Hyperbaric oxygen augments susceptibility to C. difficile infection by impairing gut microbiota ability to stimulate the HIF-1α-IL-22 axis in ILC3

References

• Huang X, Liang P, Jiang B, Zhang P, Yu W, Duan M, Guo L, Cui X, Huang M, Huang X. Hyperbaric oxygen potentiates diabetic wound healing by promoting fibroblast cell proliferation and endothelial cell angiogenesis. Life Sci. 2020;259:118246. doi:10.1016/j.lfs.2020.118246.
   PubMed Web of Science ®Google Scholar
• Dhingra S, Buckey JC, Cramer RA. Hyperbaric oxygen reduces aspergillus fumigatus proliferation in vitro and influences in vivo disease outcomes. Antimicrob Agents Chemother. 2018;62(3):62. doi:10.1128/AAC.01953-17.
   Web of Science ®Google Scholar
• Memar MY, Yekani M, Alizadeh N, Baghi HB. Hyperbaric oxygen therapy: antimicrobial mechanisms and clinical application for infections. Biomed Pharmacother. 2019;109:440–26. doi:10.1016/j.biopha.2018.10.142.
   PubMed Web of Science ®Google Scholar
• Tuk B, Tong M, Fijneman EMG, van Neck JW, Deli MA. Hyperbaric oxygen therapy to treat diabetes impaired wound healing in rats. PLoS ONE. 2014;9(10):e108533. doi:10.1371/journal.pone.0108533.
   PubMed Web of Science ®Google Scholar
• Glover LE, Lee JS, Colgan SP. Oxygen metabolism and barrier regulation in the intestinal mucosa. J Clin Invest. 2016;126(10):3680–3688. doi:10.1172/JCI84429.
   PubMed Web of Science ®Google Scholar
• Singhal R, Shah YM. Oxygen battle in the gut: hypoxia and hypoxia-inducible factors in metabolic and inflammatory responses in the intestine. J Biol Chem. 2020;295(30):10493–10505. doi:10.1074/jbc.REV120.011188.
   PubMed Web of Science ®Google Scholar
• Pral LP, Fachi JL, Corrêa RO, Colonna M, Vinolo MAR. Hypoxia and HIF-1 as key regulators of gut microbiota and host interactions. Trends Immunol. 2021;42(7):604–621. doi:10.1016/j.it.2021.05.004.
   PubMed Web of Science ®Google Scholar
• Vacca I. The microbiota maintains oxygen balance in the gut. Nat Rev Microbiol. 2017;15(10):574–575. doi:10.1038/nrmicro.2017.112.
   Web of Science ®Google Scholar
• Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–71. doi:10.1038/s41579-020-0433-9.
   PubMed Web of Science ®Google Scholar
• Rigottier-Gois L. Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis. ISME J. 2013;7(7):1256–1261. doi:10.1038/ismej.2013.80.
   PubMed Web of Science ®Google Scholar
• Henson MA, Phalak P. Microbiota dysbiosis in inflammatory bowel diseases: in silico investigation of the oxygen hypothesis. BMC Syst Biol. 2017;11(1):145. doi:10.1186/s12918-017-0522-1.
   PubMedGoogle Scholar
• Ott SJ. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53(5):685–693. doi:10.1136/gut.2003.025403.
   PubMed Web of Science ®Google Scholar
• Manichanh C. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut. 2006;55:205–211. doi:10.1136/gut.2005.073817.
   PubMed Web of Science ®Google Scholar
• Frank DN, St. Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA. 2007;104(34):13780–13785. doi:10.1073/pnas.0706625104.
   PubMed Web of Science ®Google Scholar
• Ashley SL, Sjoding MW, Popova AP, Cui TX, Hoostal MJ, Schmidt TM, Branton WR, Dieterle MG, Falkowski NR, Baker JM, et al. Lung and gut microbiota are altered by hyperoxia and contribute to oxygen-induced lung injury in mice. Sci Transl Med. 2020;12(556):12. doi:10.1126/scitranslmed.aau9959.
   Web of Science ®Google Scholar
• Li Y, Tao Y, Xu J, He Y, Zhang W, Jiang Z, He Y, Liu H, Chen M, Zhang W, et al. Hyperoxia provokes time- and dose-dependent gut injury and endotoxemia and alters gut microbiome and transcriptome in mice. Front Med. 2021;8. doi:10.3389/fmed.2021.732039.
   Web of Science ®Google Scholar
• Ni Y-N, Wang Y-M, Liang B-M, Liang Z-A. The effect of hyperoxia on mortality in critically ill patients: a systematic review and meta analysis. BMC Pulm Med. 2019;19(1):53. doi:10.1186/s12890-019-0810-1.
   PubMedGoogle Scholar
• Douin DJ, Anderson EL, Dylla L, Rice JD, Jackson CL, Wright FL, Bebarta VS, Schauer SG, Ginde AA. Association between Hyperoxia, supplemental Oxygen, and mortality in critically injured patients. Crit Care Explor. 2021;3(5):e0418. doi:10.1097/CCE.0000000000000418.
   PubMedGoogle Scholar
• Pelletier JH, Ramgopal S, Horvat CM. Hyperoxemia is associated with mortality in critically Ill children. Front Med. 2021;8. doi:10.3389/fmed.2021.675293.
   Web of Science ®Google Scholar
• Novak S, Drenjancevic I, Vukovic R, Kellermayer Z, Cosic A, Tolusic Levak M, Balogh P, Culo F, Mihalj M. Anti-inflammatory effects of hyperbaric oxygenation during DSS-Induced colitis in BALB/c mice include changes in gene expression of HIF-1 α , proinflammatory cytokines, and antioxidative enzymes. Mediators Inflamm. 2016;2016:1–19. doi:10.1155/2016/7141430.
   Web of Science ®Google Scholar
• Gonzalez CG, Mills RH, Kordahi MC, Carrillo-Terrazas M, Secaira-Morocho H, Widjaja CE, Tsai MS, Mittal Y, Yee BA, Vargas F, et al. The host-microbiome response to hyperbaric oxygen therapy in ulcerative colitis patients. Cell Mol Gastroenterol Hepatol. 2022;14(1):35–53. doi:10.1016/j.jcmgh.2022.03.008.
   PubMed Web of Science ®Google Scholar
• Atug O, Hamzaoglu H, Tahan V, Alican I, Kurtkaya O, Elbuken E, Ozdogan O, Tozun N. Hyperbaric oxygen therapy is as effective as Dexamethasone in the treatment of TNBS-E-Induced experimental colitis. Dig Dis Sci. 2008;53(2):481–485. doi:10.1007/s10620-007-9956-4.
   PubMed Web of Science ®Google Scholar
• Vivier E, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, Koyasu S, Locksley RM, McKenzie ANJ, Mebius RE, et al. Innate lymphoid cells: 10 years on. Cell. 2018;174(5):1054–1066. doi:10.1016/j.cell.2018.07.017.
   PubMed Web of Science ®Google Scholar
• Guo X, Qiu J, Tu T, Yang X, Deng L, Anders RA, Zhou L, Fu Y-X. Induction of innate lymphoid cell-derived interleukin-22 by the transcription factor STAT3 mediates protection against intestinal infection. Immunity. 2014;40(1):25–39. doi:10.1016/j.immuni.2013.10.021.
   PubMed Web of Science ®Google Scholar
• Glal D, Sudhakar JN, Lu H-H, Liu M-C, Chiang H-Y, Liu Y-C, Cheng C-F, Shui J-W. ATF3 sustains IL-22-Induced STAT3 phosphorylation to maintain mucosal immunity through inhibiting phosphatases. Front Immunol. 2018;9. doi:10.3389/fimmu.2018.02522.
   PubMed Web of Science ®Google Scholar
• Longeville S, Stingaciu L-R. Hemoglobin diffusion and the dynamics of oxygen capture by red blood cells. Sci Rep. 2017;7(1):10448. doi:10.1038/s41598-017-09146-9.
   PubMedGoogle Scholar
• Taylor CT, Colgan SP. Hypoxia and gastrointestinal disease. J Mol Med (Berl). 2007;85(12):1295–1300. doi:10.1007/s00109-007-0277-z.
   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
• La Reau AJ, Suen G. The Ruminococci: key symbionts of the gut ecosystem. J Microbiol. 2018;56(3):199–208. doi:10.1007/s12275-018-8024-4.
   PubMed Web of Science ®Google Scholar
• Becattini S, Taur Y, Pamer EG. Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol Med. 2016;22(6):458–478. doi:10.1016/j.molmed.2016.04.003.
   PubMed Web of Science ®Google Scholar
• Kumar A, Pramanik J, Goyal N, Chauhan D, Sivamaruthi BS, Prajapati BG, Chaiyasut C. Gut microbiota in anxiety and depression: unveiling the relationships and management options. Pharmaceuticals. 2023;16(4):565. doi:10.3390/ph16040565.
   Web of Science ®Google Scholar
• Parker BJ, Wearsch PA, Veloo ACM, Rodriguez-Palacios A. The genus alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front Immunol. 2020;11:11. doi:10.3389/fimmu.2020.00906.
   PubMed Web of Science ®Google Scholar
• Chen X, Katchar K, Goldsmith JD, Nanthakumar N, Cheknis A, Gerding DN, Kelly CP. A mouse model of clostridium difficile–associated disease. Gastroenterology. 2008;135(6):1984–1992. doi:10.1053/j.gastro.2008.09.002.
   PubMed Web of Science ®Google Scholar
• Theriot CM, Koenigsknecht MJ, Carlson PE, Hatton GE, Nelson AM, Li B, GB H, Li JZ, Young VB. Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to clostridium difficile infection. Nat Commun. 2014;5(1):3114. doi:10.1038/ncomms4114.
   PubMed Web of Science ®Google Scholar
• Fachi JL, Sécca C, Rodrigues PB, de Mato FCP, Di Luccia B, de Felipe JS, LP P, Rungue M, de Rocha VM, Sato FT, et al. Acetate coordinates neutrophil and ILC3 responses against C. difficile through FFAR2. J Exp Med. 2020;217(3). doi: 10.1084/jem.20190489.
   Web of Science ®Google Scholar
• Merrigan M, Venugopal A, Mallozzi M, Roxas B, Viswanathan VK, Johnson S, Gerding DN, Vedantam G. Human hypervirulent clostridium difficile strains exhibit increased sporulation as well as robust toxin production. J Bacteriol. 2010;192(19):4904–4911. doi:10.1128/JB.00445-10.
   PubMed Web of Science ®Google Scholar
• Zhu S, Han M, Liu S, Fan L, Shi H, Li P. Composition and diverse differences of intestinal microbiota in ulcerative colitis patients. Front Cell Infect Microbiol. 2022;12:12. doi:10.3389/fcimb.2022.953962.
   Web of Science ®Google Scholar
• Vester-Andersen MK, Mirsepasi-Lauridsen HC, Prosberg MV, Mortensen CO, Träger C, Skovsen K, Thorkilgaard T, Nøjgaard C, Vind I, Krogfelt KA, et al. Increased abundance of proteobacteria in aggressive Crohn’s disease seven years after diagnosis. Sci Rep. 2019;9(1):13473. doi:10.1038/s41598-019-49833-3.
   PubMed Web of Science ®Google Scholar
• Shin N-R, Whon TW, Bae J-W. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;33(9):496–503. doi:10.1016/j.tibtech.2015.06.011.
   PubMed Web of Science ®Google Scholar
• Corrêa-Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short-chain fatty acids. Clin Trans Immunol. 2016;5(4):e73. doi:10.1038/cti.2016.17.
   PubMedGoogle Scholar
• Fachi JL, de Sde Felipe JS, Pral LP, da Silva BK, RO C, de Andrade MCP, da Fonseca DM, PJ B, Câmara NOS, de Sales ÉL, et al. Butyrate protects mice from clostridium difficile-induced colitis through an HIF-1-Dependent mechanism. Cell Rep. 2019;27(3):750–761.e7. doi:10.1016/j.celrep.2019.03.054.
   PubMed Web of Science ®Google Scholar
• Comalada M, Bailón E, de Haro O, Lara-Villoslada F, Xaus J, Zarzuelo A, Gálvez J. The effects of short-chain fatty acids on colon epithelial proliferation and survival depend on the cellular phenotype. J Cancer Res Clin Oncol. 2006;132(8):487–497. doi:10.1007/s00432-006-0092-x.
   PubMed Web of Science ®Google Scholar
• Peng L, Li Z-R, Green RS, Holzmanr IR, Lin J. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-Activated protein kinase in caco-2 cell monolayers. J Nutr. 2009;139(9):1619–1625. doi:10.3945/jn.109.104638.
   PubMed Web of Science ®Google Scholar
• Kelly CJ, Zheng L, Campbell EL, Saeedi B, Scholz CC, Bayless AJ, Wilson KE, Glover LE, Kominsky DJ, Magnuson A, et al. Crosstalk between microbiota-derived short-chain fatty acids and intestinal epithelial HIF augments tissue barrier function. Cell Host & Microbe. 2015;17(5):662–671. doi:10.1016/j.chom.2015.03.005.
   PubMed Web of Science ®Google Scholar
• Byndloss MX, Olsan EE, Rivera-Chávez F, Tiffany CR, Cevallos SA, Lokken KL, Torres TP, Byndloss AJ, Faber F, Gao Y, et al. Microbiota-activated PPAR-γ signaling inhibits dysbiotic enterobacteriaceae expansion. Sci. 2017;357(6351):570–575. doi:10.1126/science.aam9949. 1979.
   PubMed Web of Science ®Google Scholar
• Thio C-P, Chi P-Y, Lai A-Y, Chang Y-J. Regulation of type 2 innate lymphoid cell–dependent airway hyperreactivity by butyrate. J Allergy Clin Immunol. 2018;142(6):1867–1883.e12. doi:10.1016/j.jaci.2018.02.032.
   PubMed Web of Science ®Google Scholar
• Pickert G, Neufert C, Leppkes M, Zheng Y, Wittkopf N, Warntjen M, Lehr H-A, Hirth S, Weigmann B, Wirtz S, et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med. 2009;206(7):1465–1472. doi:10.1084/jem.20082683.
   PubMed Web of Science ®Google Scholar
• Fachi JL, Pral LP, dos Santos JAC, Codo AC, de Oliveira S, Felipe JS, Zambom FFF, Câmara NOS, Vieira PMMM, Colonna M, et al. Hypoxia enhances ILC3 responses through HIF-1α-dependent mechanism. Mucosal Immunol. 2021;14(4):828–841. doi:10.1038/s41385-020-00371-6.
   PubMed Web of Science ®Google Scholar
• Di Luccia B, Gilfillan S, Cella M, Colonna M, Huang S-C. ILC3s integrate glycolysis and mitochondrial production of reactive oxygen species to fulfill activation demands. J Exp Med. 2019;216(10):2231–2241. doi:10.1084/jem.20180549.
   PubMed Web of Science ®Google Scholar
• Teufel C, Horvath E, Peter A, Ercan C, Piscuoglio S, Hall MN, Finke D, Lehmann FM. mTOR signaling mediates ILC3-driven immunopathology. Mucosal Immunol. 2021;14(6):1323–1334. doi:10.1038/s41385-021-00432-4.
   PubMed Web of Science ®Google Scholar
• Yu F, White SB, Zhao Q, Lee FS. HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA. 2001;98(17):9630–9635. doi:10.1073/pnas.181341498.
   PubMed Web of Science ®Google Scholar
• Alenazi N, Alsaeed H, Alsulami A, Alanzi T. A review of hyperbaric oxygen therapy for inflammatory bowel disease. Int J Gen Med. 2021;14:7099–7105. doi:10.2147/IJGM.S336678.
   PubMed Web of Science ®Google Scholar
• Pagoldh M, Hultgren E, Arnell P, Eriksson A. Hyperbaric oxygen therapy does not improve the effects of standardized treatment in a severe attack of ulcerative colitis: a prospective randomized study. Scand J Gastroenterol. 2013;48(9):1033–1040. doi:10.3109/00365521.2013.819443.
   PubMed Web of Science ®Google Scholar
• Abt MC, Lewis BB, Caballero S, Xiong H, Carter RA, Sušac B, Ling L, Leiner I, Pamer EG. Innate immune defenses mediated by two ILC subsets are critical for protection against acute clostridium difficile infection. Cell Host & Microbe. 2015;18(1):27–37. doi:10.1016/j.chom.2015.06.011.
   PubMed Web of Science ®Google Scholar
• Nagao-Kitamoto H, Leslie JL, Kitamoto S, Jin C, Thomsson KA, Gillilland MG, Kuffa P, Goto Y, Jenq RR, Ishii C, et al. Interleukin-22-mediated host glycosylation prevents clostridioides difficile infection by modulating the metabolic activity of the gut microbiota. Nat Med. 2020;26(4):608–617. doi:10.1038/s41591-020-0764-0.
   PubMed Web of Science ®Google Scholar
• Cribas ES, Denny JE, Maslanka JR, Abt MC, Freitag NE. Loss of interleukin-10 (IL-10) signaling promotes IL-22-Dependent host defenses against acute clostridioides difficile infection. Infect Immun. 2021;89(5):89. doi:10.1128/IAI.00730-20.
   Web of Science ®Google Scholar
• Hasegawa M, Yada S, Liu MZ, Kamada N, Muñoz-Planillo R, Do N, Núñez G, Inohara N. Interleukin-22 regulates the complement system to promote resistance against pathobionts after pathogen-induced intestinal damage. Immunity. 2014;41(4):620–632. doi:10.1016/j.immuni.2014.09.010.
   PubMed Web of Science ®Google Scholar
• Albenberg L, Esipova TV, Judge CP, Bittinger K, Chen J, Laughlin A, Grunberg S, Baldassano RN, Lewis JD, Li H, et al. Correlation between intraluminal oxygen gradient and radial partitioning of intestinal microbiota. Gastroenterology. 2014;147(5):1055–1063.e8. doi:10.1053/j.gastro.2014.07.020.
   PubMed Web of Science ®Google Scholar
• Moreno-Indias I, Torres M, Montserrat JM, Sanchez-Alcoholado L, Cardona F, Tinahones FJ, Gozal D, Poroyko VA, Navajas D, Queipo-Ortuño MI, et al. Intermittent hypoxia alters gut microbiota diversity in a mouse model of sleep apnoea. Eur Respir J. 2015;45(4):1055–1065. doi:10.1183/09031936.00184314.
   PubMed Web of Science ®Google Scholar
• Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux J-J, Blugeon S, Bridonneau C, Furet J-P, Corthier G, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008;105(43):16731–16736. doi:10.1073/pnas.0804812105.
   PubMed Web of Science ®Google Scholar
• Baughn AD, Malamy MH. The strict anaerobe bacteroides fragilis grows in and benefits from nanomolar concentrations of oxygen. Nature. 2004;427(6973):441–444. doi:10.1038/nature02285.
   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
• Earley H, Lennon G, Balfe Á, Coffey JC, Winter DC, O’Connell PR. The abundance of Akkermansia muciniphila and its relationship with sulphated colonic mucins in health and ulcerative colitis. Sci Rep. 2019;9(1):15683. doi:10.1038/s41598-019-51878-3.
   PubMedGoogle Scholar
• Collado MC, Derrien M, Isolauri E, de Vos WM, Salminen S. Intestinal integrity and akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Appl Environ Microbiol. 2007;73(23):7767–7770. doi:10.1128/AEM.01477-07.
   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
• Caesar R, Tremaroli V, Kovatcheva-Datchary P, Cani PD, Bäckhed F. Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab. 2015;22(4):658–668. doi:10.1016/j.cmet.2015.07.026.
   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. doi:10.3389/fmicb.2022.841920.
   Web of Science ®Google Scholar
• van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, Visser CE, Kuijper EJ, Bartelsman JFWM, Tijssen JGP, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. N Engl J Med. 2013;368(5):407–415. doi:10.1056/NEJMoa1205037.
   PubMed Web of Science ®Google Scholar
• Zuo T, Zhang F, Lui GCY, Yeoh YK, AYL L, Zhan H, Wan Y, Chung ACK, Cheung CP, Chen N, et al. Alterations in gut microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology. 2020;159(3):944–955.e8. doi:10.1053/j.gastro.2020.05.048.
   PubMed Web of Science ®Google Scholar
• Baccolini V, Migliara G, Isonne C, Dorelli B, Barone LC, Giannini D, Marotta D, Marte M, Mazzalai E, Alessandri F, et al. The impact of the COVID-19 pandemic on healthcare-associated infections in intensive care unit patients: a retrospective cohort study. Antimicrob Resist Infect Control. 2021;10(1):87. doi:10.1186/s13756-021-00959-y.
   PubMed Web of Science ®Google Scholar
• Kampmeier S, Tönnies H, Correa-Martinez CL, Mellmann A, Schwierzeck V. A nosocomial cluster of vancomycin resistant enterococci among COVID-19 patients in an intensive care unit. Antimicrob Resist Infect Control. 2020;9(1):154. doi:10.1186/s13756-020-00820-8.
   PubMed Web of Science ®Google Scholar
• Maslennikov R, Ivashkin V, Ufimtseva A, Poluektova E, Ulyanin A. Clostridioides difficile co-infection in patients with COVID-19. Future Microbiol. 2022;17(9):653–663. doi:10.2217/fmb-2021-0145.
   PubMed Web of Science ®Google Scholar
• Rivera-Chávez F, Zhang LF, Faber F, Lopez CA, Byndloss MX, Olsan EE, Xu G, Velazquez EM, Lebrilla CB, Winter SE, et al. Depletion of Butyrate-Producing Clostridia from the gut microbiota drives an aerobic luminal expansion of Salmonella. Cell Host & Microbe. 2016;19(4):443–454. doi:10.1016/j.chom.2016.03.004.
   PubMed Web of Science ®Google Scholar
• Yang W, Yu T, Huang X, Bilotta AJ, Xu L, Lu Y, Sun J, Pan F, Zhou J, Zhang W, et al. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020;11(1):4457. doi:10.1038/s41467-020-18262-6.
   PubMed Web of Science ®Google Scholar
• Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–450. doi:10.1038/nature12721.
   PubMed Web of Science ®Google Scholar
• Lührs H, Gerke T, Müller JG, Melcher R, Schauber J, Boxberger F, Scheppach W, Menzel T. Butyrate inhibits NF-κB activation in lamina propria macrophages of patients with ulcerative colitis. Scand J Gastroenterol. 2002;37(4):458–466. doi:10.1080/003655202317316105.
   PubMed Web of Science ®Google Scholar
• Zimmerman MA, Singh N, Martin PM, Thangaraju M, Ganapathy V, Waller JL, Shi H, Robertson KD, Munn DH, Liu K. Butyrate suppresses colonic inflammation through HDAC1-dependent fas upregulation and fas-mediated apoptosis of T cells. Am J Physiol-Gastr L. 2012;302(12):G1405–15. doi:10.1152/ajpgi.00543.2011.
   PubMed Web of Science ®Google Scholar
• Chun E, Lavoie S, Fonseca-Pereira D, Bae S, Michaud M, Hoveyda HR, Fraser GL, Gallini Comeau CA, Glickman JN, Fuller MH, et al. Metabolite-sensing receptor Ffar2 regulates colonic group 3 Innate Lymphoid Cells and gut immunity. Immunity. 2019;51(5):871–884.e6. doi:10.1016/j.immuni.2019.09.014.
   PubMed Web of Science ®Google Scholar
• Lindemans CA, Calafiore M, Mertelsmann AM, O’Connor MH, Dudakov JA, Jenq RR, Velardi E, Young LF, Smith OM, Lawrence G, et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature. 2015;528(7583):560–564. doi:10.1038/nature16460.
   PubMed Web of Science ®Google Scholar
• Keir ME, Yi T, Lu TT, Ghilardi N. The role of IL-22 in intestinal health and disease. J Exp Med. 2020;217(3). doi: 10.1084/jem.20192195.
   PubMed Web of Science ®Google Scholar
• Bäcker V, Cheung F-Y, Siveke JT, Fandrey J, Winning S, Taylor CT. Knockdown of myeloid cell hypoxia-inducible factor-1α ameliorates the acute pathology in DSS-induced colitis. PLoS ONE. 2017;12(12):e0190074. doi:10.1371/journal.pone.0190074.
   PubMed Web of Science ®Google Scholar
• Flück K, Breves G, Fandrey J, Winning S. Hypoxia-inducible factor 1 in dendritic cells is crucial for the activation of protective regulatory T cells in murine colitis. Mucosal Immunol. 2016;9(2):379–390. doi:10.1038/mi.2015.67.
   PubMed Web of Science ®Google Scholar
• Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, et al. HIF-1α Is Essential for Myeloid Cell-Mediated Inflammation. Cell. 2003;112(5):645–657. doi:10.1016/S0092-8674(03)00154-5.
   PubMed Web of Science ®Google Scholar
• Dang EV, Barbi J, Yang H-Y, Jinasena D, Yu H, Zheng Y, Bordman Z, Fu J, Kim Y, Yen H-R, et al. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell. 2011;146(5):772–784. doi:10.1016/j.cell.2011.07.033.
   PubMed Web of Science ®Google Scholar
• Krzywinska E, Sobecki M, Nagarajan S, Zacharjasz J, Tambuwala MM, Pelletier A, Cummins E, Gotthardt D, Fandrey J, Kerdiles YM, et al. The transcription factor HIF-1α mediates plasticity of NKp46+ innate lymphoid cells in the gut. J Exp Med. 2022;219(2). doi: 10.1084/jem.20210909.
   PubMed Web of Science ®Google Scholar
• Klose CSN, Kiss EA, Schwierzeck V, Ebert K, Hoyler T, d’Hargues Y, Göppert N, Croxford AL, Waisman A, Tanriver Y, et al. A T-bet gradient controls the fate and function of CCR6−RORγt+ innate lymphoid cells. Nature. 2013;494(7436):261–265. doi:10.1038/nature11813.
   PubMed Web of Science ®Google Scholar
• Vonarbourg C, Mortha A, Bui VL, Hernandez PP, Kiss EA, Hoyler T, Flach M, Bengsch B, Thimme R, Hölscher C, et al. Regulated expression of nuclear receptor RORγt confers distinct functional fates to NK cell receptor-expressing RORγt+ innate lymphocytes. Immunity. 2010;33(5):736–751. doi:10.1016/j.immuni.2010.10.017.
   PubMed Web of Science ®Google Scholar
• Rankin LC, Groom JR, Chopin M, Herold MJ, Walker JA, Mielke LA, McKenzie ANJ, Carotta S, Nutt SL, Belz GT. The transcription factor T-bet is essential for the development of NKp46+ innate lymphocytes via the notch pathway. Nat Immunol. 2013;14(4):389–395. doi:10.1038/ni.2545.
   PubMed Web of Science ®Google Scholar
• Victorino F, Bigley TM, Park E, Yao C-H, Benoit J, Yang L-P, Piersma SJ, Lauron EJ, Davidson RM, Patti GJ, et al. HIF1α is required for NK cell metabolic adaptation during virus infection. Elife. 2021;10:10. doi:10.7554/eLife.68484.
   Web of Science ®Google Scholar
• Sécca C, Bando JK, Fachi JL, Gilfillan S, Peng V, Di Luccia B, Cella M, McDonald KG, Newberry RD, Colonna M. Spatial distribution of LTi-like cells in intestinal mucosa regulates type 3 innate immunity. Proc Natl Acad Sci USA. 2021;118(23):118. doi:10.1073/pnas.2101668118.
   Web of Science ®Google Scholar
• McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med. 1989;320(4):204–210. doi:10.1056/NEJM198901263200402.
   PubMed Web of Science ®Google Scholar
• Best EL, Freeman J, Wilcox MH. Models for the study of Clostridium difficile infection. Gut Microbes. 2012;3(2):145–167. doi:10.4161/gmic.19526.
   PubMed Web of Science ®Google Scholar
• Sorg JA, Sonenshein AL. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol. 2008;190(7):2505–2512. doi:10.1128/JB.01765-07.
   PubMed Web of Science ®Google Scholar
• Paredes-Sabja D, Shen A, Sorg JA. Clostridium difficile spore biology: sporulation, germination, and spore structural proteins. Trends Microbiol. 2014;22(7):406–416. doi:10.1016/j.tim.2014.04.003.
   PubMed Web of Science ®Google Scholar
• Leshem A, Liwinski T, Elinav E. Immune-microbiota interplay and colonization resistance in infection. Mol Cell. 2020;78(4):597–613. doi:10.1016/j.molcel.2020.03.001.
   PubMed Web of Science ®Google Scholar
• Winston JA, Theriot CM. Impact of microbial derived secondary bile acids on colonization resistance against Clostridium difficile in the gastrointestinal tract. Anaerobe. 2016;41:44–50. doi:10.1016/j.anaerobe.2016.05.003.
   PubMed Web of Science ®Google Scholar
• McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, Dubberke ER, Garey KW, Gould CV, Kelly C, et al. Clinical practice guidelines for clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66(7):e1–48. doi:10.1093/cid/cix1085.
   PubMed Web of Science ®Google Scholar
• Muroya D, Nadayoshi S, Yamada K, Kai Y, Masuda N, Nishida T, Shimokobe M, Hisaka T. Effects of hyperbaric oxygen therapy for clostridioides difficile-associated colitis: a retrospective study. J Anus Rectum Colon. 2023;7:264–272. doi:10.23922/jarc.2023-033.
   PubMed Web of Science ®Google Scholar
• Blanco YC, Farias AS, Goelnitz U, Lopes SCP, Arrais-Silva WW, Carvalho BO, Amino R, Wunderlich G, Santos LMB, Giorgio S, et al. Hyperbaric oxygen prevents early death caused by experimental cerebral malaria. PLoS ONE. 2008;3(9):e3126. doi:10.1371/journal.pone.0003126.
   PubMed Web of Science ®Google Scholar
• Bastos MF, Kayano AV, Silva‐Filho JL, Dos‐Santos JCK, Judice C, Blanco YC, Shryock N, Sercundes MK, Ortolan LS, Francelin C, et al. Inhibition of hypoxia‐associated response and kynurenine production in response to hyperbaric oxygen as mechanisms involved in protection against experimental cerebral malaria. FASEB J. 2018;32(8):4470–4481. doi:10.1096/fj.201700844R.
   PubMed Web of Science ®Google Scholar
• Fellows R, Denizot J, Stellato C, Cuomo A, Jain P, Stoyanova E, Balázsi S, Hajnády Z, Liebert A, Kazakevych J, et al. Microbiota derived short chain fatty acids promote histone crotonylation in the colon through histone deacetylases. Nat Commun. 2018;9(1):105. doi:10.1038/s41467-017-02651-5.
   PubMed Web of Science ®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
• Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi:10.1038/s41587-019-0209-9.
   PubMed Web of Science ®Google Scholar
• Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome. 2018;6:90. doi:10.1186/s40168-018-0470-z.
   PubMed Web of Science ®Google Scholar
• Robeson MS, O’Rourke DR, Kaehler BD, Ziemski M, Dillon MR, Foster JT, Bokulich NA, Pertea M. RESCRIPt: Reproducible sequence taxonomy reference database management. PLoS Comput Biol. 2021;17(11):e1009581. doi:10.1371/journal.pcbi.1009581.
   PubMed Web of Science ®Google Scholar
• Cao Y, Dong Q, Wang D, Zhang P, Liu Y, Niu C, Marschall T. microbiomeMarker: an R/Bioconductor package for microbiome marker identification and visualization. Bioinformatics. 2022;38(16):4027–4029. doi:10.1093/bioinformatics/btac438.
   PubMed Web of Science ®Google Scholar
• Fernandes AD, Reid JN, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB. Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome. 2014;2(1):15. doi:10.1186/2049-2618-2-15.
   PubMedGoogle Scholar
• Douglas GM, Maffei VJ, Zaneveld JR, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MGI. PICRUSt2 for prediction of metagenome functions. Nat Biotechnol. 2020;38(6):685–688. doi:10.1038/s41587-020-0548-6.
   PubMed Web of Science ®Google Scholar
• Yang C, Mai J, Cao X, Burberry A, Cominelli F, Zhang L, Elofsson A. ggpicrust2: an R package for PICRUSt2 predicted functional profile analysis and visualization. Bioinformatics. 2023;39(8):39. doi:10.1093/bioinformatics/btad470.
   Web of Science ®Google Scholar
• Molloy MJ, Grainger JR, Bouladoux N, Hand TW, Koo LY, Naik S, Quinones M, Dzutsev AK, Gao J-L, Trinchieri G, et al. Intraluminal containment of commensal outgrowth in the gut during Infection-Induced Dysbiosis. Cell Host & Microbe. 2013;14(3):318–328. doi:10.1016/j.chom.2013.08.003.
   PubMed Web of Science ®Google Scholar
• Allan DS, Kirkham CL, Aguilar OA, Qu LC, Chen P, Fine JH, Serra P, Awong G, Gommerman JL, Zúñiga-Pflücker JC, et al. An in vitro model of innate lymphoid cell function and differentiation. Mucosal Immunol. 2015;8(2):340–351. doi:10.1038/mi.2014.71.
   PubMed Web of Science ®Google Scholar