbazi, Hamed Yasavoli-Sharahi, Nawal Alsadi, Nafissa Ismail, Chantal Matar

Abstract

Inflammation is a biological response to the activation of the immune system by various infectious or non-infectious agents, which may lead to tissue damage and various diseases. Gut commensal bacteria maintain a symbiotic relationship with the host and display a critical function in the homeostasis of the host immune system. Disturbance to the gut microbiota leads to immune dysfunction both locally and at distant sites, which causes inflammatory conditions not only in the intestine but also in the other organs such as lungs and brain, and may induce a disease state. Probiotics are well known to reinforce immunity and counteract inflammation by restoring symbiosis within the gut microbiota. As a result, probiotics protect against various diseases, including respiratory infections and neuroinflammatory disorders. A growing body of research supports the beneficial role of probiotics in lung and mental health through modulating the gut-lung and gut-brain axes. In the current paper, we discuss the potential role of probiotics in the treatment of viral respiratory infections, including the COVID-19 disease, as major public health crisis in 2020, and influenza virus infection, as well as treatment of neurological disorders like multiple sclerosis and other mental illnesses.

Keywords: COVID-19; gut microbiota; gut-brain axis; gut-lung axis; immunomodulation; influenza virus infection; multiple sclerosis; neuroinflammation; probiotics; viral respiratory infections.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Role of gut microbiota in the prevention of viral respiratory infections. Commensals-derived fragments and metabolites travel to the lung via systemic circulation and can act as signaling molecules and induce immune responses. Furthermore, activated immune cells travel to the lung via the lymphatic system. Besides, gut bacteria regulate the activation of STAT1 and IFNs signaling, which are involved in antiviral defense genes induction prior to infection and immune-mediated resistance to viral infection. INFs: interferons; STAT1: signal transducer and activator of transcription-1; LPS: Lipopolysaccharide; SCFAs: Short-chain fatty acids. Created with BioRender.com.
Figure 2
Figure 2
Role of gut microbiota in the prevention of neuroinflammation. Microbial products and metabolites can induce brain immunity indirectly by activating signaling pathways or directly through passing BBB. Gut microbiota regulates gut immunity hemostasis and modulates systemic immunity and brain immunity as well. Finally, gut commensal and their metabolites modulate microglia maturation and function, maintain BBB integrity, and prevent neuroinflammation. SCFAs: Short-chain fatty acids; Tregs; t regulatory cells; Th17: T-helper 17. Created with BioRender.com.

References

    1. Rinninella E., Raoul P., Cintoni M., Franceschi F., Miggiano G.A.D., Gasbarrini A., Mele M.C. What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms. 2019;7:14. doi: 10.3390/microorganisms7010014.
    1. Villanueva-Millán M., Perez-Matute P., Oteo J. Gut microbiota: A key player in health and disease. A review focused on obesity. J. Physiol. Biochem. 2015;71:509–525. doi: 10.1007/s13105-015-0390-3.
    1. Thursby E., Juge N. Introduction to the human gut microbiota. Biochem. J. 2017;474:1823–1836. doi: 10.1042/BCJ20160510.
    1. Petersen C., Round J.L. Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 2014;16:1024–1033. doi: 10.1111/cmi.12308.
    1. Carding S., Verbeke K., Vipond D.T., Corfe B.M., Owen L.J. Dysbiosis of the gut microbiota in disease. Microb. Ecol. Health Dis. 2015;26:26191. doi: 10.3402/mehd.v26.26191.
    1. Wu R.Y., Jeffrey M.P., Johnson-Henry K.C., Green-Johnson J.M., Sherman P.M. Impact of prebiotics, probiotics, and gut derived metabolites on host immunity. LymphoSign J. 2016;4:1–24. doi: 10.14785/lymphosign-2016-0012.
    1. Mowat A.M., Agace W.W. Regional specialization within the intestinal immune system. Nat. Rev. Immunol. 2014;14:667–685. doi: 10.1038/nri3738.
    1. Sichetti M., De Marco S., Pagiotti R., Traina G., Pietrella D. Anti-inflammatory effect of multistrain probiotic formulation (L. rhamnosus, B. lactis, and B. longum) Nutrition. 2018;53:95–102. doi: 10.1016/j.nut.2018.02.005.
    1. Kamada N., Seo S.U., Chen G.Y., Núñez G. Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 2013;13:321–335. doi: 10.1038/nri3430.
    1. Belkaid Y., Hand T.W. Role of the Microbiota in Immunity and Inflammation. Cell. 2014;157:121–141. doi: 10.1016/j.cell.2014.03.011.
    1. Caricilli A.M., Castoldi A., Câmara N.O.S. Intestinal barrier: A gentlemen’s agreement between microbiota and immunity. World J. Gastrointest. Pathophysiol. 2014;5:18–32. doi: 10.4291/wjgp.v5.i1.18.
    1. Nishio J., Honda K. Immunoregulation by the gut microbiota. Cell Mol. Life Sci. 2012;69:3635–3650. doi: 10.1007/s00018-012-0993-6.
    1. Anand S., Mande S.S. Diet, Microbiota and Gut-Lung Connection. Front. Microbiol. 2018;9:2147. doi: 10.3389/fmicb.2018.02147.
    1. El Aidy S., Dinan T.G., Cryan J.F. Immune modulation of the brain-gut-microbe axis. Front. Microbiol. 2014;5:146. doi: 10.3389/fmicb.2014.00146.
    1. Azab A., Nassar A., Azab A.N. Anti-inflammatory activity of natural products. Molecules. 2016;21:1321. doi: 10.3390/molecules21101321.
    1. Chen L., Deng H., Cui H., Fang J., Zuo Z., Deng J., Li Y., Wang X., Zhao L. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget. 2018;9:7204–7218. doi: 10.18632/oncotarget.23208.
    1. Frank M.G., Fonken L.K., Watkins L.R., Maier S.F., Lowry C.A. Could probiotics be used to mitigate neuroinflammation? ACS Chem. Neurosci. 2019;10:13–15. doi: 10.1021/acschemneuro.8b00386.
    1. Derwa Y., Gracie D., Hamlin P., Ford A. Systematic review with meta-analysis: The efficacy of probiotics in inflammatory bowel disease. Aliment. Pharmacol. Ther. 2017;46:389–400. doi: 10.1111/apt.14203.
    1. Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S., et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66.
    1. Zhang S., Chen D.C. Facing a new challenge: The adverse effects of antibiotics on gut microbiota and host immunity. Chin. Med. J. 2019;132:1135–1138. doi: 10.1097/CM9.0000000000000245.
    1. Yoon M.Y., Yoon S.S. Disruption of the Gut Ecosystem by Antibiotics. Yonsei Med. J. 2018;59:4–12. doi: 10.3349/ymj.2018.59.1.4.
    1. Yahfoufi N., Mallet J.F., Graham E., Matar C. Role of probiotics and prebiotics in immunomodulation. Curr. Opin. Food Sci. 2018;20:82–91. doi: 10.1016/j.cofs.2018.04.006.
    1. Bermúdez-Brito M., Bermudez-Brito M., Plaza-Díaz J., Muñoz-Quezada S., Gómez-Llorente C., Gil A. Probiotic Mechanisms of Action. Annu. Nutr. Metab. 2012;61:160–174. doi: 10.1159/000342079.
    1. Wang K., Dong H., Qi Y., Pei Z., Yi S., Yang X., Zhao Y., Meng F., Yu S., Zhou T., et al. Lactobacillus casei regulates differentiation of Th17/Treg cells to reduce intestinal inflammation in mice. Can. J. Vet. Res. 2017;81:122–128.
    1. Tanabe S. The Effect of Probiotics and Gut Microbiota on Th17 Cells. Int. Rev. Immunol. 2013;32:511–525. doi: 10.3109/08830185.2013.839665.
    1. Owaga E., Hsieh R.H., Mugendi B., Masuku S., Shih C.K., Chang J.S. Th17 Cells as Potential Probiotic Therapeutic Targets in Inflammatory Bowel Diseases. Int. J. Mol. Sci. 2015;16:20841–20858. doi: 10.3390/ijms160920841.
    1. Plaza-Diaz J., Ruiz-Ojeda F.J., Gil-Campos M., Gil A. Mechanisms of Action of Probiotics. Adv. Nutr. 2019;10(Suppl. 1):S49–S66. doi: 10.1093/advances/nmy063.
    1. Dwivedi M., Kumar P., Laddha N.C., Kemp E.H. Induction of regulatory T cells: A role for probiotics and prebiotics to suppress autoimmunity. Autoimmun Rev. 2016;15:379–392. doi: 10.1016/j.autrev.2016.01.002.
    1. Islam S.U. Clinical uses of probiotics. Medicine. 2016;95:e2658. doi: 10.1097/MD.0000000000002658.
    1. Ganji-Arjenaki M., Rafieian-Kopaei M. Probiotics are a good choice in remission of inflammatory bowel diseases: A meta analysis and systematic review. J. Cell Physiol. 2018;233:2091–2103. doi: 10.1002/jcp.25911.
    1. Budden K.F., Gellatly S.L., Wood D.L., Cooper M.A., Morrison M., Hugenholtz P., Hansbro P.M. Emerging pathogenic links between microbiota and the gut–lung axis. Nat. Rev. Microbiol. 2017;15:55–63. doi: 10.1038/nrmicro.2016.142.
    1. Keely S., Talley N.J., Hansbro P.M. Pulmonary-intestinal cross-talk in mucosal inflammatory disease. Mucosal Immunol. 2012;5:7–18. doi: 10.1038/mi.2011.55.
    1. Baud D., Agri V.D., Gibson G.R., Reid G., Giannoni E. Using Probiotics to Flatten the Curve of Coronavirus Disease COVID-2019 Pandemic. Front. Public Health. 2020;8:186. doi: 10.3389/fpubh.2020.00186.
    1. Rooks M.G., Garrett W.S. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 2016;16:341–352. doi: 10.1038/nri.2016.42.
    1. Zheng D., Liwinski T., Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30:492–506. doi: 10.1038/s41422-020-0332-7.
    1. Bingula R., Filaire M., Radosevic-Robin N., Bey M., Berthon J.-Y., Bernalier-Donadille A., Vasson M.-P., Filaire E. Desired turbulence? Gut-lung axis, immunity, and lung cancer. J. Oncol. 2017;2017:5035371.
    1. Trompette A., Gollwitzer E.S., Yadava K., Sichelstiel A.K., Sprenger N., Ngom-Bru C., Blanchard C., Junt T., Nicod L.P., Harris N.L. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 2014;20:159–166.
    1. Marsland B.J., Trompette A., Gollwitzer E.S. The gut–lung axis in respiratory disease. Ann. Am. Thorac. Soc. 2015;12(Suppl. 2):S150–S156.
    1. Gray L.E., O’Hely M., Ranganathan S., Sly P.D., Vuillermin P. The maternal diet, gut bacteria, and bacterial metabolites during pregnancy influence offspring asthma. Front. Immunol. 2017;8:365. doi: 10.3389/fimmu.2017.00365.
    1. Alonso W.J., Laranjeira B.J., Pereira S.A., Florencio C.M., Moreno E.C., Miller M.A., Giglio R., Schuck-Paim C., Moura F.E. Comparative dynamics, morbidity and mortality burden of pediatric viral respiratory infections in an equatorial city. Pediatr. Infect. Dis. J. 2012;31:e9–e14. doi: 10.1097/INF.0b013e31823883be.
    1. Dang A.T., Marsland B.J. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol. 2019;12:843–850.
    1. Abt M.C., Osborne L.C., Monticelli L.A., Doering T.A., Alenghat T., Sonnenberg G.F., Paley M.A., Antenus M., Williams K.L., Erikson J. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity. 2012;37:158–170.
    1. Filyk H.A., Sharon A.J., Fonseca N.M., Simister R.L., Yuen W., Hardman B.K., Robinson H.G., Seo J.H., Rocha-Pereira J., Welch I., et al. STAT1-dependent tolerance of intestinal viral infection. bioRxiv. 2020 doi: 10.1101/2020.02.13.936252.
    1. Forsythe P. Probiotics and lung immune responses. Ann. Am. Thorac. Soc. 2014;11(Suppl. 1):S33–S37.
    1. Mortaz E., Adcock I.M., Folkerts G., Barnes P.J., Paul Vos A., Garssen J. Probiotics in the management of lung diseases. Mediators Inflamm. 2013;2013:751068.
    1. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783–801. doi: 10.1016/j.cell.2006.02.015.
    1. Mahooti M., Miri S.M., Abdolalipour E., Ghaemi A. The immunomodulatory effects of probiotics on respiratory viral infections: A hint for COVID-19 treatment? Microb. Pathog. 2020;148:104452.
    1. Sun J., He W.-T., Wang L., Lai A., Ji X., Zhai X., Li G., Suchard M.A., Tian J., Zhou J. COVID-19: Epidemiology, evolution, and cross-disciplinary perspectives. Trends Mol. Med. 2020;26:483–495.
    1. Li Q., Guan X., Wu P., Wang X., Zhou L., Tong Y., Ren R., Leung K.S., Lau E.H., Wong J.Y. Early transmission dynamics in Wuhan, China, of novel coronavirus–infected pneumonia. N. Engl. J. Med. 2020;382:1199–1207.
    1. Dhar D., Mohanty A. Gut microbiota and Covid-19-possible link and implications. Virus Res. 2020;258:198018.
    1. Abdollahi E., Champredon D., Langley J.M., Galvani A.P., Moghadas S.M. Temporal estimates of case-fatality rate for COVID-19 outbreaks in Canada and the United States. CMAJ. 2020;192:E666–E670. doi: 10.1503/cmaj.200711.
    1. Effenberger M., Grabherr F., Mayr L., Schwaerzler J., Nairz M., Seifert M., Hilbe R., Seiwald S., Scholl-Buergi S., Fritsche G. Faecal calprotectin indicates intestinal inflammation in COVID-19. Gut. 2020;69:1543–1544.
    1. Ceccarelli G., Scagnolari C., Pugliese F., Mastroianni C.M., d’Ettorre G. Probiotics and COVID-19. Lancet Gastroenterol. Hepatol. 2020;5:721–722.
    1. Groves H.T., Higham S.L., Moffatt M.F., Cox M.J., Tregoning J.S. Respiratory viral infection alters the gut microbiota by inducing inappetence. mBio. 2020;11:e03236–e03319. doi: 10.1128/mBio.03236-19.
    1. Dickson R.P. The microbiome and critical illness. Lancet Respir. Med. 2016;4:59–72. doi: 10.1016/S2213-2600(15)00427-0.
    1. Lake M.A. What we know so far: COVID-19 current clinical knowledge and research. Clin. Med. 2020;20:124–127. doi: 10.7861/clinmed.2019-coron.
    1. Liang T. Handbook of COVID-19 Prevention and Treatment. Zhejiang University School of Medicine; Zhejiang, China: 2020.
    1. Mak J.W., Chan F.K., Ng S.C. Probiotics and COVID-19: One size does not fit all. Lancet Gastroenterol. Hepatol. 2020;5:644–645. doi: 10.1016/S2468-1253(20)30122-9.
    1. Aguila E.J.T., Lontok M.A.D.C., Aguila E.J.T. Letter: Role of probiotics in the COVID-19 pandemic. Aliment. Pharmacol. Ther. 2020;52:931–932.
    1. Zuo T., Zhang F., Lui G.C., Yeoh Y.K., Li A.Y., Zhan H., Wan Y., Chung A., Cheung C.P., Chen N. Alterations in Gut Microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology. 2020;159:944–955.e8.
    1. Zuo T., Liu Q., Zhang F., Lui G.C., Tso E.Y., Yeoh Y.K., Chen Z., Boon S.S., Chan F.K., Chan P.K., et al. Depicting SARS-CoV-2 faecal viral activity in association with gut microbiota composition in patients with COVID-19. Gut. 2020;2020:322294. doi: 10.1136/gutjnl-2020-322294.
    1. Gagliardi A., Totino V., Cacciotti F., Iebba V., Neroni B., Bonfiglio G., Trancassini M., Passariello C., Pantanella F., Schippa S. Rebuilding the Gut Microbiota Ecosystem. Int. J. Environ. Res. Public Health. 2018;15:1679. doi: 10.3390/ijerph15081679.
    1. Enaud R., Prevel R., Ciarlo E., Beaufils F., Wieërs G., Guery B., Delhaes L. The gut-lung axis in health and respiratory diseases: A place for inter-organ and inter-kingdom crosstalks. Front. Cell Infect. Microbiol. 2020;10:9. doi: 10.3389/fcimb.2020.00009.
    1. McAleer J.P., Kolls J.K. Contributions of the intestinal microbiome in lung immunity. Eur. J. Immunol. 2018;48:39–49. doi: 10.1002/eji.201646721.
    1. Vinderola G., Matar C., Perdigón G. Milk fermentation products of L. helveticus R389 activate calcineurin as a signal to promote gut mucosal immunity. BMC Immunol. 2007;8:19. doi: 10.1186/1471-2172-8-19.
    1. Vinderola G., Matar C., Perdigón G. Milk fermented by Lactobacillus helveticus R389 and its non-bacterial fraction confer enhanced protection against Salmonella enteritidis serovar Typhimurium infection in mice. Immunobiology. 2007;212:107–118. doi: 10.1016/j.imbio.2006.09.003.
    1. LeBlanc J.G., Matar C., Valdéz J.C., LeBlanc J., Perdigon G. Immunomodulating effects of peptidic fractions issued from milk fermented with Lactobacillus helveticus. J. Dairy Sci. 2002;85:2733–2742. doi: 10.3168/jds.S0022-0302(02)74360-9.
    1. Leblanc J., Fliss I., Matar C. Induction of a humoral immune response following an Escherichia coli O157:H7 infection with an immunomodulatory peptidic fraction derived from Lactobacillus helveticus-fermented milk. Clin. Diagn. Lab. Immunol. 2004;11:1171–1181. doi: 10.1128/CDLI.11.6.1171-1181.2004.
    1. Matar C., Valdez J.C., Medina M., Rachid M., Perdigon G. Immunomodulating effects of milks fermented by Lactobacillus helveticus and its non-proteolytic variant. J. Dairy Res. 2001;68:601–609. doi: 10.1017/S0022029901005143.
    1. Matricardi P.M., Dal Negro R.W., Nisini R. The first, holistic immunological model of COVID-19: Implications for prevention, diagnosis, and public health measures. Pediatr. Allergy Immunol. 2020 doi: 10.1111/pai.13271.
    1. Shinde T., Hansbro P.M., Sohal S.S., Dingle P., Eri R., Stanley R. Microbiota modulating nutritional approaches to countering the effects of viral respiratory infections including SARS-CoV-2 through promoting metabolic and immune fitness with probiotics and plant bioactives. Microorganisms. 2020;8:921. doi: 10.3390/microorganisms8060921.
    1. Hardy H., Harris J., Lyon E., Beal J., Foey A.D. Probiotics, prebiotics and immunomodulation of gut mucosal defences: Homeostasis and immunopathology. Nutrients. 2013;5:1869–1912. doi: 10.3390/nu5061869.
    1. King S., Glanville J., Sanders M.E., Fitzgerald A., Varley D. Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: A systematic review and meta-analysis. Br. J. Nutr. 2014;112:41–54. doi: 10.1017/S0007114514000075.
    1. Han H., Ma Q., Li C., Liu R., Zhao L., Wang W., Zhang P., Liu X., Gao G., Liu F. Profiling serum cytokines in COVID-19 patients reveals IL-6 and IL-10 are disease severity predictors. Emerg. Microbes Infect. 2020;9:1123–1130. doi: 10.1080/22221751.2020.1770129.
    1. Villapol S. Gastrointestinal symptoms associated with COVID-19: Impact on the gut microbiome. Transl. Res. 2020;226:57–69. doi: 10.1016/j.trsl.2020.08.004.
    1. Milajerdi A., Mousavi S.M., Sadeghi A., Salari-Moghaddam A., Parohan M., Larijani B., Esmaillzadeh A. The effect of probiotics on inflammatory biomarkers: A meta-analysis of randomized clinical trials. Eur. J. Nutr. 2020;59:633–649. doi: 10.1007/s00394-019-01931-8.
    1. Carter C., Osborn M., Agagah G., Aedy H., Notter J. COVID-19 disease: Invasive ventilation. Clin. Integr. Care. 2020;1:100004. doi: 10.1016/j.intcar.2020.100004.
    1. Hanada S., Pirzadeh M., Carver K.Y., Deng J.C. Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. Front Immunol. 2018;9:2640. doi: 10.3389/fimmu.2018.02640.
    1. Pang I.K., Iwasaki A. Inflammasomes as mediators of immunity against influenza virus. Trends Immunol. 2011;32:34–41. doi: 10.1016/j.it.2010.11.004.
    1. Yaqoob P. Ageing, immunity and influenza: A role for probiotics? Proc. Nutr. Soc. 2014;73:309–317. doi: 10.1017/S0029665113003777.
    1. Takeda S., Takeshita M., Kikuchi Y., Dashnyam B., Kawahara S., Yoshida H., Watanabe W., Muguruma M., Kurokawa M. Efficacy of oral administration of heat-killed probiotics from Mongolian dairy products against influenza infection in mice: Alleviation of influenza infection by its immunomodulatory activity through intestinal immunity. Int. Immunopharmacol. 2011;11:1976–1983. doi: 10.1016/j.intimp.2011.08.007.
    1. Ichinohe T., Pang I.K., Kumamoto Y., Peaper D.R., Ho J.H., Murray T.S., Iwasaki A. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA. 2011;108:5354–5359. doi: 10.1073/pnas.1019378108.
    1. Lehtoranta L., Pitkäranta A., Korpela R. Probiotics in respiratory virus infections. Eur. J. Clin. Microbiol. Infect. Dis. 2014;33:1289–1302. doi: 10.1007/s10096-014-2086-y.
    1. Kawase M., He F., Kubota A., Yoda K., Miyazawa K., Hiramatsu M. Heat-killed Lactobacillus gasseri TMC0356 protects mice against influenza virus infection by stimulating gut and respiratory immune responses. FEMS Immunol. Med. Microbiol. 2012;64:280–288. doi: 10.1111/j.1574-695X.2011.00903.x.
    1. Yitbarek A., Taha-Abdelaziz K., Hodgins D.C., Read L., Nagy É., Weese J.S., Caswell J.L., Parkinson J., Sharif S. Gut microbiota-mediated protection against influenza virus subtype H9N2 in chickens is associated with modulation of the innate responses. Sci. Rep. 2018;8:13189. doi: 10.1038/s41598-018-31613-0.
    1. Dudakov J.A., van den Brink M.R.M. Chapter 6—Strategies to Improve Posttransplant Immunity. In: Socié G., Zeiser R., Blazar B.R., editors. Immune Biology of Allogeneic Hematopoietic Stem Cell Transplantation. 2nd ed. Academic Press; Cambridge, MA, USA: 2019. pp. 89–105.
    1. Kawahara T., Takahashi T., Oishi K., Tanaka H., Masuda M., Takahashi S., Takano M., Kawakami T., Fukushima K., Kanazawa H. Consecutive oral administration of Bifidobacterium longum MM-2 improves the defense system against influenza virus infection by enhancing natural killer cell activity in a murine model. Microbiol. Immunol. 2015;59:1–12. doi: 10.1111/1348-0421.12210.
    1. Iwabuchi N., Xiao J.-Z., Yaeshima T., Iwatsuki K. Oral administration of Bifidobacterium longum ameliorates influenza virus infection in mice. Biol. Pharm. Bull. 2011;34:1352–1355. doi: 10.1248/bpb.34.1352.
    1. Youn H.-N., Lee D.-H., Lee Y.-N., Park J.-K., Yuk S.-S., Yang S.-Y., Lee H.-J., Woo S.-H., Kim H.-M., Lee J.-B. Intranasal administration of live Lactobacillus species facilitates protection against influenza virus infection in mice. Antiviral Res. 2012;93:138–143. doi: 10.1016/j.antiviral.2011.11.004.
    1. Iwabuchi N., Yonezawa S., Odamaki T., Yaeshima T., Iwatsuki K., Xiao J.-Z. Immunomodulating and anti-infective effects of a novel strain of Lactobacillus paracasei that strongly induces interleukin-12. FEMS Immunol. Med. Microbiol. 2012;66:230–239. doi: 10.1111/j.1574-695X.2012.01003.x.
    1. Waki N., Yajima N., Suganuma H., Buddle B., Luo D., Heiser A., Zheng T. Oral administration of L actobacillus brevis KB 290 to mice alleviates clinical symptoms following influenza virus infection. Lett. Appl. Microbiol. 2014;58:87–93. doi: 10.1111/lam.12160.
    1. Goto H., Sagitani A., Ashida N., Kato S., Hirota T., Shinoda T., Yamamoto N. Anti-influenza virus effects of both live and non-live Lactobacillus acidophilus L-92 accompanied by the activation of innate immunity. Br. J. Nutr. 2013;110:1810–1818. doi: 10.1017/S0007114513001104.
    1. Park M.K., Vu N., Kwon Y.M., Lee Y.T., Yoo S., Cho Y.-H., Hong S.-M., Hwang H.S., Ko E.-J., Jung Y.-J. Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity. PLoS ONE. 2013;8:e75368. doi: 10.1371/journal.pone.0075368.
    1. Yeo J.M., Lee H.J., Kim J.W., Lee J.B., Park S.Y., Choi I.S., Song C.S. Lactobacillus fermentum CJL-112 protects mice against influenza virus infection by activating T-helper 1 and eliciting a protective immune response. Int. Immunopharmacol. 2014;18:50–54. doi: 10.1016/j.intimp.2013.10.020.
    1. Asama T., Uematsu T., Kobayashi N., Tatefuji T., Hashimoto K. Oral administration of heat-killed Lactobacillus kunkeei YB38 improves murine influenza pneumonia by enhancing IgA production. Biosci. Microbiota Food Health. 2017;36:1–9. doi: 10.12938/bmfh.16-010.
    1. Waki N., Matsumoto M., Fukui Y., Suganuma H. Effects of probiotic Lactobacillus brevis KB290 on incidence of influenza infection among schoolchildren: An open-label pilot study. Lett. Appl. Microbiol. 2014;59:565–571. doi: 10.1111/lam.12340.
    1. Boge T., Rémigy M., Vaudaine S., Tanguy J., Bourdet-Sicard R., Van Der Werf S. A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine. 2009;27:5677–5684. doi: 10.1016/j.vaccine.2009.06.094.
    1. Bosch M., Mendez M., Perez M., Farran A., Fuentes M., Cune J. Lactobacillus plantarum CECT7315 and CECT7316 stimulate immunoglobulin production after influenza vaccination in elderly. Nutr. Hosp. 2012;27:504–509.
    1. Kanauchi O., Andoh A., AbuBakar S., Yamamoto N. Probiotics and Paraprobiotics in Viral Infection: Clinical Application and Effects on the Innate and Acquired Immune Systems. Curr. Pharm. Des. 2018;24:710–717. doi: 10.2174/1381612824666180116163411.
    1. Van Puyenbroeck K., Hens N., Coenen S., Michiels B., Beunckens C., Molenberghs G., Van Royen P., Verhoeven V. Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: A randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am. J. Clin. Nutr. 2012;95:1165–1171. doi: 10.3945/ajcn.111.026831.
    1. Kumpu M., Lehtoranta L., Roivainen M., Rönkkö E., Ziegler T., Söderlund-Venermo M., Kautiainen H., Järvenpää S., Kekkonen R., Hatakka K., et al. The use of the probiotic Lactobacillus rhamnosus GG and viral findings in the nasopharynx of children attending day care. J. Med. Virol. 2013;85:1632–1638. doi: 10.1002/jmv.23623.
    1. Kinoshita T., Maruyama K., Suyama K., Nishijima M., Akamatsu K., Jogamoto A., Katakami K., Saito I. The effects of OLL1073R-1 yogurt intake on influenza incidence and immunological markers among women healthcare workers: A randomized controlled trial. Food Funct. 2019;10:8129–8136. doi: 10.1039/C9FO02128K.
    1. Mayer E.A., Tillisch K., Gupta A. Gut/brain axis and the microbiota. J. Clin. Investig. 2015;125:926–938. doi: 10.1172/JCI76304.
    1. Osadchiy V., Martin C.R., Mayer E.A. The Gut-Brain Axis and the Microbiome: Mechanisms and Clinical Implications. Clin. Gastroenterol. Hepatol. 2019;17:322–332. doi: 10.1016/j.cgh.2018.10.002.
    1. Carabotti M., Scirocco A., Maselli M.A., Severi C. The gut-brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 2015;28:203–209.
    1. Cryan J.F., Dinan T.G. Microbiota and neuroimmune signalling—Metchnikoff to microglia. Nat. Rev. Gastroenterol. Hepatol. 2015;12:494–496. doi: 10.1038/nrgastro.2015.127.
    1. Abdel-Haq R., Schlachetzki J.C.M., Glass C.K., Mazmanian S.K. Microbiome–microglia connections via the gut–brain axis. J. Exp. Med. 2018;216:41–59. doi: 10.1084/jem.20180794.
    1. Parker A., Fonseca S., Carding S.R. Gut microbes and metabolites as modulators of blood-brain barrier integrity and brain health. Gut Microbes. 2020;11:135–157. doi: 10.1080/19490976.2019.1638722.
    1. Logsdon A.F., Erickson M.A., Rhea E.M., Salameh T.S., Banks W.A. Gut reactions: How the blood-brain barrier connects the microbiome and the brain. Exp. Biol. Med. 2018;243:159–165. doi: 10.1177/1535370217743766.
    1. Cryan J.F., Dinan T.G. Mind-altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 2012;13:701–712. doi: 10.1038/nrn3346.
    1. Mayer E.A. Gut feelings: The emerging biology of gut-brain communication. Nat. Rev. Neurosci. 2011;12:453–466. doi: 10.1038/nrn3071.
    1. Houlden A., Goldrick M., Brough D., Vizi E.S., Lénárt N., Martinecz B., Roberts I.S., Denes A. Brain injury induces specific changes in the caecal microbiota of mice via altered autonomic activity and mucoprotein production. Brain Behav. Immun. 2016;57:10–20. doi: 10.1016/j.bbi.2016.04.003.
    1. Miyake S., Kim S., Suda W., Oshima K., Nakamura M., Matsuoka T., Chihara N., Tomita A., Sato W., Kim S.-W. 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. 2015;10:e0137429.
    1. Zeng Q., Gong J., Liu X., Chen C., Sun X., Li H., Zhou Y., Cui C., Wang Y., Yang Y. Gut dysbiosis and lack of short chain fatty acids in a Chinese cohort of patients with multiple sclerosis. Neurochem. Int. 2019;129:104468.
    1. Saresella M., Marventano I., Barone M., La Rosa F., Piancone F., Mendozzi L., d’Arma A., Rossi V., Pugnetti L., Roda G., et al. Alterations in Circulating Fatty Acid Are Associated with Gut Microbiota Dysbiosis and Inflammation in Multiple Sclerosis. Front. Immunol. 2020;11:1390.
    1. Ma Q., Xing C., Long W., Wang H.Y., Liu Q., Wang R.-F. Impact of microbiota on central nervous system and neurological diseases: The gut-brain axis. J. Neuroinflamm. 2019;16:53.
    1. Leclercq S., Mian F.M., Stanisz A.M., Bindels L.B., Cambier E., Ben-Amram H., Koren O., Forsythe P., Bienenstock J. Low-dose penicillin in early life induces long-term changes in murine gut microbiota, brain cytokines and behavior. Nat. Commun. 2017;8:15062.
    1. Minato T., Maeda T., Fujisawa Y., Tsuji H., Nomoto K., Ohno K., Hirayama M. Progression of Parkinson’s disease is associated with gut dysbiosis: Two-year follow-up study. PLoS ONE. 2017;12:e0187307.
    1. Houser M.C., Tansey M.G. The gut-brain axis: Is intestinal inflammation a silent driver of Parkinson’s disease pathogenesis? NPJ Parkinsons Dis. 2017;3:1–9.
    1. Santos S.F., de Oliveira H.L., Yamada E.S., Neves B.C., Pereira A. The Gut and Parkinson’s Disease—A Bidirectional Pathway. Front. Neurol. 2019;10:574.
    1. Chen C., Ahn E.H., Kang S.S., Liu X., Alam A., Ye K. Gut dysbiosis contributes to amyloid pathology, associated with C/EBPβ/AEP signaling activation in Alzheimer’s disease mouse model. Sci. Adv. 2020;6:eaba0466.
    1. Wang X., Sun G., Feng T., Zhang J., Huang X., Wang T., Xie Z., Chu X., Yang J., Wang H. Sodium oligomannate therapeutically remodels gut microbiota and suppresses gut bacterial amino acids-shaped neuroinflammation to inhibit Alzheimer’s disease progression. Cell Res. 2019;29:787–803.
    1. Sochocka M., Donskow-Łysoniewska K., Diniz B.S., Kurpas D., Brzozowska E., Leszek J. The gut microbiome alterations and inflammation-driven pathogenesis of Alzheimer’s disease—A critical review. Mol. Neurobiol. 2019;56:1841–1851. doi: 10.1007/s12035-018-1188-4.
    1. Westfall S., Lomis N., Kahouli I., Dia S.Y., Singh S.P., Prakash S. Microbiome, probiotics and neurodegenerative diseases: Deciphering the gut brain axis. Cell Mol. Life Sci. 2017;74:3769–3787. doi: 10.1007/s00018-017-2550-9.
    1. Chu F., Shi M., Lang Y., Shen D., Jin T., Zhu J., Cui L. Gut microbiota in multiple sclerosis and experimental autoimmune encephalomyelitis: Current applications and future perspectives. Mediators Inflamm. 2018;2018:8168717. doi: 10.1155/2018/8168717.
    1. Kirby T.O., Ochoa-Repáraz J. The gut microbiome in multiple sclerosis: A potential therapeutic avenue. Med. Sci. 2018;6:69. doi: 10.3390/medsci6030069.
    1. Camara-Lemarroy C.R., Metz L.M., Yong V.W. Focus on the gut-brain axis: Multiple sclerosis, the intestinal barrier and the microbiome. World J. Gastroenterol. 2018;24:4217–4223. doi: 10.3748/wjg.v24.i37.4217.
    1. van Baarlen P., Wells J.M., Kleerebezem M. Regulation of intestinal homeostasis and immunity with probiotic lactobacilli. Trends Immunol. 2013;34:208–215. doi: 10.1016/j.it.2013.01.005.
    1. Antonini M., Lo Conte M., Sorini C., Falcone M. How the Interplay Between the Commensal Microbiota, Gut Barrier Integrity, and Mucosal Immunity Regulates Brain Autoimmunity. Front. Immunol. 2019;10:1937. doi: 10.3389/fimmu.2019.01937.
    1. Dopkins N., Nagarkatti P.S., 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. 2018;154:178–185. doi: 10.1111/imm.12903.
    1. Takata K., Kinoshita M., Okuno T., Moriya M., Kohda T., Honorat J.A., Sugimoto T., Kumanogoh A., Kayama H., Takeda K. The lactic acid bacterium Pediococcus acidilactici suppresses autoimmune encephalomyelitis by inducing IL-10-producing regulatory T cells. PLoS ONE. 2011;6:e27644. doi: 10.1371/journal.pone.0027644.
    1. Ochoa-Reparaz J., Mielcarz D., Wang Y., Begum-Haque S., Dasgupta S., Kasper D., Kasper L. A polysaccharide from the human commensal Bacteroides fragilis protects against CNS demyelinating disease. Mucosal Immunol. 2010;3:487–495.
    1. Wang Y., Telesford K.M., Ochoa-Repáraz J., Haque-Begum S., Christy M., Kasper E.J., Wang L., Wu Y., Robson S.C., Kasper D.L. An intestinal commensal symbiosis factor controls neuroinflammation via TLR2-mediated CD39 signalling. Nat. Commun. 2014;5:1–10. doi: 10.1038/ncomms5432.
    1. Wang Y., Begum-Haque S., Telesford K.M., Ochoa-Repáraz J., Christy M., Kasper E.J., Kasper D.L., Robson S.C., Kasper L.H. A commensal bacterial product elicits and modulates migratory capacity of CD39+ CD4 T regulatory subsets in the suppression of neuroinflammation. Gut Microbes. 2014;5:552–561. doi: 10.4161/gmic.29797.
    1. Kwon H.-K., Kim G.-C., Kim Y., Hwang W., Jash A., Sahoo A., Kim J.-E., Nam J.H., Im S.-H. Amelioration of experimental autoimmune encephalomyelitis by probiotic mixture is mediated by a shift in T helper cell immune response. Clin. Immunol. 2013;146:217–227. doi: 10.1016/j.clim.2013.01.001.
    1. Lavasani S., Dzhambazov B., Nouri M., Fåk F., Buske S., Molin G., Thorlacius H., Alenfall J., Jeppsson B., Weström B. A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS ONE. 2010;5:e9009. doi: 10.1371/journal.pone.0009009.
    1. Takata K., Tomita T., Okuno T., Kinoshita M., Koda T., Honorat J.A., Takei M., Hagihara K., Sugimoto T., Mochizuki H. Dietary yeasts reduce inflammation in central nerve system via microflora. Ann. Clin. Transl. Neurol. 2015;2:56–66. doi: 10.1002/acn3.153.
    1. He B., Hoang T.K., Tian X., Taylor C.M., Blanchard E., Luo M., Bhattacharjee M.B., Freeborn J., Park S., Couturier J. Lactobacillus reuteri reduces the severity of experimental autoimmune encephalomyelitis in mice by modulating gut microbiota. Front. Immunol. 2019;10:385. doi: 10.3389/fimmu.2019.00385.
    1. Chen H., Ma X., Liu Y., Ma L., Chen Z., Lin X., Si L., Ma X., Chen X. Gut Microbiota Interventions With Clostridium butyricum and Norfloxacin Modulate Immune Response in Experimental Autoimmune Encephalomyelitis Mice. Front. Immunol. 2019;10:1662. doi: 10.3389/fimmu.2019.01662.
    1. Tankou S.K., Regev K., Healy B.C., Tjon E., Laghi L., Cox L.M., Kivisäkk P., Pierre I.V., Hrishikesh L., Gandhi R. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann. Neurol. 2018;83:1147–1161. doi: 10.1002/ana.25244.
    1. Tankou S.K., Regev K., Healy B.C., Cox L.M., Tjon E., Kivisakk P., Vanande I.P., Cook S., Gandhi R., Glanz B., et al. Investigation of probiotics in multiple sclerosis. Mult. Scler. 2018;24:58–63. doi: 10.1177/1352458517737390.
    1. Kouchaki E., Tamtaji O.R., Salami M., Bahmani F., Daneshvar Kakhaki R., Akbari E., Tajabadi-Ebrahimi M., Jafari P., Asemi Z. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: A randomized, double-blind, placebo-controlled trial. Clin. Nutr. 2017;36:1245–1249. doi: 10.1016/j.clnu.2016.08.015.
    1. Salami M., Kouchaki E., Asemi Z., Tamtaji O.R. How probiotic bacteria influence the motor and mental behaviors as well as immunological and oxidative biomarkers in multiple sclerosis? A double blind clinical trial. J. Funct. Foods. 2019;52:8–13. doi: 10.1016/j.jff.2018.10.023.
    1. Rogers G., Keating D., Young R., Wong M., Licinio J., Wesselingh S. From gut dysbiosis to altered brain function and mental illness: Mechanisms and pathways. Mol. Psychiatr. 2016;21:738–748. doi: 10.1038/mp.2016.50.
    1. Clapp M., Aurora N., Herrera L., Bhatia M., Wilen E., Wakefield S. Gut microbiota’s effect on mental health: The gut-brain axis. Clin. Pract. 2017;7:987. doi: 10.4081/cp.2017.987.
    1. Cheung S.G., Goldenthal A.R., Uhlemann A.-C., Mann J.J., Miller J.M., Sublette M.E. Systematic review of gut microbiota and major depression. Front. Psychiatr. 2019;10:34. doi: 10.3389/fpsyt.2019.00034.
    1. Murray E., Sharma R., Smith K.B., Mar K.D., Barve R., Lukasik M., Pirwani A.F., Malette-Guyon E., Lamba S., Thomas B.J., et al. Probiotic consumption during puberty mitigates LPS-induced immune responses and protects against stress-induced depression- and anxiety-like behaviors in adulthood in a sex-specific manner. Brain Behav. Immun. 2019;81:198–212. doi: 10.1016/j.bbi.2019.06.016.
    1. Stiemsma L.T., Michels K.B. The Role of the Microbiome in the Developmental Origins of Health and Disease. Pediatrics. 2018;141:e20172437. doi: 10.1542/peds.2017-2437.
    1. Fouhse J.M., Yang K., More-Bayona J., Gao Y., Goruk S., Plastow G., Field C.J., Barreda D.R., Willing B.P. Neonatal Exposure to Amoxicillin Alters Long-Term Immune Response Despite Transient Effects on Gut-Microbiota in Piglets. Front. Immunol. 2019;10:2059. doi: 10.3389/fimmu.2019.02059.
    1. Neuman H., Forsythe P., Uzan A., Avni O., Koren O. Antibiotics in early life: Dysbiosis and the damage done. FEMS Microbiol. Rev. 2018;42:489–499. doi: 10.1093/femsre/fuy018.
    1. Möhle L., Mattei D., Heimesaat M.M., Bereswill S., Fischer A., Alutis M., French T., Hambardzumyan D., Matzinger P., Dunay I.R. Ly6Chi monocytes provide a link between antibiotic-induced changes in gut microbiota and adult hippocampal neurogenesis. Cell Rep. 2016;15:1945–1956. doi: 10.1016/j.celrep.2016.04.074.
    1. Guida F., Turco F., Iannotta M., De Gregorio D., Palumbo I., Sarnelli G., Furiano A., Napolitano F., Boccella S., Luongo L. Antibiotic-induced microbiota perturbation causes gut endocannabinoidome changes, hippocampal neuroglial reorganization and depression in mice. Brain Behav. Immun. 2018;67:230–245. doi: 10.1016/j.bbi.2017.09.001.
    1. Foster J.A., Rinaman L., Cryan J.F. Stress and the gut-brain axis: Regulation by the microbiome. Neurobiol. Stress. 2017;7:124–136. doi: 10.1016/j.ynstr.2017.03.001.
    1. Tetel M.J., De Vries G.J., Melcangi R.C., Panzica G., O’Mahony S.M. Steroids, stress and the gut microbiome-brain axis. J. Neuroendocrinol. 2018;30:e12548. doi: 10.1111/jne.12548.
    1. Tian P., Wang G., Zhao J., Zhang H., Chen W. Bifidobacterium with the role of 5-hydroxytryptophan synthesis regulation alleviates the symptom of depression and related microbiota dysbiosis. J. Nutr. Biochem. 2019;66:43–51. doi: 10.1016/j.jnutbio.2019.01.007.
    1. Tian P., O’Riordan K.J., Lee Y.-k., Wang G., Zhao J., Zhang H., Cryan J.F., Chen W. Towards a psychobiotic therapy for depression: Bifidobacterium breve CCFM1025 reverses chronic stress-induced depressive symptoms and gut microbial abnormalities in mice. Neurobiol. Stress. 2020;12:100216. doi: 10.1016/j.ynstr.2020.100216.
    1. Tian P., Zou R., Song L., Zhang X., Jiang B., Wang G., Lee Y.-k., Zhao J., Zhang H., Chen W. Ingestion of Bifidobacterium longum subspecies infantis strain CCFM687 regulated emotional behavior and the central BDNF pathway in chronic stress-induced depressive mice through reshaping the gut microbiota. Food Funct. 2019;10:7588–7598. doi: 10.1039/C9FO01630A.
    1. Jang H.M., Lee K.E., Kim D.H. The preventive and curative effects of Lactobacillus reuteri NK33 and Bifidobacterium adolescentis NK98 on immobilization stress-induced anxiety/depression and colitis in mice. Nutrients. 2019;11:819. doi: 10.3390/nu11040819.
    1. Han S.-K., Kim D.-H. Lactobacillus mucosae and Bifidobacterium longum Synergistically Alleviate Immobilization Stress-Induced Anxiety/Depression in Mice by Suppressing Gut Dysbiosis. J. Microbiol. Biotechnol. 2019;29:1369–1374. doi: 10.4014/jmb.1907.07044.
    1. Pirbaglou M., Katz J., de Souza R.J., Stearns J.C., Motamed M., Ritvo P. Probiotic supplementation can positively affect anxiety and depressive symptoms: A systematic review of randomized controlled trials. Nutr. Res. 2016;36:889–898. doi: 10.1016/j.nutres.2016.06.009.
    1. Messaoudi M., Lalonde R., Violle N., Javelot H., Desor D., Nejdi A., Bisson J.-F., Rougeot C., Pichelin M., Cazaubiel M. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br. J. Nutr. 2011;105:755–764. doi: 10.1017/S0007114510004319.
    1. Steenbergen L., Sellaro R., van Hemert S., Bosch J.A., Colzato L.S. A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 2015;48:258–264. doi: 10.1016/j.bbi.2015.04.003.
    1. Rao A.V., Bested A.C., Beaulne T.M., Katzman M.A., Iorio C., Berardi J.M., Logan A.C. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009;1:1–6. doi: 10.1186/1757-4749-1-6.

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