Dysregulation of CD177⁺ neutrophils on intraepithelial lymphocytes exacerbates gut inflammation via decreasing microbiota-derived DMF

References

• Papayannopoulos V. Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol. 2018;18(2):134–17. doi:10.1038/nri.2017.105.
   PubMed Web of Science ®Google Scholar
• Honda M, Kubes P. Neutrophils and neutrophil extracellular traps in the liver and gastrointestinal system. Nat Rev Gastroenterol Hepatol. 2018;15(4):206–221. doi:10.1038/nrgastro.2017.183.
   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 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. doi:10.1136/gutjnl-2016-313535.
   PubMed Web of Science ®Google Scholar
• Hoytema van Konijnenburg DP, Reis BS, Pedicord VA, Farache J, Victora GD, Mucida D. Intestinal epithelial and intraepithelial T cell crosstalk mediates a dynamic response to infection. Cell. 2017;171(4):783–794 e13. doi:10.1016/j.cell.2017.08.046.
   PubMed Web of Science ®Google Scholar
• Ismail AS, Behrendt CL, Hooper LV. Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury. J Immunol. 2009;182(5):3047–3054. doi:10.4049/jimmunol.0802705.
   PubMed Web of Science ®Google Scholar
• Ismail AS, Severson KM, Vaishnava S, Behrendt CL, Yu X, Benjamin JL, Ruhn KA, Hou B, DeFranco AL, Yarovinsky F, et al. Gammadelta intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface. Proc Natl Acad Sci U S A. 2011;108(21):8743–8748. doi:10.1073/pnas.1019574108.
   PubMed Web of Science ®Google Scholar
• Lu H, Lin J, Xu C, Sun M, Zuo K, Zhang X, Li M, Huang H, Li Z, Wu W, et al. Cyclosporine modulates neutrophil functions via the SIRT6-HIF-1α-glycolysis axis to alleviate severe ulcerative colitis. Clin Transl Med. 2021;11(2):e334. doi:10.1002/ctm2.334.
   PubMed Web of Science ®Google Scholar
• Catalan-Serra I, Sandvik AK, Bruland T, Andreu-Ballester JC. Gammadelta T Cells in Crohn’s Disease: a New Player in the Disease Pathogenesis? J Crohns Colitis. 2017;11(9):1135–1145. doi:10.1093/ecco-jcc/jjx039.
   PubMed Web of Science ®Google Scholar
• McDonald BD, Jabri B, Bendelac A. Diverse developmental pathways of intestinal intraepithelial lymphocytes. Nat Rev Immunol. 2018;18(8):514–525. doi:10.1038/s41577-018-0013-7.
   PubMed Web of Science ®Google Scholar
• Antia A, Alvarado D, Ding S, Ciorba MA. Adding fuel to the fire? A role of intraepithelial lymphocytes in enteric immune responses to SARS-CoV-2 infection. Gastroenterology. 2021;S0016-5085(21): 03814–2. doi:10.1053/j.gastro.2021.12.001.
   Google Scholar
• Liu L, Gong T, Tao W, Lin B, Li C, Zheng X, Zhu S, Jiang W, Zhou R. Commensal viruses maintain intestinal intraepithelial lymphocytes via noncanonical RIG-I signaling. Nat Immunol. 2019;20(12):1681–1691. doi:10.1038/s41590-019-0513-z.
   PubMed Web of Science ®Google Scholar
• Lu H, Zhang C, Wu W, Chen H, Lin R, Sun R, Gao X, Li G, He Q, Gao H, et al. MCPIP1 restrains mucosal inflammation by orchestrating the intestinal monocyte to macrophage maturation via an ATF3-AP1S2 axis. Gut. 2022 Sep 8; online. doi:10.1136/gutjnl-2022-327183.
   Web of Science ®Google Scholar
• Li G, Lin J, Zhang C, Gao H, Lu H, Gao X, Zhu R, Li Z, Li M, Liu Z. Microbiota metabolite butyrate constrains neutrophil functions and ameliorates mucosal inflammation in inflammatory bowel disease. Gut Microbes. 2021;13(1):1968257. doi:10.1080/19490976.2021.1968257.
   PubMed Web of Science ®Google Scholar
• He Q, Gao H, Chang YL, Wu X, Lin R, Li G, Lin J, Lu H, Chen H, Li Z, et al. ETS-1 facilitates Th1 cell-mediated mucosal inflammation in inflammatory bowel disease through upregulating CIRBP. J Autoimmun. 2022;132:102872. doi:10.1016/j.jaut.2022.102872.
   PubMed Web of Science ®Google Scholar
• Finisguerra V, Di Conza G, Di Matteo M, Serneels J, Costa S, Thompson AA, Wauters E, Walmsley S, Prenen H, Granot Z, et al. MET is required for the recruitment of anti-tumoural neutrophils. Nature. 2015;522(7556):349–353. doi:10.1038/nature14407.
   PubMed Web of Science ®Google Scholar
• Wang X, Ota N, Manzanillo P, Kates L, Zavala-Solorio J, Eidenschenk C, Zhang J, Lesch J, Lee WP, Ross J, et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature. 2014;514(7521):237–241. doi:10.1038/nature13564.
   PubMed Web of Science ®Google Scholar
• Diehl G, Longman RS, Zhang JX, Breart B, Galan C, Cuesta A, Schwab SR, Littman DR. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature. 2013;494(7435):116–120. doi:10.1038/nature11809.
   PubMed Web of Science ®Google Scholar
• Birey F, Andersen J, Makinson CD, Islam S, Wei W, Huber N, Fan HC, Metzler KRC, Panagiotakos G, Thom N, et al. Assembly of functionally integrated human forebrain spheroids. Nature. 2017;545(7562):54–59. doi:10.1038/nature22330.
   PubMedGoogle Scholar
• Di Marco Barros R, Roberts NA, Dart RJ, Vantourout P, Jandke A, Nussbaumer O, Deban L, Cipolat S, Hart R, Iannitto ML, et al. Epithelia use butyrophilin-like molecules to shape organ-specific gammadelta T cell compartments. Cell. 2016;167(1):203–18.e17. doi:10.1016/j.cell.2016.08.030.
   PubMed Web of Science ®Google Scholar
• Do JS, Kim S, Keslar K, Jang E, Huang E, Fairchild RL, Pizarro TT, Min B. γδ T cells coexpressing gut homing α4β7 and αE integrins define a novel subset promoting intestinal inflammation. J Immunol. 2017;198(2):908–915. doi:10.4049/jimmunol.1601060.
   PubMed Web of Science ®Google Scholar
• Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol. 2013;13(3):159–175. doi:10.1038/nri3399.
   PubMed Web of Science ®Google Scholar
• Chen H, Li H, Liu Z. Interplay of intestinal microbiota and mucosal immunity in inflammatory bowel disease: a relationship of frenemies. Ther Adv Gastroenterol. 2020;13:1–11. doi:10.1177/1756284820935188.
   Web of Science ®Google Scholar
• Ma L, Ni Y, Wang Z, Tu W, Ni L, Zhuge F, Zheng A, Hu L, Zhao Y, Zheng L, et al. Spermidine improves gut barrier integrity and gut microbiota function in diet-induced obese mice. Gut Microbes. 2020;12(1):1–19. doi:10.1080/19490976.2020.1832857.
   PubMed Web of Science ®Google Scholar
• Gülden E, Chao C, Tai N, Pearson JA, Peng J, Majewska-Szczepanik M, Zhou Z, Wong FS, Wen L. TRIF deficiency protects non-obese diabetic mice from type 1 diabetes by modulating the gut microbiota and dendritic cells. J Autoimmun. 2018;93:57–65. doi:10.1016/j.jaut.2018.06.003.
   PubMed Web of Science ®Google Scholar
• Seo B, Jeon K, Moon S, Lee K, Kim WK, Jeong H, Cha KH, Lim MY, Kang W, Kweon MN, et al. Roseburia spp. abundance associates with alcohol consumption in humans and its administration ameliorates alcoholic fatty liver in mice. Cell Host Microbe. 2020;27(1):25–40 e6. doi:10.1016/j.chom.2019.11.001.
   PubMed Web of Science ®Google Scholar
• Kasahara K, Krautkramer KA, Org E, Romano KA, Kerby RL, Vivas EI, Mehrabian M, Denu JM, Bäckhed F, J LA, et al. Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model. Nat Microbiol. 2018;3(12):1461–1471. doi:10.1038/s41564-018-0272-x.
   PubMed Web of Science ®Google Scholar
• Mirsepasi-Lauridsen HC, Vallance BA, Krogfelt KA, Petersen AM. Escherichia coli pathobionts associated with inflammatory bowel disease. Clin Microbiol Rev. 2019;32(2):e00060–18. doi:10.1128/CMR.00060-18.
   PubMed Web of Science ®Google Scholar
• Seishima J, Iida N, Kitamura K, Yutani M, Wang Z, Seki A, Yamashita T, Sakai Y, Honda M, Yamashita T, et al. Gut-derived Enterococcus faecium from ulcerative colitis patients promotes colitis in a genetically susceptible mouse host. Genome Biol. 2019;20(1):252. doi:10.1186/s13059-019-1879-9.
   PubMed Web of Science ®Google Scholar
• Steck N, Hoffmann M, Sava IG, Kim SC, Hahne H, Tonkonogy SL, Mair K, Krueger D, Pruteanu M, Shanahan F, et al. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology. 2011;141(3):959–971. doi:10.1053/j.gastro.2011.05.035.
   PubMed Web of Science ®Google Scholar
• Sookoian S, Salatino A, Castaño GO, Landa MS, Fijalkowky C, Garaycoechea M, Pirola CJ. Intrahepatic bacterial metataxonomic signature in non-alcoholic fatty liver disease. Gut. 2020;69(8):1483–1491. doi:10.1136/gutjnl-2019-318811.
   PubMed Web of Science ®Google Scholar
• Kornberg MD, Bhargava P, Kim PM, Putluri V, Snowman AM, Putluri N, Calabresi PA, Snyder SH. Dimethyl fumarate targets GAPDH and aerobic glycolysis to modulate immunity. Science. 2018;360(6387):449–453. doi:10.1126/science.aan4665.
   PubMed Web of Science ®Google Scholar
• Wu Q, Wang Q, Mao G, Dowling CA, Lundy SK, Mao-Draayer Y. Dimethyl fumarate selectively reduces memory T cells and shifts the balance between Th1/Th17 and Th2 in multiple sclerosis patients. J Immunol. 2017;198(8):3069–3080. doi:10.4049/jimmunol.1601532.
   PubMed Web of Science ®Google Scholar
• Casili G, Cordaro M, Impellizzeri D, Bruschetta G, Paterniti I, Cuzzocrea S, Esposito E. Dimethyl fumarate reduces inflammatory responses in experimental colitis. J Crohns Colitis. 2016;10(4):472–483. doi:10.1093/ecco-jcc/jjv231.
   PubMed Web of Science ®Google Scholar
• Humphries F, Shmuel-Galia L, Ketelut-Carneiro N, Li S, Wang B, Nemmara VV, Wilson R, Jiang Z, Khalighinejad F, Muneeruddin K, et al. Succination inactivates gasdermin D and blocks pyroptosis. Science. 2020;369(6511):1633–1637. doi:10.1126/science.abb9818.
   PubMed Web of Science ®Google Scholar
• Li CN, Wang X, Lei L, Liu MZ, Li RC, Sun SJ, Liu SN, Huan Y, Zhou T, Liu Q, et al. Berberine combined with stachyose induces better glycometabolism than berberine alone through modulating gut microbiota and fecal metabolomics in diabetic mice. Phytother Res. 2020;34(5):1166–1174. doi:10.1002/ptr.6588.
   PubMed Web of Science ®Google Scholar
• Park SE, Kwon SJ, Cho KM, Seo SH, Kim EJ, Unno T, Bok SH, Park DH, Son HS. Intervention with kimchi microbial community ameliorates obesity by regulating gut microbiota. J Microbiol. 2020;58(10):859–867. doi:10.1007/s12275-020-0266-2.
   PubMed Web of Science ®Google Scholar
• Dorn M, Andreesen J, Gottschalk G. Fermentation of fumarate and L-malate by Clostridium formicoaceticum. J Bacteriol. 1978;133(1):26–32. doi:10.1128/jb.133.1.26-32.1978.
   PubMed Web of Science ®Google Scholar
• Iannotti E, Kafkewitz D, Wolin M, Bryant MP. Glucose fermentation products in Ruminococcus albus grown in continuous culture with Vibrio succinogenes: changes caused by interspecies transfer of H 2. J Bacteriol. 1973;114(3):1231–1240. doi:10.1128/jb.114.3.1231-1240.1973.
   PubMed Web of Science ®Google Scholar
• Katz Sand I, Zhu Y, Ntranos A, Clemente JC, Cekanaviciute E, Brandstadter R, Crabtree-Hartman E, Singh S, Bencosme Y, Debelius J, et al. Disease-modifying therapies alter gut microbial composition in MS. Neurol Neuroimmunol Neuroinflamm. 2019;6(1):e517. doi:10.1212/nxi.0000000000000517.
   PubMed Web of Science ®Google Scholar
• Schleicher L, Trautmann A, Stegmann DP, Fritz G, Gätgens J, Bott M, Hein S, Simon J, Seifert J, Steuber J. A sodium-translocating module linking succinate production to formation of a membrane potential in Prevotella bryantii. Appl Environ Microbiol. 2021;87:e0121121. doi:10.1128/aem.01211-21.
   PubMed Web of Science ®Google Scholar
• Semenec L, Laloo AE, Schulz BL, Vergara IA, Bond PL, Franks AE. Deciphering the electric code of Geobacter sulfurreducens in cocultures with Pseudomonas aeruginosa via SWATH-MS proteomics. Bioelectrochemistry. 2018;119:150–160. doi:10.1016/j.bioelechem.2017.09.013.
   PubMed Web of Science ®Google Scholar
• Spiga L, Winter MG, Furtado de Carvalho T, Zhu W, Hughes ER, Gillis CC, Behrendt CL, Kim J, Chessa D, Andrews-Polymenis HL, et al. An oxidative central metabolism enables Salmonella to utilize microbiota-derived succinate. Cell Host Microbe. 2017;22(3):291–301.e6. doi:10.1016/j.chom.2017.07.018.
   PubMed Web of Science ®Google Scholar
• Valentini M, Storelli N, Lapouge K. Identification of C(4)-dicarboxylate transport systems in Pseudomonas aeruginosa PAO1. J Bacteriol. 2011;193(17):4307–4316. doi:10.1128/jb.05074-11.
   PubMed Web of Science ®Google Scholar
• Bulek K, Zhao J, Liao Y, Rana N, Corridoni D, Antanaviciute A, Chen X, Wang H, Qian W, Miller-Little WA, et al. Epithelial-derived gasdermin D mediates nonlytic IL-1β release during experimental colitis. J Clin Invest. 2020;130:4218–4234. doi:10.1172/jci138103.
   PubMed Web of Science ®Google Scholar
• Chen H, Wu X, Xu C, Lin J, Liu Z. Dichotomous roles of neutrophils in modulating pathogenic and repair processes of inflammatory bowel diseases. Precis Clin Med. 2021;4(4):246–257. doi:10.1093/pcmedi/pbab025.
   PubMedGoogle Scholar
• Semenkovich NP, Planer JD, Ahern PP, Griffin NW, Lin CY, Gordon JI. Impact of the gut microbiota on enhancer accessibility in gut intraepithelial lymphocytes. Proc Natl Acad Sci U S A. 2016;113(51):14805–14810. doi:10.1073/pnas.1617793113.
   PubMed Web of Science ®Google Scholar
• Diebold M, Meola M, Purushothaman S, Siewert LK, Pössnecker E, Roloff T, Lindberg RL, Kuhle J, Kappos L, Derfuss T, et al. Gut microbiota composition as a candidate risk factor for dimethyl fumarate-induced lymphopenia in multiple sclerosis. Gut Microbes. 2022;14(1):2147055. doi:10.1080/19490976.2022.2147055.
   PubMed Web of Science ®Google Scholar