3,231
Views
17
CrossRef citations to date
0
Altmetric
Review

Cross-talk between immune system and microbiota in COVID-19

, , , , , , , , , & show all
Pages 1281-1294 | Received 16 Jun 2021, Accepted 06 Oct 2021, Published online: 02 Nov 2021

References

  • Mathew S, Smatti MK, Al Ansari K, et al. Mixed viral-bacterial infections and their effects on gut microbiota and clinical illnesses in children. Sci Rep. 2019;9(1):865.
  • Hanada S, Pirzadeh M, Carver KY, et al. Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. Front Immunol. 2018;9:2640.
  • Zhu H, Wei L, Niu P. The novel coronavirus outbreak in Wuhan, China. Glob Health Res Policy. 2020;5:6.
  • Cully M. Immune status could determine efficacy of COVID-19 therapies. Nat Rev Drug Discov. 2020;19(7):431–434.
  • Cheung KS, Hung IFN, Chan PPY, et al. Gastrointestinal manifestations of SARS-CoV-2 infection and virus load in fecal samples from a Hong Kong cohort: systematic review and meta-analysis. Gastroenterology. 2020;159(1):81–95.
  • El Moheb M, Naar L, Christensen MA, et al. Gastrointestinal complications in critically ill patients with and without COVID-19. JAMA. 2020;324(18):1899–901.
  • Kaafarani HM, El Moheb M, Hwabejire JO, et al. Gastrointestinal complications in critically ill patients with COVID-19. Ann Surg. 2020;272(2):e61.
  • Budden KF, Gellatly SL, Wood DLA, et al. Emerging pathogenic links between microbiota and the gut–lung axis. Nature Rev Microbiol. 2017;15(1):55.
  • Hugon P, Dufour J-C, Colson P, et al. A comprehensive repertoire of prokaryotic species identified in human beings. Lancet Infect Dis. 2015;15(10):1211–19.
  • Cianci R, Pagliari D, Piccirillo CA, et al. The microbiota and immune system crosstalk in health and disease. Mediators of Inflammation. 2018;2018:1–3.
  • Zhu G, Jiang Y, Yao Y, et al. Ovotransferrin ameliorates the dysbiosis of immunomodulatory function and intestinal microbiota induced by cyclophosphamide. Food Funct. 2019;10(2):1109–1122.
  • Xie Q, Pan M, Huang R, et al. Modulation of the small intestinal microbial community composition over short-term or long-term administration with Lactobacillus plantarum ZDY2013. J Dairy Sci. 2016;99(9):6913–21.
  • Belizário JE, Faintuch J. Microbiome and gut dysbiosis. Exp Suppl. 2018;109:459–476.
  • Round JL, Mazmanian SKJNRI. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol. 2009;9(5):313–23.
  • Kamada N, Seo S-U, Chen GY, et al. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321–35.
  • Flint HJ, Scott KP, Louis P, et al. The role of the gut microbiota in nutrition and health. Nat Clin Pract Gastroenterol Hepatol. 2012;9(10):577.
  • Mazmanian SK, Round JL, Kasper DLJN. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620–5.
  • Gérard PJP. Metabolism of cholesterol and bile acids by the gut microbiota. Pathogens. 2014;3(1):14–24.
  • Mezouar S, Chantran Y, Michel J, et al. Microbiome and the immune system: from a healthy steady-state to allergy associated disruption. Hum Microbiome J. 2018;10:11–20.
  • Fleck A-K, Schuppan D, Wiendl H,et al. Gut–CNS-axis as possibility to modulate inflammatory disease activity—Implications for multiple sclerosis. Int J Mol Sci. 2017;18(7):1526.
  • Wiest R, Albillos A, and Trauner, M et al. Targeting the gut-liver axis in liver disease. J Hepatol . 2017;67(5):1084–1103.
  • Yurkovetskiy L, Burrows M, Khan A, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity. 2013;39(2):400–412.
  • Salem I, Ramser, A, and Isham, N, et al. The gut microbiome as a major regulator of the gut-skin axis Front Microbiol . 2018;9:1459.
  • Sencio V, Barthelemy A, Tavares LP, et al. Gut dysbiosis during influenza contributes to pulmonary pneumococcal superinfection through altered short-chain fatty acid production. Cell Rep. 2020;30(9):2934–2947.
  • Schuijt TJ, Lankelma JM, Scicluna BP, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65(4):575–83.
  • Keely S, Talley NJ, Hansbro PMJMI. Pulmonary-intestinal cross-talk in mucosal inflammatory disease. Mucosal Immunol. 2012;5(1):7–18.
  • Yazar A, Atis S, Konca K, et al. Respiratory symptoms and pulmonary functional changes in patients with irritable bowel syndrome. Am J Gastroenterol. 2001;96(5):1511–1516.
  • Lotz MT, Peebles RS. Mechanisms of respiratory syncytial virus modulation of airway immune responses. Curr Allergy Asthma Rep. 2012;12(5):380–387.
  • Brodin P, Davis MM. Human immune system variation. Nat Rev Immunol. 2017;17(1):21.
  • Odamaki T, Kato K, Sugahara H, et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 2016;16(1):1–12.
  • Fouhy F, Ross RP, Fitzgerald GF, et al. Composition of the early intestinal microbiota: knowledge, knowledge gaps and the use of high-throughput sequencing to address these gaps. Gut Microbes. 2012;3(3):203–220.
  • Levine KM, Priedigkeit N, Basudan A, et al. FGFR4 overexpression and hotspot mutations in metastatic ER+ breast cancer are enriched in the lobular subtype. NPJ Breast Cancer. 2019;5(1):1–5.
  • Lloyd-Price J, Abu-Ali G, Huttenhower C. The healthy human microbiome. Genome Med. 2016;8:51.
  • Russell SL, Gold MJ, Reynolds LA, et al. Perinatal antibiotic-induced shifts in gut microbiota have differential effects on inflammatory lung diseases. J Allergy Clin Immunol. 2015;135(1):100–9. e5.
  • Han Y, Jia, Z, and Shi, J, et al. The active lung microbiota landscape of COVID-19 patients. medRxiv, 2020.
  • Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–1062.
  • Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474(11):1823–1836.
  • Scarpellini E, Fagoonee S, Rinninella E, et al. Gut microbiota and liver interaction through immune system cross-talk: a comprehensive review at the time of the SARS-COV-2 pandemic. J Clin Med. 2020;9(8):2488.
  • Rinninella E, Raoul P, Cintoni M, et al. What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 2019;7(1):14.
  • Rabizadeh S, Rhee K-J, Wu S, et al. Enterotoxigenic Bacteroides fragilis: a potential instigator of colitis. Inflamm Bowel Dis. 2007;13(12):1475–1483.
  • Atarashi K, Tanoue T, Shima T, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011;331(6015):337–341.
  • Mukhopadhya I, Segal, JP, and Carding, SR, et al. The gut virome: the ‘missing link’between gut bacteria and host immunity? Therap Adv Gastroenterol. 2019;12:1756284819836620.
  • Scarpellini E, Ianiro G, Attili F, et al. The human gut microbiota and virome: potential therapeutic implications. Digestive Liver Dis. 2015;47(12):1007–1012.
  • Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res. 2020;30(6):492–506.
  • Belkaid Y, Hand TW. Role of the microbiota in immunity and inflammation. Cell. 2014;157(1):121–141.
  • Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature. 2016;535(7610):75–84.
  • Owaga E, Hsieh R-H, Mugendi B, et al. Th17 cells as potential probiotic therapeutic targets in inflammatory bowel diseases. Int J Mol Sci. 2015;16(9):20841–20858.
  • Arpaia N, Campbell C, Fan X, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature. 2013;504(7480):451–455.
  • Cheng H-Y, Ning, MX, and Chen, DK, et al. Interactions between the gut microbiota and the host innate immune response against pathogens. Front Immunol. 2019;10. DOI:https://doi.org/10.3389/fimmu.2019.00607.
  • Pagliari D, Piccirillo CA, Larbi A, et al. The interactions between innate immunity and microbiota in gastrointestinal diseases. J Immunol Res. 2015;2015:1–3.
  • Ivanov II, Atarashi K, Manel N, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 2009;139(3):485–498.
  • Hooper LV, Littman DR, Macpherson AJ. Interactions between the microbiota and the immune system. Science. 2012;336(6086):1268–1273.
  • Gaudino SJ, Kumar P. Cross-Talk between antigen presenting cells and T cells impacts intestinal homeostasis, bacterial infections, and tumorigenesis. Front Immunol. 2019;10:360.
  • Bene K, Varga Z, Petrov VO, et al. Gut microbiota species can provoke both inflammatory and tolerogenic immune responses in human dendritic cells mediated by retinoic acid receptor alpha ligation. Front Immunol. 2017;8:427.
  • Wu H-J, Wu E. The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes. 2012;3(1):4–14.
  • Flannigan KL, Denning TL. Segmented filamentous bacteria‐induced immune responses: a balancing act between host protection and autoimmunity. Immunology. 2018;154(4):537–546.
  • Lécuyer E, Rakotobe S, Lengliné-Garnier H, et al. Segmented filamentous bacterium uses secondary and tertiary lymphoid tissues to induce gut IgA and specific T helper 17 cell responses. Immunity. 2014;40(4):608–620.
  • Salzman NHJG. m., Paneth cell defensins and the regulation of the microbiome: detente at mucosal surfaces. Gut Microbes. 2010;1(6):401–406.
  • Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity. 2009;31(4):677–689.
  • Louis P, Flint HJ. Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol. 2017;19(1):29–41.
  • Silva YP, Bernardi A, Frozza RL. The role of short-chain fatty acids from gut microbiota in gut-brain communication. Front Endocrinol (Lausanne). 2020;11:25.
  • Corrêa‐Oliveira R, Fachi JL, Vieira A, et al. Regulation of immune cell function by short‐chain fatty acids. Clin Transl Immunology. 2016;5(4):e73.
  • Rosshart SP, Vassallo BG, Angeletti D, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171(5):1015–1028.
  • Khosravi A, Yáñez, A, and Price, JG, et al. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe. 2014;15(3):374–381.
  • Lo BC, Shin, SB, and Canals Hernaez, D, et al. IL-22 preserves gut epithelial integrity and promotes disease remission during chronic Salmonella infection. J Immunol. 2019;202(3):956–965.
  • Chen GY, Liu, M, and Wang, F, et al. A functional role for Nlrp6 in intestinal inflammation and tumorigenesis. J Immunol. 2011;186(12):7187–7194.
  • Lukasova M, Malaval, C, and Gille, A, et al. Nicotinic acid inhibits progression of atherosclerosis in mice through its receptor GPR109A expressed by immune cells. J Clin Investig. 2011;121(3):1163–1173.
  • Maslowski KM, Vieira AT, Ng A, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461(7268):1282–1286.
  • Gustafsson JK, Ermund A, Johansson MEV, et al. An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants. Am J Physiol Gastrointest Liver Physiol. 2012;302(4):G430–8.
  • Jung T-H, Park JH, Jeon W-M, et al. Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretion and MAPK signaling pathway. Nutr Res Pract. 2015;9(4):343–349.
  • Diamond G, Beckloff N, Weinberg A, et al. The roles of antimicrobial peptides in innate host defense. Curr Pharm Des. 2009;15(21):2377–2392.
  • Kim D, Zeng MY, Núñez G, et al. The interplay between host immune cells and gut microbiota in chronic inflammatory diseases. Exp Mol Med. 2017;49(5):e339.
  • Canani RB, Costanzo, MD, and Leone L, et al. Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol. 2011;17(12):1519–1528.
  • Salvi PS, Cowles RA. Butyrate and the intestinal epithelium: modulation of proliferation and inflammation in homeostasis and disease. Cells. 2021;10(7):1775.
  • Jiminez JA, Uwiera, TC, and Abbott, DW, et al. Butyrate supplementation at high concentrations alters enteric bacterial communities and reduces intestinal in flammation in mice infected with Citrobacter rodentium. MSphere. 2017;2(4);e00243–17.
  • Frieman M, Heise M, Baric RJVR. SARS coronavirus and innate immunity. Virus Res. 2008;133(1):101–12.
  • Yitbarek A, Taha-Abdelaziz, K, and Hodgins, DC, et al. Gut microbiota-mediated protection against influenza virus subtype H9N2 in chickens is associated with modulation of the innate responses. Sci Rep. 2018;8(1):1–12.
  • Menendez A, Willing, BP, and Montero, M, et al. Bacterial stimulation of the TLR-MyD88 pathway modulates the homeostatic expression of ileal Paneth cell α-defensins. J Innate Immun. 2013;5(1):39–49.
  • Cianci R, et al. Tissue infiltrating lymphocytes: the role of cytokines in their growth and differentiation. J Biol Regul Homeostat Agents. 2010;24(3):239
  • Francino MPJP. Early development of the gut microbiota and immune health. Pathogens. 2014;3(3):769–790.
  • Arrazuria R, Pérez V, Molina E, et al. Diet induced changes in the microbiota and cell composition of rabbit gut associated lymphoid tissue (GALT). Sci Rep. 2018;8(1):14103.
  • Ahluwalia B, Magnusson MK, Öhman L. Mucosal immune system of the gastrointestinal tract: maintaining balance between the good and the bad. Scand J Gastroenterol. 2017;52(11):1185–1193.
  • Fagarasan S, Muramatsu M, Suzuki K, et al. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science. 2002;298(5597):1424–1427.
  • Kasarello K, Sajdel-Sulkowska EM. Developmental significance of early gut-associated lymphoid tissue (GALT)-microbiota interactions in health and disease: creating balance between tolerance and inflammation in children. Open J Pediatr Child Health. 2019;4(1): 040–6. doi:https://doi.org/10.17352/ojpch.000019.
  • Sze MA, Dimitriu PA, Hayashi S, et al. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185(10):1073–1080.
  • Marsland BJ, Trompette A, Gollwitzer ESJAOTATS. The gut–lung axis in respiratory disease. Ann Am Thorac Soc. 2015;12(Supplement 2):S150–S156.
  • Enaud R, Prevel R, Ciarlo E, et al. 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.
  • Dickson RP, Singer BH, Newstead MW, et al. Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome. Nat Microbiol. 2016;1(10):1–9.
  • Fanos V, Pintus, MC, and Pintus, R, et al. Lung microbiota in the acute respiratory disease: from coronavirus to metabolomics. J Pediatr Neonatal Individ Med(JPNIM). 2020;9(1): e090139
  • Battaglini D, Robba C, Fedele A, et al. The role of dysbiosis in critically ill patients with COVID-19 and acute respiratory distress syndrome. Front Med. 2021;8:826.
  • Looft T, Allen HKJGM. Collateral effects of antibiotics on mammalian gut microbiomes. Gut Microbes. 2012;3(5):463–467.
  • Fujimura KE, Lynch SVJCH. Microbiota in allergy and asthma and the emerging relationship with the gut microbiome. Cell Host Microbe. 2015;17(5):592–602.
  • Young RP, Hopkins RJ, Marsland B, et al. The gut–liver–lung axis. Modulation of the innate immune response and its possible role in chronic obstructive pulmonary disease. Am J Resp Cell Mol Biol. 2016;54(2):161–169.
  • Baradaran Ghavami SH, Sharokh, SH, and Hossein-Khannazer, N, et al. IBD patients could be silent carriers for novel coronavirus and less prone to its severe adverse events: true or false? Cell J. 2020;22(Suppl 1):151–4.
  • Denny JE, Powell WL, Schmidt NW, et al. Local and long-distance calling: conversations between the gut microbiota and intra-and extra-gastrointestinal tract infections. Front Cell Infect Microbiol. 2016;6:41.
  • Coopersmith CM, Stromberg PE, Davis CG, et al. Sepsis from Pseudomonas aeruginosa pneumonia decreases intestinal proliferation and induces gut epithelial cell cycle arrest. Crit Care Med. 2003;31(6):1630–1637.
  • Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus–infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–1069.
  • Rajput S, Paliwal, D, and Naithani, M, et al. COVID-19 and gut microbiota: a potential connection. Indian J Clin Biochem. 2021;36(3) ;1–12.
  • Anand S, Mande SS. Diet, microbiota and gut-lung connection. Front Microbiol. 2018;9:2147.
  • Arrieta M-C, Stiemsma LT, Dimitriu PA, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med. 2015;7(307):307ra152.
  • Lynch S, Sitarik, AR, and Havstad, S, et al. Neonatal gut microbiota associates with childhood multisensitized atopy and T cell differentiation Nat Med . 2016;22(10):1187–1191 .
  • Demirci M, Tokman HB, Uysal HK, et al. Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergol Immunopathol (Madr). 2019;47(4):365–371.
  • Kalliomäki M, Kirjavainen P, Eerola E, et al. Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol. 2001;107(1):129–134.
  • Hilty M, Burke, C, and Pedro, H, et al. Disordered microbial communities in asthmatic airways. PloS One. 2010;5(1):e8578.
  • Charlson ES, Bittinger K, Haas AR, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. 2011;184(8):957–963.
  • Antosca KM, Chernikova DA, Price CE, et al. Altered stool microbiota of infants with cystic fibrosis shows a reduction in genera associated with immune programming from birth. J Bacteriol. 2019;201(16):e00274–19.
  • Burke DG, Fouhy, F, and Harrison, MJ, et al. The altered gut microbiota in adults with cystic fibrosis. BMC Microbiol. 2017;17(1):58.
  • Fouhy F, Ronan NJ, O’Sullivan O, et al. A pilot study demonstrating the altered gut microbiota functionality in stable adults with cystic fibrosis. Sci Rep. 2017;7(1):1–12.
  • Debyser G, Mesuere B, Clement L, et al. Faecal proteomics: a tool to investigate dysbiosis and inflammation in patients with cystic fibrosis. J Cyst Fibros. 2016;15(2):242–250.
  • Blainey PC, Milla, CE, and Cornfield, DN, et al. Quantitative analysis of the human airway microbial ecology reveals a pervasive signature for cystic fibrosis. Sci Transl Med. 2012;4(153):153ra130.
  • Kolak M, Karpati, F, and Monstein, H-J, et al. Molecular typing of the bacterial flora in sputum of cystic fibrosis patients. Int J Med Microbiol. 2003;293(4):309–317.
  • Zhuang H, Cheng L, Wang Y, et al. Dysbiosis of the gut microbiome in lung cancer. Front Cell Infect Microbiol. 2019;9:112.
  • Rosas-Salazar C, Shilts MH, Tovchigrechko A, et al. Differences in the nasopharyngeal microbiome during acute respiratory tract infection with human rhinovirus and respiratory syncytial virus in infancy. J Infect Dis. 2016;214(12):1924–8.
  • Hofstra JJ, Matamoros, S, and van de Pol, MA, et al. Changes in microbiota during experimental human Rhinovirus infection. BMC Infect Dis. 2015;15(1):1–9.
  • Karppinen S, Teräsjärvi, J, and Auranen, K, et al. Acquisition and transmission of Streptococcus pneumoniae are facilitated during rhinovirus infection in families with children. Am J Respir Crit Care Med. 2017;196(9):1172–1180.
  • Molyneaux PL, Mallia P, Cox MJ, et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013;188(10):1224–1231.
  • Allen EK, Koeppel, AF, and Hendley, JO, et al. Characterization of the nasopharyngeal microbiota in health and during rhinovirus challenge. Microbiome. 2014;2(1):22.
  • Lu H-F, Li, A, and Zhang, T, et al. Disordered oropharyngeal microbial communities in H7N9 patients with or without secondary bacterial lung infection. Emerg Microbes Infect. 2017;6(1):1–11.
  • Leung R-K, Zhou J-W, Guan W, et al. Modulation of potential respiratory pathogens by pH1N1 viral infection. Clin Microbiol Infect. 2013;19(10):930–935.
  • Rogers GB, Shaw D, Marsh RL, et al. Respiratory microbiota: addressing clinical questions, informing clinical practice. Thorax. 2015;70(1):74–81.
  • Qin N, Zheng, B, and Yao, J, et al. Influence of H7N9 virus infection and associated treatment on human gut microbiota. Sci Rep. 2015;5:14771.
  • Saitou M, Nemoto D, Utano K, et al. Identification of intestinal abnormalities in patients with active pulmonary tuberculosis using small bowel capsule endoscopy. Endosc Int Open. 2018;6(9):E1103.
  • Luo M, Liu Y, Wu P, et al. Alternation of gut microbiota in patients with pulmonary tuberculosis. Front Physiol. 2017;8:822.
  • Zhang D, Li, S, and Wang, N, et al. The cross-talk between gut microbiota and lungs in common lung diseases. Front Microbiol. 2020;11: 301.
  • Neu U, Mainou BA, Evans MJ. Virus interactions with bacteria: partners in the infectious dance. PLoS Pathog. 2020;16(2):e1008234.
  • Mustafa S, Balkhy H, Gabere MN. Current treatment options and the role of peptides as potential therapeutic components for Middle East Respiratory Syndrome (MERS): a review. J Infect Public Health. 2018;11(1):9–17.
  • Du L, He Y, Zhou Y, et al. The spike protein of SARS-CoV—a target for vaccine and therapeutic development. Nat Rev Microbiol. 2009;7(3):226–236.
  • Zeppa SD, Agostini, D, and Piccoli, G, et al. Gut microbiota status in COVID-19: an unrecognized player? Front Cell Infect Microbiol. 2020;10 576551 .
  • Ichinohe T, Pang IK, Kumamoto Y, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci. 2011;108(13):5354–5359.
  • Abt MC, Osborne L, Monticelli L, et al. Commensal bacteria calibrate the activation threshold of innate antiviral. immunity. 2012;37(1):158–170.
  • Allie SR, Bradley JE, Mudunuru U, et al. The establishment of resident memory B cells in the lung requires local antigen encounter. Nat Immunol. 2019;20(1):97–108.
  • Dong L, Hu S, Gao J. Discovering drugs to treat coronavirus disease 2019 (COVID-19). Drug Discov Ther. 2020;14(1):58–60.
  • Lv L, Gu S, Jiang H, et al. Gut mycobiota alterations in patients with COVID-19 and H1N1 infections and their associations with clinical features. Commun Biol. 2021;4(1):480.
  • Forbes JD, Bernstein CN, Tremlett H, et al. A fungal world: could the gut mycobiome be involved in neurological disease? Front Microbiol. 2019;9:3249.
  • Lv L, Gu, S, and Jiang, H, et al. Gut mycobiota alterations in patients with COVID-19 and H1N1 and their associations with clinical features Commun Biol . 2021;4(1): 480 .
  • Zuo T, Zhang F, Lui GCY, et al. Alterations in gut microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology. 2020;159(3):944–955. e8.
  • Gou W, Fu, Y, and Yue, L, et al., Gut microbiota may underlie the predisposition of healthy individuals to COVID-19. MedRxiv, 2020.
  • Zuo T, Liu, Q, and Zhang, F, et al. Depicting SARS-CoV-2 faecal viral activity in association with gut microbiota composition in patients with COVID-19. Gut. 2021;70(2):276–284.
  • Zhou Y, Shi X, Fu W, et al. Gut microbiota dysbiosis correlates with abnormal immune response in moderate COVID-19 patients with fever. J Inflamm Res. 2021;14:2619–2631.
  • Gu S, Chen Y, Wu Z, et al. Alterations of the gut microbiota in patients with coronavirus disease 2019 or H1N1 Influenza. Clin Infect Dis. 2020;71(10):2669–2678.
  • Yeoh YK, Zuo T, Lui GC-Y, et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut. 2021;70(4):698–706.
  • Tang L, Gu S, Gong Y, et al. Clinical significance of the correlation between changes in the major intestinal bacteria species and COVID-19 severity. Engineering. 2020;6(10):1178–1184.
  • Khatiwada S, Subedi A. Lung microbiome and coronavirus disease 2019 (COVID-19): possible link and implications. Hum Microbiome J. 2020;17:100073.
  • Kalina U, Koyama N, Hosoda T, et al. Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region. Eur J Immunol. 2002;32(9):2635–2643.
  • Domínguez-Cherit G, Lapinsky, SE, and Macias, AE, et al. Critically ill patients with 2009 influenza A (H1N1) in Mexico. JAMA. 2009;302(17):1880–1887.
  • Yasui H, Kiyoshima J, Hori TJCDLI. Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei Shirota. Clin Vaccin Immunol. 2004;11(4):675–679.
  • Tomosada Y, Chiba E, Zelaya H, et al. Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection. BMC Immunol. 2013;14(1):40.
  • Mailliard RB, Son Y-I, Redlinger R, et al. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol. 2003;171(5):2366–2373.
  • Kitazawa H, Villena JJFII. Modulation of respiratory TLR3-anti-viral response by probiotic microorganisms: lessons learned from Lactobacillus rhamnosus CRL1505. Front Immunol. 2014;5:201.
  • Yilla M, Harcourt BH, Hickman CJ, et al. SARS-coronavirus replication in human peripheral monocytes/macrophages. Virus Res. 2005;107(1):93–101.
  • Cinatl J Jr., Hoever G, Morgenstern B, et al. Infection of cultured intestinal epithelial cells with severe acute respiratory syndrome coronavirus. Cell Mol Life Sci. 2004;61(16):2100–12.
  • Spiegel M, Schneider K, Weber F, et al. Interaction of severe acute respiratory syndrome-associated coronavirus with dendritic cells. J Gen Virol. 2006;87(7):1953–60.
  • Simmons G, Gosalia DN, Rennekamp AJ, et al. Inhibitors of cathepsin L prevent severe acute respiratory syndrome coronavirus entry. Proc Natl Acad Sci U S A. 2005;102(33):11876–11881.
  • Fischer DD, Kandasamy S, Paim FC, et al. Protein malnutrition alters tryptophan and angiotensin-converting enzyme 2 homeostasis and adaptive immune responses in human rotavirus-infected gnotobiotic pigs with human infant fecal microbiota transplant. Clin Vaccin Immunol. 2017;24(8):e00172–17.
  • Vighi G, Marcucci F, Sensi L, et al. Allergy and the gastrointestinal system. Clin Exp Immunol. 2008;153(Suppl 1):3–6.
  • Mikelsaar M, Lazar V, Onderdonk A, et al. Do probiotic preparations for humans really have efficacy? Microb Ecol Health Dis. 2011;22(1):10128.
  • Kong YH, Shi, Q, and Han, N, et al. Structural modulation of gut microbiota in rats with allergic bronchial asthma treated with recuperating lung decoction. Biomed Environ Sci. 2016;29(8):574–583.
  • Villena J, Salva S, Barbieri N, et al. Immunobiotics for the Prevention of Bacterial and Viral Respiratory Infections Probiotics 1. Boca Raton: CRC Press. 2013:128–168. 9780429090684 .
  • Mullish BH, Marchesi JR, McDonald JAK, et al. Probiotics reduce self-reported symptoms of upper respiratory tract infection in overweight and obese adults: should we be considering probiotics during viral pandemics? Gut Microbes. 2021;13(1):1900997.
  • Bron PA, Kleerebezem M, Brummer R-J, et al. Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr. 2017;117(1):93–107.
  • Davani-Davari D, Negahdaripour M, Karimzadeh I, et al. Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods. 2019;8(3):92.
  • Olaimat AN, Aolymat I, Al-Holy M, et al. The potential application of probiotics and prebiotics for the prevention and treatment of COVID-19. NPJ Science Food. 2020;4(1):1–7.
  • Fujiwara S, Seto Y, Kimura A, et al. Establishment of orally‐administered Lactobacillus gasseri SBT2055SR in the gastrointestinal tract of humans and its influence on intestinal microflora and metabolism. J Appl Microbiol. 2001;90(3):343–352.
  • Takahashi H, Fujita T, Suzuki Y, et al. Monitoring and survival of Lactobacillus gasseri SBT2055 in the human intestinal tract. Microbiol Immunol. 2006;50(11):867–870.
  • Sakai F, Hosoya T, Ono-Ohmachi A, et al. Lactobacillus gasseri SBT2055 induces TGF-β expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PloS One. 2014;9(8):e105370.
  • Nakayama Y, Moriya T, Sakai F, et al. Oral administration of Lactobacillus gasseri SBT2055 is effective for preventing influenza in mice. Sci Rep. 2014;4:4638.
  • Eguchi K, Fujitani N, Nakagawa H, et al. Prevention of respiratory syncytial virus infection with probiotic lactic acid bacterium Lactobacillus gasseri SBT2055. Sci Rep. 2019;9(1):1–11.
  • Hori T, Kiyoshima J, Shida K, et al. Effect of intranasal administration oflactobacillus casei Shirota on influenza virus infection of upper respiratory tract in mice. Clin Diagn Lab Immunol. 2001;8(3):593–597.
  • Vickers NJJCB. Animal communication: when i’m calling you, will you answer too? Curr Biol. 2017;27(14):R713–15.
  • Gabryszewski SJ, Bachar O, Dyer KD, et al. Lactobacillus-mediated priming of the respiratory mucosa protects against lethal pneumovirus infection. J Immunol. 2011;186(2):1151–1161.
  • Villena J, Barbieri N, Salva S, et al. Enhanced immune response to pneumococcal infection in malnourished mice nasally treated with heat‐killed Lactobacillus casei. Microbiol Immunol. 2009;53(11):636–46.
  • Weiss G, Rasmussen S, Zeuthen LH, et al. Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll‐like receptor‐2‐dependent mechanism. Immunology. 2010;131(2):268–81.
  • Khailova L, Petrie B, Baird CH, et al. Lactobacillus rhamnosus GG and Bifidobacterium longum attenuate lung injury and inflammatory response in experimental sepsis. PLoS One. 2014;9(5):e97861.
  • Iwabuchi N, Xiao J-Z, Yaeshima T, et al. Oral administration of Bifidobacterium longum ameliorates influenza virus infection in mice. Biol Pharm Bull. 2011;34(8):1352–1355.
  • Kawahara T, Takahashi T, Oishi K, et al. 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):1–12.
  • Namba K, Hatano M, Yaeshima T, et al. Effects of Bifidobacterium longum BB536 administration on influenza infection, influenza vaccine antibody titer, and cell-mediated immunity in the elderly. Biosci Biotechnol Biochem. 2010;74(5):939–945.
  • Furuhashi K, Suda T, Hasegawa H, et al. Mouse lung CD103+ and CD11bhigh dendritic cells preferentially induce distinct CD4+ T-cell responses. Am J Respir Cell Mol Biol. 2012;46(2):165–172.
  • Gleeson M, Pyne DB. Respiratory inflammation and infections in high‐performance athletes. Immunol Cell Biol. 2016;94(2):124–131.
  • Van Puyenbroeck K, Hens N, Coenen S, et al. 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(5):1165–1171.
  • Sindhu KN, Sowmyanarayanan TV, Paul A, et al. Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clinl Infect Dis. 2014;58(8):1107–1115.
  • Hirose Y, Murosaki, S, and Yamamoto, Y, et al. Daily intake of heat-killed Lactobacillus plantarum L-137 augments acquired immunity in healthy adults. J Nutr. 2006;136(12):3069–3073.
  • Maeda N, Nakamura, R, and Hirose, Y, et al. Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. Int Immunopharmacol. 2009;9(9):1122–1125.
  • Izumo T, Maekawa, T, and Ida, M, et al. Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice. Int Immunopharmacol. 2010;10(9):1101–1106.
  • Fujimura KE, Demoor T, Rauch M, et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc Natl Acad Sci U S A. 2014;111(2):805–810.
  • Yasui H, Kiyoshima J, Hori T, et al. Protection against influenza virus infection of mice fed Bifidobacterium breve YIT4064. Clin Diagn Lab Immunol. 1999;6(2):186–192.
  • Bandoro C, Runstadler JA, Lowen AC. Bacterial lipopolysaccharide destabilizes influenza viruses. MSphere. 2017;2(5):e00267–17.
  • Deitch EA. Gut-origin sepsis: evolution of a concept. Surgeon. 2012;10(6):350–356.
  • Bradley KC, Finsterbusch K, Schnepf D, et al. Microbiota-driven tonic interferon signals in lung stromal cells protect from influenza virus infection. Cell Rep. 2019;28(1):245–256. e4.
  • Albenberg LG, Wu GDJG. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146(6):1564–1572.
  • Varraso R, Chiuve SE, Fung TT, et al. Alternate Healthy Eating Index 2010 and risk of chronic obstructive pulmonary disease among US women and men: prospective study. BMJ. 2015;350:h286.
  • King DE, Egan BM, Woolson RF, et al. Effect of a high-fiber diet vs a fiber-supplemented diet on C-reactive protein level. Arch Intern Med. 2007;167(5):502–506.
  • Kazemian N, Kao D, Pakpour S. Fecal microbiota transplantation during and post-COVID-19 pandemic. Int J Mol Sci. 2021;22(6):3004.
  • Liu F, Ye S, Zhu X, et al. Gastrointestinal disturbance and effect of fecal microbiota transplantation in discharged COVID-19 patients. J Med Case Rep. 2021;15(1):1–9.
  • Stewart CJ, Ajami NJ, O’Brien JL, et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature. 2018;562(7728):583–588.
  • Mutlu EA, Keshavarzian A, Losurdo J, et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog. 2014;10(2):e1003829.
  • Vabret N, Britton GJ, Gruber C, et al. Immunology of COVID-19: current state of the science. Immunity. 2020;52(6):910–941 .
  • Verdoni L, Mazza A, Gervasoni A, et al. An outbreak of severe Kawasaki-like disease at the Italian epicentre of the SARS-CoV-2 epidemic: an observational cohort study. Lancet. 2020;395(10239):1771–1778.
  • Chhibber-Goel J, Gopinathan S, Sharma A. Interplay between severities of COVID-19 and the gut microbiome: implications of bacterial co-infections? Gut Pathog. 2021;13(1):1–6.
  • Goncalves Mendes Neto A, Lo KB, Wattoo A, et al. Bacterial infections and patterns of antibiotic use in patients with COVID‐19. J Med Virol. 2021;93(3):1489–1495.
  • Vila AV, Collij, V, and Sanna, S, et al. Impact of commonly used drugs on the composition and metabolic function of the gut microbiota. Nat Commun. 2020;11(1):1–11.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.