Akkermansia muciniphila reduces susceptibility to Listeria monocytogenes infection in mice fed a high-fat diet

References

• Statovci D, Aguilera M, MacSharry J, Melgar S. The impact of western diet and nutrients on the microbiota and immune response at mucosal interfaces. Front Immunol. 2017;8:838. doi:10.3389/fimmu.2017.00838.
   PubMed Web of Science ®Google Scholar
• Las Heras V, Melgar S, MacSharry J, Gahan CGM. The influence of the western diet on microbiota and gastrointestinal immunity. Annu Rev Food Sci Technol. 2022;13(1):489–14. doi:10.1146/annurev-food-052720-011032.
   PubMedGoogle Scholar
• Las Heras V, Clooney AG, Ryan FJ, Cabrera-Rubio R, Casey PG, Hueston CM, Pinheiro J, Rudkin JK, Melgar S, Cotter PD, et al. Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection. Microbiome. 2019;7(1):7. doi:10.1186/s40168-019-0621-x.
   PubMedGoogle Scholar
• Wotzka SY, Kreuzer M, Maier L, Arnoldini M, Nguyen BD, Brachmann AO, Berthold DL, Zünd M, Hausmann A, Bakkeren E, et al. Escherichia coli limits Salmonella Typhimurium infections after diet shifts and fat-mediated microbiota perturbation in mice. Nature Microbiology. 2019;4(12):2164–2174. doi:10.1038/s41564-019-0568-5.
   PubMed Web of Science ®Google Scholar
• Nikitas G, Deschamps C, Disson O, Niault T, Cossart P, Lecuit M. Transcytosis of Listeria monocytogenes across the intestinal barrier upon specific targeting of goblet cell accessible E-cadherin. J Exp Med. 2011;208(11):2263–2277. doi:10.1084/jem.20110560.
   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
• Ouwerkerk Janneke P, van der Ark Kees CH, Davids M, Claassens Nico J, Finestra Teresa R, de Vos Willem M, van der Ark KCH, de Vos WM, Belzer C. Adaptation of akkermansia muciniphila to the oxic-anoxic interface of the mucus layer. Appl Environ Microbiol. 2016;82(23):6983–6993. doi:10.1128/AEM.01641-16.
   PubMed Web of Science ®Google Scholar
• Sonoyama K, Fujiwara R, Takemura N, Ogasawara T, Watanabe J, Ito H, Morita T. Response of gut microbiota to fasting and hibernation in syrian hamsters. Appl Environ Microb. 2009;75(20):6451–6456. doi:10.1128/AEM.00692-09.
   PubMed Web of Science ®Google Scholar
• van Passel MW, Kant R, Zoetendal EG, Plugge CM, Derrien M, Malfatti SA, van Passel MWJ, Chain PSG, Woyke T, Palva A, et al. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS One. 2011;6(3):e16876. doi:10.1371/journal.pone.0016876.
   PubMed Web of Science ®Google Scholar
• Derrien M, van Baarlen P, Hooiveld G, Norin E, Muller M, de Vos W. Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the mucin-degrader akkermansia muciniphila. Front Microbiol. 2011;2. doi:10.3389/fmicb.2011.00166.
   Web of Science ®Google Scholar
• Derrien M, van Passel MW, van de Bovenkamp JH, Schipper RG, de Vos WM, Dekker J, de Vos W. Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes. 2010;1(4):254–268. doi:10.4161/gmic.1.4.12778.
   PubMed Web of Science ®Google Scholar
• Belzer C, Chia LW, Aalvink S, Chamlagain B, Piironen V, Knol J, de Vos WM. Microbial metabolic networks at the mucus layer lead to diet-independent butyrate and vitamin B 12 production by intestinal symbionts. mBio. 2017;8(5). doi:10.1128/mBio.00770-17.
   PubMed Web of Science ®Google Scholar
• Amiri P, Hosseini SA, Ghaffari S, Tutunchi H, Ghaffari S, Mosharkesh E, Asghari S, Roshanravan N. Role of butyrate, a gut microbiota derived metabolite, in cardiovascular diseases: a comprehensive narrative review. Front Pharmacol. 2022;12:12. doi:10.3389/fphar.2021.837509.
   Web of Science ®Google Scholar
• Ottman N, Reunanen J, Meijerink M, Pietilä TE, Kainulainen V, Klievink J, Huuskonen L, Aalvink S, Skurnik M, Boeren S, et al. Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS One. 2017;12(3):e0173004. doi:10.1371/journal.pone.0173004.
   PubMed Web of Science ®Google Scholar
• Shin NR, Lee JC, Lee HY, Kim MS, Whon TW, Lee MS, Bae J-W. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut. 2014;63(5):727–735. doi:10.1136/gutjnl-2012-303839.
   PubMed Web of Science ®Google Scholar
• Bodogai M, O’Connell J, Kim K, Kim Y, Moritoh K, Chen C, Gusev F, Vaughan K, Shulzhenko N, Mattison JA, et al. Commensal bacteria contribute to insulin resistance in aging by activating innate B1a cells. Sci Transl Med. 2018;10(467). doi:10.1126/scitranslmed.aat4271.
   PubMed Web of Science ®Google Scholar
• Xu Y, Wang N, Tan H-Y, Li S, Zhang C, Feng Y. Function of Akkermansia muciniphila in obesity: interactions with lipid metabolism, immune response and gut systems. Front Microbiol. 2020;11:11. doi:10.3389/fmicb.2020.00219.
   Web of Science ®Google Scholar
• Ashrafian F, Keshavarz Azizi Raftar S, Lari A, Shahryari A, Abdollahiyan S, Moradi HR, Masoumi M, Davari M, Khatami S, Omrani MD, et al. Extracellular vesicles and pasteurized cells derived from Akkermansia muciniphila protect against high-fat induced obesity in mice. Microb Cell Fact. 2021;20(1):219. doi:10.1186/s12934-021-01709-w.
   PubMed Web of Science ®Google Scholar
• Schneeberger M, Everard A, Gómez-Valadés AG, Matamoros S, Ramírez S, Delzenne NM, Gomis R, Claret M, Cani PD. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5(1):16643. doi:10.1038/srep16643.
   PubMed Web of Science ®Google Scholar
• Png CW, Lindén SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin THJ. Mucolytic bacteria with increased prevalence in IBD mucosa AugmentIn VitroUtilization of mucin by other bacteria. Official Am J Gastroentero. 2010;105(11):2420–2428. doi:10.1038/ajg.2010.281.
   PubMed Web of Science ®Google Scholar
• Takiishi T, Fenero CIM, Câmara NOS. Intestinal barrier and gut microbiota: shaping our immune responses throughout life. Tissue Barriers. 2017;5(4):e1373208. doi:10.1080/21688370.2017.1373208.
   PubMed Web of Science ®Google Scholar
• Magne F, Gotteland M, Gauthier L, Zazueta A, Pesoa S, Navarrete P, Balamurugan R. The firmicutes/bacteroidetes ratio: a relevant marker of gut dysbiosis in obese patients? Nutrients. 2020;12(5):1474. doi:10.3390/nu12051474.
   PubMed Web of Science ®Google Scholar
• Xu Y, Wang N, Tan HY, Li S, Zhang C, Feng Y. Function of Akkermansia muciniphila in obesity: interactions with lipid metabolism, immune response and gut systems. Front Microbiol. 2020;11:219. doi:10.3389/fmicb.2020.00219.
   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 USA. 2013;110(22):9066–9071. doi:10.1073/pnas.1219451110.
   PubMed Web of Science ®Google Scholar
• Wu W, Lv L, Shi D, Ye J, Fang D, Guo F, Li Y, He X, Li L. Protective effect of Akkermansia muciniphila against immune-mediated liver injury in a mouse model. Front Microbiol. 2017;8:1804. doi:10.3389/fmicb.2017.01804.
   PubMed Web of Science ®Google Scholar
• Rao Y, Kuang Z, Li C, Guo S, Xu Y, Zhao D, Hu Y, Song B, Jiang Z, Ge Z, et al. Gut Akkermansia muciniphila ameliorates metabolic dysfunction-associated fatty liver disease by regulating the metabolism of L-aspartate via gut-liver axis. Gut Microbes. 2021;13(1):1–19. doi:10.1080/19490976.2021.1927633.
   PubMed Web of Science ®Google Scholar
• Collado MC, Laitinen K, Salminen S, Isolauri E. Maternal weight and excessive weight gain during pregnancy modify the immunomodulatory potential of breast milk. Pediatr Res. 2012;72(1):77–85. doi:10.1038/pr.2012.42.
   PubMed Web of Science ®Google Scholar
• Wu Z, Xu Q, Gu S, Chen Y, Lv L, Zheng B, Wang Q, Wang K, Wang S, Xia J, et al. Akkermansia muciniphila ameliorates clostridioides difficile infection in mice by modulating the intestinal microbiome and metabolites. Front Microbiol. 2022;13:841920. doi:10.3389/fmicb.2022.841920.
   PubMed Web of Science ®Google Scholar
• Serbina NV, Shi C, Pamer EG. Monocyte-mediated immune defense against murine Listeria monocytogenes infection. Adv Immunol. 2012;113:119–134.
   PubMed Web of Science ®Google Scholar
• Singh RP, Halaka DA, Hayouka Z, Tirosh O. High-fat diet induced alteration of mice microbiota and the functional ability to utilize fructooligosaccharide for ethanol production. Front Cell Infect Microbiol. 2020;10:376. doi:10.3389/fcimb.2020.00376.
   PubMed Web of Science ®Google Scholar
• Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD, et al. High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology. 2009;137(5):1716-24.e1–2. doi:10.1053/j.gastro.2009.08.042.
   Web of Science ®Google Scholar
• Hänninen A, Toivonen R, Pöysti 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, Everard A, Druart C, Plovier H, Van Hul M, Vieira-Silva S, Falony G, Raes J, Maiter D, Delzenne NM, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: a proof-of-concept exploratory study. Nat Med. 2019;25(7):1096–1103. doi:10.1038/s41591-019-0495-2.
   PubMed Web of Science ®Google Scholar
• Becattini S, Littmann ER, Carter RA, Kim SG, Morjaria SM, Ling L, Gyaltshen Y, Fontana E, Taur Y, Leiner IM, et al. Commensal microbes provide first line defense against Listeria monocytogenes infection. J Exp Med. 2017;214(7):1973–1989. doi:10.1084/jem.20170495.
   PubMed Web of Science ®Google Scholar
• Drolia R, Tenguria S, Durkes AC, Turner JR, Bhunia AK. Listeria adhesion protein induces intestinal epithelial barrier dysfunction for bacterial translocation. Cell Host & Microbe. 2018;23(4):470–84.e7. doi:10.1016/j.chom.2018.03.004.
   PubMed Web of Science ®Google Scholar
• Andrews S, Krueger F, Segonds-Pichon A, Biggins L, Krueger C, Wingett S. FastQC: a quality control tool for high throughput sequence data. Cambridge, UK: Babraham Institute; 2010.
   Google Scholar
• Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32(19):3047–3048. doi:10.1093/bioinformatics/btw354.
   PubMed Web of Science ®Google Scholar
• Marcel M. Cutadapt removes adapter sequences from high-throughput sequencing reads, EMB net. EMBnet J. 2011;17(1):10–12. doi:10.14806/ej.17.1.200.
   Google Scholar
• Weinstein MM, Prem A, Jin M, Tang S, Bhasin JM. FIGARO: an efficient and objective tool for optimizing microbiome rRNA gene trimming parameters. bioRxiv. 2019;610394. doi:10.1101/610394.
   Google Scholar
• Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi:10.1038/nmeth.3869.
   PubMed Web of Science ®Google Scholar
• Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–D6. doi:10.1093/nar/gks1219.
   PubMed Web of Science ®Google Scholar
• Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6(1):226. doi:10.1186/s40168-018-0605-2.
   PubMedGoogle Scholar
• McMurdie PJ, Holmes S, Watson M. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217. doi:10.1371/journal.pone.0061217.
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi:10.1186/s13059-014-0550-8.
   PubMed Web of Science ®Google Scholar
• Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin P, O’hara R, Simpson GL, Solymos P, Stevens MH, Wagner H. Community ecology package. R Package Version. 2013;2:321–326.
   Google Scholar
• Johnsen LG, Skou PB, Khakimov B, Bro R. Gas chromatography - mass spectrometry data processing made easy. J Chromatogr A. 2017;1503:57–64. doi:10.1016/j.chroma.2017.04.052.
   PubMed Web of Science ®Google Scholar
• Doneanu CE, Chen W, Mazzeo JR. Uplc/Ms monitoring of water-soluble vitamin bs in cell culture media in minutes. Waters Corporation Application Note. 2011;1–7. https://www.waters.com/webassets/cms/library/docs/720004042en.pdf
   Google Scholar