Clostridioides difficile aggravates dextran sulfate solution (DSS)-induced colitis by shaping the gut microbiota and promoting neutrophil recruitment

References

• Schnizlein MK, Young VB. Capturing the environment of the Clostridioides difficile infection cycle. Nat Rev Gastroenterol Hepatol. 2022;19(8):508–23. doi:10.1038/s41575-022-00610-0. In eng.
   PubMed Web of Science ®Google Scholar
• Baumgartner M, Pfrunder-Cardozo KR, Hall AR. Microbial community composition interacts with local abiotic conditions to drive colonization resistance in human gut microbiome samples. Proc Biol Sci. 2021;288(1947):20203106. doi:10.1098/rspb.2020.3106. In eng.
   PubMed Web of Science ®Google Scholar
• Rodriguez C, Van Broeck J, Taminiau B, Delmée M, Daube G. Clostridium difficile infection: early history, diagnosis and molecular strain typing methods. Microb Pathog. 2016;97:59–78. doi:10.1016/j.micpath.2016.05.018. In eng.
   PubMed Web of Science ®Google Scholar
• Kucharzik T, Ellul P, Greuter T, Rahier JF, Verstockt B, Abreu C, Albuquerque A, Allocca M, Esteve M, Farraye FA, et al. ECCO guidelines on the prevention, diagnosis, and management of infections in inflammatory bowel disease. J Crohns Colitis. 2021;15(6):879–913. doi:10.1093/ecco-jcc/jjab052.
   PubMed Web of Science ®Google Scholar
• Ananthakrishnan AN. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol. 2011;8(1):17–26. doi:10.1038/nrgastro.2010.190. In eng.
   PubMed Web of Science ®Google Scholar
• Rao K, Higgins PD. Epidemiology, diagnosis, and management of clostridium difficile infection in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2016;22(7):1744–1754. doi:10.1097/mib.0000000000000793. In eng.
   PubMed Web of Science ®Google Scholar
• Singh H, Nugent Z, Yu BN, Lix LM, Targownik LE, Bernstein CN. Higher incidence of clostridium difficile infection among individuals with inflammatory bowel disease. Gastroenterology. 2017;153(2):430–438.e2. doi:10.1053/j.gastro.2017.04.044. In eng.
   PubMed Web of Science ®Google Scholar
• Balram B, Battat R, Al-Khoury A, D’aoust J, Afif W, Bitton A, Lakatos PL, Bessissow T. Risk factors associated with clostridium difficile infection in inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis. 2019;13(1):27–38. doi:10.1093/ecco-jcc/jjy143.
   PubMed Web of Science ®Google Scholar
• Abernathy-Close L, Barron MR, George JM, Dieterle MG, Vendrov KC, Bergin IL, Young VB. Intestinal inflammation and altered gut microbiota associated with Inflammatory bowel disease render mice susceptible to clostridioides difficile colonization and infection. mBio. 2021;12(3):e0273320. doi:10.1128/mBio.02733-20.
   PubMed Web of Science ®Google Scholar
• Saleh MM, Frisbee AL, Leslie JL, Buonomo EL, Cowardin CA, Ma JZ, Simpson ME, Scully KW, Abhyankar MM, Petri WA. Colitis-induced Th17 cells increase the risk for severe subsequent clostridium difficile infection. Cell Host Microbe. 2019;25(5):756–765 e5. doi:10.1016/j.chom.2019.03.003.
   PubMed Web of Science ®Google Scholar
• Neurath MF. Targeting immune cell circuits and trafficking in inflammatory bowel disease. Nat Immunol. 2019;20(8):970–979. doi:10.1038/s41590-019-0415-0.
   PubMed Web of Science ®Google Scholar
• Lavelle A, Sokol H. Gut microbiota-derived metabolites as key actors in inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2020;17(4):223–237. doi:10.1038/s41575-019-0258-z.
   PubMed Web of Science ®Google Scholar
• Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, Timmis KN, Schreiber S . Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53(5):685–693. In eng. doi:10.1136/gut.2003.025403.
   PubMed Web of Science ®Google Scholar
• Sokol H, Jegou S, McQuitty C, Straub M, Leducq V, Landman C, Kirchgesner J, Le Gall G, Bourrier A, Nion-Larmurier I. Specificities of the intestinal microbiota in patients with inflammatory bowel disease and Clostridium difficile infection. Gut Microbes. 2018;9(1):55–60. doi:10.1080/19490976.2017.1361092.
   PubMed Web of Science ®Google Scholar
• Uhlig HH, Powrie F. Translating immunology into therapeutic concepts for inflammatory bowel disease. Annu Rev Immunol. 2018;36:755–781. doi:10.1146/annurev-immunol-042617-053055. In eng.
   PubMed Web of Science ®Google Scholar
• Hayashi F, Means TK, Luster AD. Toll-like receptors stimulate human neutrophil function. Blood. 2003 In eng;102(7):2660–2669. doi:10.1182/blood-2003-04-1078.
   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. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013;504(7480):446–450. In eng. doi:10.1038/nature12721.
   PubMed Web of Science ®Google Scholar
• Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016 In eng;165(6):1332–1345. doi:10.1016/j.cell.2016.05.041.
   PubMed Web of Science ®Google Scholar
• Zhang D, Frenette PS. Cross talk between neutrophils and the microbiota. Blood. 2019 In eng;133(20):2168–2177. doi:10.1182/blood-2018-11-844555.
   PubMed Web of Science ®Google Scholar
• Kühl AA, Kakirman H, Janotta M, Dreher S, Cremer P, Pawlowski NN, Loddenkemper C, Heimesaat MM, Grollich K, Zeitz, M. Aggravation of different types of experimental colitis by depletion or adhesion blockade of neutrophils. Gastroenterology. 2007;133(6):1882–1892. In eng. doi:10.1053/j.gastro.2007.08.073.
   PubMed Web of Science ®Google Scholar
• Fournier BM, Parkos CA. The role of neutrophils during intestinal inflammation. Mucosal Immunol. 2012;5(4):354–366. doi:10.1038/mi.2012.24.
   PubMed Web of Science ®Google Scholar
• Zhou F, Hamza T, Fleur AS, Zhang Y, Yu H, Chen K, Heath JE, Chen Y, Huang H, Feng H. Mice with inflammatory bowel disease are susceptible to clostridium difficile infection with severe disease outcomes. Inflamm Bowel Dis. 2018;24(3):573–582. doi:10.1093/ibd/izx059.
   PubMed Web of Science ®Google Scholar
• Voth E, Solanky D, Loftus EV Jr., Pardi DS, Khanna S. Novel risk factors and outcomes in inflammatory bowel disease patients with Clostridioides difficile infection. Therap Adv Gastroenterol. 2021;14:1756284821997792. doi:10.1177/1756284821997792. In eng.
   Web of Science ®Google Scholar
• Yanai H, Nguyen GC, Yun L, Lebwohl O, Navaneethan U, Stone CD, Ghazi L, Moayyedi P, Brooks J, Bernstein CN, et al. Practice of gastroenterologists in treating flaring inflammatory bowel disease patients with clostridium difficile: antibiotics alone or combined antibiotics/immunomodulators? Inflamm Bowel Dis. 2011;17(7):1540–1546. doi:10.1002/ibd.21514.
   PubMed Web of Science ®Google Scholar
• Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007 In eng;448(7152):427–434. doi:10.1038/nature06005.
   PubMed Web of Science ®Google Scholar
• Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, De Angelis M. The controversial role of human gut lachnospiraceae. Microorganisms. 2020;8(4). doi:10.3390/microorganisms8040573.
   PubMed Web of Science ®Google Scholar
• Gu X, Sim JXY, Lee WL, Cui L, Chan YFZ, Chang ED, Teh YE, Zhang AN, Armas F, Chandra F. Gut Ruminococcaceae levels at baseline correlate with risk of antibiotic-associated diarrhea. iScience. 2022;25(1):103644. doi:10.1016/j.isci.2021.103644.
   PubMed Web of Science ®Google Scholar
• Lee YJ, Arguello ES, Jenq RR, Littmann E, Kim GJ, Miller LC, Ling L, Figueroa C, Robilotti E, Perales M-A, et al. Protective factors in the intestinal microbiome against clostridium difficile infection in recipients of allogeneic hematopoietic stem cell transplantation. J Infect Dis. 2017;215(7):1117–1123. In eng. doi:10.1093/infdis/jix011.
   PubMed Web of Science ®Google Scholar
• Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes. 2016 In eng;7(3):189–200. doi:10.1080/19490976.2015.1134082.
   PubMed Web of Science ®Google Scholar
• Vincent C, Miller MA, Edens TJ, Mehrotra S, Dewar K, Manges AR. Bloom and bust: intestinal microbiota dynamics in response to hospital exposures and Clostridium difficile colonization or infection. Microbiome. 2016;4:12. doi:10.1186/s40168-016-0156-3. In eng.
   PubMed Web of Science ®Google Scholar
• Wang D, Dong D, Wang C, Cui Y, Jiang C, Ni Q, Su T, Wang G, Mao E, Peng Y. Risk factors and intestinal microbiota: clostridioides difficile infection in patients receiving enteral nutrition at intensive care units. Crit Care. 2020;24(1):426. doi:10.1186/s13054-020-03119-7.
   PubMed Web of Science ®Google Scholar
• Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G. Environmental and gut bacteroidetes: the food connection. Front Microbiol. 2011;2:93. doi:10.3389/fmicb.2011.00093. In eng.
   PubMed Web of Science ®Google Scholar
• Zafar H, Saier MH Jr. Gut bacteroides species in health and disease. Gut Microbes. 2021;13(1):1–20. doi:10.1080/19490976.2020.1848158.
   PubMed Web of Science ®Google Scholar
• Brazil JC, Louis NA, Parkos CA. The role of polymorphonuclear leukocyte trafficking in the perpetuation of inflammation during inflammatory bowel disease. Inflamm Bowel Dis. 2013;19(7):1556–1565. doi:10.1097/MIB.0b013e318281f54e. In eng.
   PubMed Web of Science ®Google Scholar
• Magro F, Doherty G, Peyrin-Biroulet L, Svrcek M, Borralho P, Walsh A, Carneiro F, Rosini F, de Hertogh G, Biedermann L, et al. ECCO position paper: harmonization of the approach to ulcerative colitis histopathology. J Crohn's Colitis. 2020;14(11):1503–1511. In eng. doi:10.1093/ecco-jcc/jjaa110.
   Google Scholar
• Zhu F, He H, Fan L, Ma C, Xu Z, Xue Y, Wang Y, Zhang C, Zhou G. Blockade of CXCR2 suppresses proinflammatory activities of neutrophils in ulcerative colitis. Am J Transl Res. 2020;12(9):5237–5251. In eng.
   PubMed Web of Science ®Google Scholar
• Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV, Merlin D. Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One. 2009;4(6):e6073. In eng. doi:10.1371/journal.pone.0006073.
   PubMed Web of Science ®Google Scholar
• Zhou G, Yu L, Fang L, Yang W, Yu T, Miao Y, Chen M, Wu K, Chen F, Cong Y, et al. CD177 + neutrophils as functionally activated neutrophils negatively regulate IBD. Gut. 2018;67(6):1052–1063. In eng. doi:10.1136/gutjnl-2016-313535.
   PubMed Web of Science ®Google Scholar
• Pereira C, Grácio D, Teixeira JP, Magro F. Oxidative stress and DNA damage: implications in inflammatory bowel disease. Inflamm Bowel Dis. 2015;21(10):2403–2417. doi:10.1097/mib.0000000000000506. In eng.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11(8):519–531. doi:10.1038/nri3024. In eng.
   PubMed Web of Science ®Google Scholar
• Bersudsky M, Luski L, Fishman D, White RM, Ziv-Sokolovskaya N, Dotan S, Rider P, Kaplanov I, Aychek T, Dinarello CA. Non-redundant properties of IL-1α and IL-1β during acute colon inflammation in mice. Gut. 2014;63(4):598–609. In eng. doi:10.1136/gutjnl-2012-303329.
   PubMed Web of Science ®Google Scholar
• Shouval DS, Biswas A, Kang YH, Griffith AE, Konnikova L, Mascanfroni ID, Redhu NS, Frei SM, Field M, Doty AL. Interleukin 1β mediates intestinal inflammation in mice and patients with interleukin 10 receptor deficiency. Gastroenterology. 2016;151(6):1100–1104. In eng. doi:10.1053/j.gastro.2016.08.055.
   PubMed Web of Science ®Google Scholar
• Coccia M, Harrison OJ, Schiering C, Asquith MJ, Becher B, Powrie F, Maloy KJ. IL-1β mediates chronic intestinal inflammation by promoting the accumulation of IL-17A secreting innate lymphoid cells and CD4+ Th17 cells. J Exp Med. 2012 In eng;209(9):1595–1609. doi:10.1084/jem.20111453.
   PubMed Web of Science ®Google Scholar
• Ng J, Hirota SA, Gross O, Li Y, Ulke–Lemee A, Potentier MS, Schenck LP, Vilaysane A, Seamone ME, Feng H, et al. Clostridium difficile toxin–Induced inflammation and intestinal injury are mediated by the inflammasome. Gastroenterology. 2010;139(2):542–552. 552.e13In eng. doi:. 552.e13In eng. doi:10.1053/j.gastro.2010.04.005.
   PubMed Web of Science ®Google Scholar
• Coll RC, Hill JR, Day CJ, Zamoshnikova A, Boucher D, Massey NL, Chitty JL, Fraser JA, Jennings MP, Robertson AAB, et al. MCC950 directly targets the NLRP3 ATP-hydrolysis motif for inflammasome inhibition. Nat Chem Biol. 2019;15(6):556–559. In eng. doi:10.1038/s41589-019-0277-7.
   PubMed Web of Science ®Google Scholar
• Perera AP, Fernando R, Shinde T, Gundamaraju R, Southam B, Sohal SS, Robertson AAB, Schroder K, Kunde D, Eri R. MCC950, a specific small molecule inhibitor of NLRP3 inflammasome attenuates colonic inflammation in spontaneous colitis mice. Sci Rep. 2018 In eng;8(1):8618. doi:10.1038/s41598-018-26775-w.
   PubMed Web of Science ®Google Scholar
• Fenton MJ. Review: transcriptional and post-transcriptional regulation of interleukin 1 gene expression. Int J Immunopharmacol. 1992;14(3):401–411. doi:10.1016/0192-0561(92)90170-p. In eng.
   PubMed Web of Science ®Google Scholar
• Liu YH, Chang YC, Chen LK, Su P-A, Ko W-C, Tsai Y-S, Chen Y-H, Lai H-C, Wu C-Y, Hung Y-P, et al. The ATP-P2X(7) signaling axis is an essential sentinel for intracellular clostridium difficile pathogen-induced inflammasome activation. Front Cell Infect Microbiol. 2018;8:84. In eng. doi:10.3389/fcimb.2018.00084.
   PubMed Web of Science ®Google Scholar
• Xu H, Yang J, Gao W, Li L, Li P, Zhang L, Gong YN, Peng X, Xi JJ, Chen S. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature. 2014;513(7517):237–241. In eng. doi:10.1038/nature13449.
   PubMed Web of Science ®Google Scholar
• Yoshimura T, Matsushima K, Oppenheim JJ, Leonard EJ. Neutrophil chemotactic factor produced by lipopolysaccharide (LPS)-stimulated human blood mononuclear leukocytes: partial characterization and separation from interleukin 1 (IL 1). J Immunol. 1987 In eng;139(3):788–793. doi:10.4049/jimmunol.139.3.788.
   PubMed Web of Science ®Google Scholar
• Pyrillou K, Burzynski LC, Clarke MCH. Alternative pathways of IL-1 activation, and its role in health and disease. Front Immunol. 2020;11:613170. doi:10.3389/fimmu.2020.613170.
   PubMed Web of Science ®Google Scholar
• Pavlidis P, Tsakmaki A, Pantazi E, Li K, Cozzetto D, Digby- Bell J, Yang F, Lo JW, Alberts E, Sa ACC, et al. Interleukin-22 regulates neutrophil recruitment in ulcerative colitis and is associated with resistance to ustekinumab therapy. Nat Commun. 2022;13(1):5820. doi:10.1038/s41467-022-33331-8.
   PubMed Web of Science ®Google Scholar
• Dong D, Zhang L, Chen X, Jiang C, Yu B, Wang X, Peng Y. Antimicrobial susceptibility and resistance mechanisms of clinical Clostridium difficile from a Chinese tertiary hospital. Int J Antimicrob Agents. 2013;41(1):80–84. doi:10.1016/j.ijantimicag.2012.08.011.
   PubMed Web of Science ®Google Scholar
• Taghipour N, Molaei M, Mosaffa N, Rostami-Nejad M, Asadzadeh Aghdaei H, Anissian A, Azimzadeh P, Zali MR. An experimental model of colitis induced by dextran sulfate sodium from acute progresses to chronicity in C57BL/6: correlation between conditions of mice and the environment. Gastroenterol Hepatol Bed Bench. 2016;9(1):45–52. In eng.
   PubMedGoogle Scholar
• Fischer AH, Jacobson KA, Rose J, Zeller R. Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc. 2008;2008:db.prot4986. doi:10.1101/pdb.prot4986. In eng.
   Google Scholar
• Dieleman LA, Palmen MJ, Akol H, Bloemena E, Peña AS, Meuwissen SGM, Van Rees EP. Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin Exp Immunol. 1998 In eng;114(3):385–391. doi:10.1046/j.1365-2249.1998.00728.x.
   PubMed Web of Science ®Google Scholar
• Rc E. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–998. doi:10.1038/nmeth.2604. In eng.
   PubMed Web of Science ®Google Scholar
• Wu J, Wei Z, Cheng P, Qian C, Xu F, Yang Y, Wang A, Chen W, Sun Z, Lu Y. Rhein modulates host purine metabolism in intestine through gut microbiota and ameliorates experimental colitis. Theranostics. 2020;10(23):10665–10679. In eng. doi:10.7150/thno.43528.
   PubMed Web of Science ®Google Scholar
• Swamydas M, Luo Y, Dorf ME, Lionakis MS. Isolation of mouse neutrophils. Curr Protoc Immunol. 2015;110(3):20 1–3 20 15. doi:10.1002/0471142735.im0320s110.
   Google Scholar