Akkermansia muciniphila: a deworming partner independent of type 2 immunity

References

• Santano R, Rubio R, Grau-Pujol B, Escola V, Muchisse O, Cuamba I, Vidal M, Cisteró P, Ruiz-Olalla G, Aguilar R. et al. Plasmodium falciparum and helminth coinfections increase ige and parasite-specific IgG responses. Microbiol Spectr. 2021;9(3):e0110921. doi:10.1128/Spectrum.01109-21.
   PubMed Web of Science ®Google Scholar
• Disease GBD, Injury I, Prevalence C, Abay SM, Abbafati C, Abbasi N, Abbastabar H, Abd-Allah F, Abdela J, Abdelalim A. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the global burden of disease study 2017. Lancet. 2018;392(10159):1789–8. doi:10.1016/S0140-6736(18)32279-7.
   PubMed Web of Science ®Google Scholar
• Cani PD. Human gut microbiome: hopes, threats and promises. Gut. 2018;67(9):1716–1725. doi:10.1136/gutjnl-2018-316723.
   PubMed Web of Science ®Google Scholar
• El Aidy S, Hooiveld G, Tremaroli V, Backhed F, Kleerebezem M. The gut microbiota and mucosal homeostasis: colonized at birth or at adulthood, does it matter? Gut Microbes. 2013;4(2):118–124. doi:10.4161/gmic.23362.
   PubMed Web of Science ®Google Scholar
• Mutapi F. The gut microbiome in the helminth infected host. Trends Parasitol. 2015;31(9):405–406. doi:10.1016/j.pt.2015.06.003.
   PubMed Web of Science ®Google Scholar
• Rapin A, Harris NL. Helminth–bacterial interactions: cause and consequence. Trends Immunol. 2018;39(9):724–733. doi:10.1016/j.it.2018.06.002.
   PubMed Web of Science ®Google Scholar
• Cani PD, Depommier C, Derrien M, Everard A, de Vos WM. Akkermansia muciniphila: paradigm for next-generation beneficial microorganisms. Nat Rev Gastroenterol Hepatol. 2022;19(10):625–637. doi:10.1038/s41575-022-00631-9.
   PubMed Web of Science ®Google Scholar
• Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM. et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A. 2013;110(22):9066–9071. doi:10.1073/pnas.1219451110.
   PubMed Web of Science ®Google Scholar
• Li J, Lin S, Vanhoutte PM, Woo CW, Xu A. Akkermansia muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe −/− Mice. Circulation. 2016;133(24):2434–2446. doi:10.1161/CIRCULATIONAHA.115.019645.
   PubMed Web of Science ®Google Scholar
• Hanninen A, Toivonen R, Poysti S, Belzer C, Plovier H, Ouwerkerk JP, Emani R, Cani PD, De Vos WM. Akkermansia muciniphila induces gut microbiota remodelling and controls islet autoimmunity in NOD mice. Gut. 2018;67(8):1445–1453. doi:10.1136/gutjnl-2017-314508.
   PubMed Web of Science ®Google Scholar
• Plovier H, Everard A, Druart C, Depommier C, Van Hul M, Geurts L, Chilloux J, Ottman N, Duparc T, Lichtenstein L. et al. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med. 2017;23(1):107–113. doi:10.1038/nm.4236.
   PubMed Web of Science ®Google Scholar
• Depommier C, Van Hul M, Everard A, Delzenne NM, De Vos WM, Cani PD. Pasteurized Akkermansia muciniphila increases whole-body energy expenditure and fecal energy excretion in diet-induced obese mice. Gut Microbes. 2020;11(5):1231–1245. doi:10.1080/19490976.2020.1737307.
   PubMed Web of Science ®Google Scholar
• Dao MC, Everard A, Aron-Wisnewsky J, Sokolovska N, Prifti E, Verger EO, Kayser BD, Levenez F, Chilloux J, Hoyles L. et al. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut. 2016;65(3):426–436. doi:10.1136/gutjnl-2014-308778.
   PubMed Web of Science ®Google Scholar
• Anthony RM, Rutitzky LI, Urban JF Jr., Stadecker MJ, Gause WC. Protective immune mechanisms in helminth infection. Nat Rev Immunol. 2007;7(12):975–987. doi:10.1038/nri2199.
   PubMed Web of Science ®Google Scholar
• Chen F, Liu Z, Wu W, Rozo C, Bowdridge S, Millman A, Van Rooijen N, Urban JF, Wynn TA, Gause WC. et al. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat Med. 2012;18(2):260–266. doi:10.1038/nm.2628.
   PubMed Web of Science ®Google Scholar
• Grencis RK. Immunity to helminths: resistance, regulation, and susceptibility to gastrointestinal nematodes. Annu Rev Immunol. 2015;33(1):201–225. doi:10.1146/annurev-immunol-032713-120218.
   PubMedGoogle Scholar
• Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature. 2007;449(7164):819–826. doi:10.1038/nature06246.
   PubMed Web of Science ®Google Scholar
• Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol. 1997;15(1):505–533. doi:10.1146/annurev.immunol.15.1.505.
   PubMedGoogle Scholar
• Urban JF Jr., Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M, Finkelman FD. IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite nippostrongylus brasiliensis. Immunity. 1998;8(2):255–264. doi:10.1016/S1074-7613(00)80477-X.
   PubMed Web of Science ®Google Scholar
• Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM. Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. J Exp Med. 2006;203(6):1435–1446. doi:10.1084/jem.20052448.
   PubMed Web of Science ®Google Scholar
• Volkmann L, Bain O, Saeftel M, Specht S, Fischer K, Brombacher F, Matthaei KI, Hoerauf A. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med Microbiol Immunol. 2003;192(1):23–31. doi:10.1007/s00430-002-0155-9.
   PubMed Web of Science ®Google Scholar
• Licona-Limon P, Henao-Mejia J, Temann AU, Gagliani N, Licona-Limon I, Ishigame H, Hao L, Herbert D, Flavell R. Th9 cells drive host immunity against gastrointestinal worm infection. Immunity. 2013;39(4):744–757. doi:10.1016/j.immuni.2013.07.020.
   PubMed Web of Science ®Google Scholar
• Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13(4):260–270. doi:10.1038/nrg3182.
   PubMed Web of Science ®Google Scholar
• Loke P, Harris NL. Networking between helminths, microbes, and mammals. Cell Host Microbe. 2023;31(4):464–471. doi:10.1016/j.chom.2023.02.008.
   PubMed Web of Science ®Google Scholar
• White EC, Houlden A, Bancroft AJ, Hayes KS, Goldrick M, Grencis RK, Roberts IS. Manipulation of host and parasite microbiotas: survival strategies during chronic nematode infection. Sci Adv. 2018;4(3):eaap7399. doi:10.1126/sciadv.aap7399.
   PubMed Web of Science ®Google Scholar
• Ramanan D, Bowcutt R, Lee SC, Tang MS, Kurtz ZD, Ding Y, Honda K, Gause WC, Blaser MJ, Bonneau RA. et al. Helminth infection promotes colonization resistance via type 2 immunity. Science. 2016;352(6285):608–612. doi:10.1126/science.aaf3229.
   PubMed Web of Science ®Google Scholar
• Osborne LC, Monticelli LA, Nice TJ, Sutherland TE, Siracusa MC, Hepworth MR, Tomov VT, Kobuley D, Tran SV, Bittinger K. et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science. 2014;345(6196):578–582. doi:10.1126/science.1256942.
   PubMed Web of Science ®Google Scholar
• Li C, Liu Y, Liu X, Bai X, Jin X, Xu F, Chen H, Zhang Y, Vallee I, Liu M. et al. The gut microbiota contributes to changes in the host immune response induced by Trichinella spiralis. PLoS Negl Trop Dis. 2023;17(8):e0011479. doi:10.1371/journal.pntd.0011479.
   PubMed Web of Science ®Google Scholar
• Paone P, Cani PD. Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut. 2020;69(12):2232–2243. doi:10.1136/gutjnl-2020-322260.
   PubMed Web of Science ®Google Scholar
• Derrien M, Vaughan EE, Plugge CM, de Vos WM. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol. 2004;54(5):1469–1476. doi:10.1099/ijs.0.02873-0.
   PubMed Web of Science ®Google Scholar
• Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM. The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol. 2008;74(5):1646–1648. doi:10.1128/AEM.01226-07.
   PubMed Web of Science ®Google Scholar
• Derrien M, Van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos WM. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila. Front Microbiol. 2011;2:166. doi:10.3389/fmicb.2011.00166.
   PubMed Web of Science ®Google Scholar
• Everard A, Lazarevic V, Gaia N, Johansson M, Stahlman M, Backhed F, Delzenne NM, Schrenzel J, François P, Cani PD. et al. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity. Isme J. 2014;8(10):2116–2130. doi:10.1038/ismej.2014.45.
   PubMed Web of Science ®Google Scholar
• Macchione IG, Lopetuso LR, Ianiro G, Napoli M, Gibiino G, Rizzatti G. et al. Key player in metabolic and gastrointestinal disorders. Eur Rev Med Pharmaco. 2019;23:8075–8083.
   PubMed Web of Science ®Google Scholar
• Zhang X, Shen D, Fang Z, Jie Z, Qiu X, Zhang C, Chen Y, Ji L. Human gut microbiota changes reveal the progression of glucose intolerance. PLoS One. 2013;8(8):e71108. doi:10.1371/journal.pone.0071108.
   PubMed Web of Science ®Google Scholar
• Kupritz J, Angelova A, Nutman TB, Gazzinelli-Guimaraes PH, Sibley LD. Helminth-induced human gastrointestinal dysbiosis: a systematic review and meta-analysis reveals insights into altered taxon diversity and microbial gradient collapse. mBio. 2021;12(6):e0289021. doi:10.1128/mBio.02890-21.
   PubMedGoogle Scholar
• Jenkins TP, Rathnayaka Y, Perera PK, Peachey LE, Nolan MJ, Krause L, Rajakaruna RS, Cantacessi C. Infections by human gastrointestinal helminths are associated with changes in faecal microbiota diversity and composition. PLoS One. 2017;12(9):e0184719. doi:10.1371/journal.pone.0184719.
   PubMed Web of Science ®Google Scholar
• Su C, Su L, Li Y, Long SR, Chang J, Zhang W, Walker WA, Xavier RJ, Cherayil BJ, Shi HN. et al. Helminth-induced alterations of the gut microbiota exacerbate bacterial colitis. Mucosal Immunol. 2018;11(1):144–157. doi:10.1038/mi.2017.20.
   PubMed Web of Science ®Google Scholar
• Su CW, Chen CY, Jiao L, Long SR, Mao T, Ji Q, O’Donnell S, Stanton C, Zheng S, Walker WA. et al. Helminth-induced and Th2-dependent alterations of the gut microbiota attenuate obesity caused by high-fat diet. Cell Mol Gastroenterol Hepatol. 2020;10(4):763–778. doi:10.1016/j.jcmgh.2020.06.010.
   PubMed Web of Science ®Google Scholar
• Wang J, Liu X, Sun R, Mao H, Liu M, Jin X, Gause WC. Akkermansia muciniphila participates in the host protection against helminth-induced cardiac fibrosis via TLR2. PLoS Pathog. 2023;19(10):e1011683. doi:10.1371/journal.ppat.1011683.
   PubMed Web of Science ®Google Scholar
• Liu S, Pan J, Meng X, Zhu J, Zhou J, Zhu X. Trichinella spiralis infection decreases the diversity of the intestinal flora in the infected mouse. J Microbiol Immunol Infect. 2021;54(3):490–500. doi:10.1016/j.jmii.2019.09.009.
   PubMedGoogle Scholar
• Xie Y, Xu D, Yan S, Hu X, Chen S, Guo K, Wang J, Chen Q, Guan W. The impact of MIF deficiency on alterations of fecal microbiota in C57BL/6 mice induced by Trichinella spiralis infection. FASEB J. 2023;37(10):e23202. doi:10.1096/fj.202300179RR.
   PubMed Web of Science ®Google Scholar
• Gui QF, Jin HL, Zhu F, Lu HF, Zhang Q, Xu J, Yang Y-M, Xiao C. Gut microbiota signatures in Schistosoma japonicum infection-induced liver cirrhosis patients: a case–control study. Infect Dis Poverty. 2021;10(1):10. doi:10.1186/s40249-021-00821-8.
   PubMed Web of Science ®Google Scholar
• Floudas A, Aviello G, Schwartz C, Jeffery IB, O’Toole PW, Fallon PG, Herbert DR. Schistosoma mansoni worm infection regulates the intestinal microbiota and susceptibility to colitis. Infect Immun. 2019;87(8). doi:10.1128/IAI.00275-19.
   PubMed Web of Science ®Google Scholar
• Jenkins TP, Peachey LE, Ajami NJ, MacDonald AS, Hsieh MH, Brindley PJ, Cantacessi C, Rinaldi G. Schistosoma mansoni infection is associated with quantitative and qualitative modifications of the mammalian intestinal microbiota. Sci Rep. 2018;8(1):12072. doi:10.1038/s41598-018-30412-x.
   PubMedGoogle Scholar
• Sharpe C, Thornton DJ, Grencis RK. A sticky end for gastrointestinal helminths; the role of the mucus barrier. Parasite Immunol. 2018;40(4):e12517. doi:10.1111/pim.12517.
   PubMed Web of Science ®Google Scholar
• Jin X, Liu Y, Wang J, Wang X, Tang B, Liu M, Liu X. β-glucan-triggered Akkermansia muciniphila expansion facilitates the expulsion of intestinal helminth via TLR2 in mice. Carbohydr Polym. 2022;275:118719. doi:10.1016/j.carbpol.2021.118719.
   PubMed Web of Science ®Google Scholar
• Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383(9936):2253–2264. doi:10.1016/S0140-6736(13)61949-2.
   PubMed Web of Science ®Google Scholar
• McManus DP, Bergquist R, Cai P, Ranasinghe S, Tebeje BM, You H. Schistosomiasis—from immunopathology to vaccines. Semin Immunopathol. 2020;42(3):355–371. doi:10.1007/s00281-020-00789-x.
   PubMed Web of Science ®Google Scholar
• Keshavarz Azizi Raftar S, Ashrafian F, Yadegar A, Lari A, Moradi HR, Shahriary A, Azimirad M, Alavifard H, Mohsenifar Z, Davari M. et al. The protective effects of live and pasteurized Akkermansia muciniphila and its extracellular vesicles against HFD/CCl4-Induced Liver Injury. Microbiol Spectr. 2021;9(2):e0048421. doi:10.1128/Spectrum.00484-21.
   PubMed Web of Science ®Google Scholar
• Schneider KM, Mohs A, Gui W, Galvez EJC, Candels LS, Hoenicke L, Muthukumarasamy U, Holland CH, Elfers C, Kilic K. et al. Imbalanced gut microbiota fuels hepatocellular carcinoma development by shaping the hepatic inflammatory microenvironment. Nat Commun. 2022;13(1):3964. doi:10.1038/s41467-022-31312-5.
   PubMed Web of Science ®Google Scholar
• Wang B, Chen X, Chen Z, Xiao H, Dong J, Li Y, Zeng X, Liu J, Wan G, Fan S. et al. Stable colonization of Akkermansia muciniphila educates host intestinal microecology and immunity to battle against inflammatory intestinal diseases. Experimental & Molecular Medicine. 2023;55(1):55–68. doi:10.1038/s12276-022-00911-z.
   PubMed Web of Science ®Google Scholar
• Ansaldo E, Slayden LC, Ching KL, Koch MA, Wolf NK, Plichta DR, Brown EM, Graham DB, Xavier RJ, Moon JJ. et al. Akkermansia muciniphila induces intestinal adaptive immune responses during homeostasis. Science. 2019;364(6446):1179–1184. doi:10.1126/science.aaw7479.
   PubMed Web of Science ®Google Scholar
• Bae M, Cassilly CD, Liu X, Park SM, Tusi BK, Chen X, Kwon J, Filipčík P, Bolze AS, Liu Z. et al. Akkermansia muciniphila phospholipid induces homeostatic immune responses. Nature. 2022;608(7921):168–173. doi:10.1038/s41586-022-04985-7.
   PubMed Web of Science ®Google Scholar
• Ierna MX, Scales HE, Mueller C, Lawrence CE. Transmembrane tumor necrosis factor alpha is required for enteropathy and is sufficient to promote parasite expulsion in gastrointestinal helminth infection. Infect Immun. 2009;77(9):3879–3885. doi:10.1128/IAI.01461-08.
   PubMed Web of Science ®Google Scholar
• Kim S, Shin YC, Kim TY, Kim Y, Lee YS, Lee SH, Kim M-N, O E, Kim KS, Kweon M-N. et al. Mucin degrader Akkermansia muciniphila accelerates intestinal stem cell-mediated epithelial development. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2021.1892441.
   PubMed Web of Science ®Google Scholar
• van der Lugt B, van Beek AA, Aalvink S, Meijer B, Sovran B, Vermeij WP, Brandt RMC, de Vos WM, Savelkoul HFJ, Steegenga WT. et al. Akkermansia muciniphila ameliorates the age-related decline in colonic mucus thickness and attenuates immune activation in accelerated aging Ercc1−/Δ7 mice. Immun Ageing. 2019;16(1):6. doi:10.1186/s12979-019-0145-z.
   PubMed Web of Science ®Google Scholar
• Yu J, Liu T, Guo Q, Wang Z, Chen Y, Dong Y, Fu Y. Disruption of the intestinal mucosal barrier induced by high fructose and restraint stress is regulated by the intestinal microbiota and microbiota metabolites. Microbiol Spectr. 2023;11(2):e0469822. doi:10.1128/spectrum.04698-22.
   PubMed Web of Science ®Google Scholar
• Martin-Gallausiaux C, Garcia-Weber D, Lashermes A, Larraufie P, Marinelli L, Teixeira V, Rolland A, Béguet-Crespel F, Brochard V, Quatremare T. et al. Akkermansia muciniphila upregulates genes involved in maintaining the intestinal barrier function via ADP-heptose-dependent activation of the ALPK1/TIFA pathway. Gut Microbes. 2022;14(1):2110639. doi:10.1080/19490976.2022.2110639.
   PubMed Web of Science ®Google Scholar
• Yoshihara T, Oikawa Y, Kato T, Kessoku T, Kobayashi T, Kato S, Misawa N, Ashikari K, Fuyuki A, Ohkubo H. et al. The protective effect of Bifidobacterium bifidum G9-1 against mucus degradation by Akkermansia muciniphila following small intestine injury caused by a proton pump inhibitor and aspirin. Gut Microbes. 2020;11(5):1385–1404. doi:10.1080/19490976.2020.1758290.
   PubMed Web of Science ®Google Scholar
• Desai MS, Seekatz AM, Koropatkin NM, Kamada N, Hickey CA, Wolter M, Pudlo NA, Kitamoto S, Terrapon N, Muller A. et al. A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell. 2016;167(5):1339–53 e21. doi:10.1016/j.cell.2016.10.043.
   PubMed Web of Science ®Google Scholar