Microbiota, not host origin drives ex vivo intestinal epithelial responses

References

• The human microbiota in health and diseaseGeremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev. 2014;13(1):3–20. doi:10.1016/j.autrev.2013.06.004.
   PubMed Web of Science ®Google Scholar
• Baohong W, Mingfei Y, Longxian L, Zongxin L, Lanjuan L. The human microbiota in health and disease. Engineering. Elsevier ;2017. Vol. 3, pp. 71–82.
   Google Scholar
• Halfvarson J, Brislawn CJ, Lamendella R, Vázquez-Baeza Y, Walters WA, Bramer LM, D’Amato M, Bonfiglio F, McDonald D. Gonzalez A and others. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol. 2017;2:17004. doi:10.1038/nmicrobiol.2017.4.
   PubMed Web of Science ®Google Scholar
• Hudcovic T, Stĕpánková R, Cebra J, Tlaskalová-Hogenová H. The role of microflora in the development of intestinal inflammation: acute and chronic colitis induced by dextran sulfate in germ-free and conventionally reared immunocompetent and immunodeficient mice. Folia Microbiol (Praha). 2001;46(6):565–572. doi:10.1007/BF02818004.
   PubMed Web of Science ®Google Scholar
• Zhou J, Zhou Z, Ji P, Ma M, Guo J, Jiang S. Effect of fecal microbiota transplantation on experimental colitis in mice. Exp Ther Med. 2019;17(4):2581–2586. doi:10.3892/etm.2019.7263.
   PubMed Web of Science ®Google Scholar
• D’Haens GR, Geboes K, Peeters M, Baert F, Penninckx F, Rutgeerts P. Early lesions of recurrent Crohn’s disease caused by infusion of intestinal contents in excluded ileum. Gastroenterology. 1998;114(2):262–267. doi:10.1016/S0016-5085(98)70476-7.
   PubMed Web of Science ®Google Scholar
• Rutgeerts P, Peeters M, Hiele M, Vantrappen G, Pennincx F, Aerts R, Kerremans R, Goboes G. Effect of faecal stream diversion on recurrence of Crohn’s disease in the neoterminal ileum. Lancet. 1991;338(8770):771–774. doi:10.1016/0140-6736(91)90663-A.
   PubMed Web of Science ®Google Scholar
• Kim D, Zeng MY, Núñez G. The interplay between host immune cells and gut microbiota in chronic inflammatory diseases. Exp Mol Med. 2017;49(5):e339. doi:10.1038/emm.2017.24.
   PubMed Web of Science ®Google Scholar
• Becker C, Neurath MF, Wirtz S. The intestinal microbiota in inflammatory bowel disease. ILAR J. 2015;56(2):192–204. doi:10.1093/ilar/ilv030.
   PubMed Web of Science ®Google Scholar
• Nagao-Kitamoto H, Kamada N. Host-microbial cross-talk in inflammatory bowel disease. Immune Netw. 2017;17(1):1–12. doi:10.4110/in.2017.17.1.1.
   PubMed Web of Science ®Google Scholar
• Van der Sluis M, De Koning BA, De Bruijn AC, Velcich A, Meijerink JP, Van Goudoever JB, Büller HA, Dekker J, Van Seuningen I, Renes IB. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006;131(1):117–129. doi:10.1053/j.gastro.2006.04.020.
   PubMed Web of Science ®Google Scholar
• Dotti I, Mora-Buch R, Ferrer-Picón E, Planell N, Jung P, Masamunt MC, Leal RF, Martín de Carpi J, Llach J, Ordás I. Alterations in the epithelial stem cell compartment could contribute to permanent changes in the mucosa of patients with ulcerative colitis. Gut. 2017;66(12):2069–2079. doi:10.1136/gutjnl-2016-312609.
   PubMed Web of Science ®Google Scholar
• Arnauts K, Verstockt B, Ramalho AS, Vermeire S, Verfaillie C, Ferrante M. Ex vivo mimicking of inflammation in organoids derived from patients with ulcerative colitis. Gastroenterology. 2020;159(4):1564–1567. doi:10.1053/j.gastro.2020.05.064.
   PubMed Web of Science ®Google Scholar
• Howell KJ, Kraiczy J, Nayak KM, Gasparetto M, Ross A, Lee C, Mak TN, Koo BK, Kumar N, Lawley T. DNA methylation and transcription patterns in intestinal epithelial cells from pediatric patients with inflammatory bowel diseases differentiate disease subtypes and associate with outcome. Gastroenterology. 2018;154(3):585–598. doi:10.1053/j.gastro.2017.10.007.
   PubMed Web of Science ®Google Scholar
• Kraiczy J, Nayak KM, Howell KJ, Ross A, Forbester J, Salvestrini C, Mustata R, Perkins S, Andersson-Rolf A, Leenen E. DNA methylation defines regional identity of human intestinal epithelial organoids and undergoes dynamic changes during development. Gut. 2019;68(1):49–61. doi:10.1136/gutjnl-2017-314817.
   PubMed Web of Science ®Google Scholar
• Nanki K, Fujii M, Shimokawa M, Matano M, Nishikori S, Date S, Takano A, Toshimitsu K, Ohta Y, Takahashi S. Somatic inflammatory gene mutations in human ulcerative colitis epithelium. Nature. 2020;577(7789):254–259. doi:10.1038/s41586-019-1844-5.
   PubMed Web of Science ®Google Scholar
• Sarrabayrouse G, Landolfi S, Pozuelo M, Willamil J, Varela E, Clark A, Campos D, Herrera C, Santiago A, Machiels K. Mucosal microbial load in Crohn’s disease: a potential predictor of response to faecal microbiota transplantation. EBioMedicine. 2020;51:102611. doi:10.1016/j.ebiom.2019.102611.
   PubMed Web of Science ®Google Scholar
• Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, Leong RWL, Connor S, Ng W, Paramsothy R. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389(10075):1218–1228. doi:10.1016/S0140-6736(17)30182-4.
   PubMed Web of Science ®Google Scholar
• Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149(1):102–109.e6. doi:10.1053/j.gastro.2015.04.001.
   PubMed Web of Science ®Google Scholar
• Costello SP, Hughes PA, Waters O, Bryant RV, Vincent AD, Blatchford P, Katsikeros R, Makanyanga J, Campaniello MA. Mavrangelos C and others. effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA. 2019;321(2):156–164. doi:10.1001/jama.2018.20046.
   PubMed Web of Science ®Google Scholar
• Poletti M, Arnauts K, Ferrante M, Korcsmaros T. Organoid-based models to study the role of host-microbiota interactions in IBD. J Crohns Colitis. 2021;15(7):1222–1235. doi:10.1093/ecco-jcc/jjaa257.
   PubMed Web of Science ®Google Scholar
• Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, Smalley D, McHargue JW, Hightower GA, Smith JT, Autieri SM. Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun. 2008;76(3):1143–1152. doi:10.1128/IAI.01386-07.
   PubMed Web of Science ®Google Scholar
• Conway T, Cohen PS. Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol Spectr. 2015;3(3). doi:10.1128/microbiolspec.MBP-0006-2014.
   PubMedGoogle Scholar
• Jalili-Firoozinezhad S, Gazzaniga FS, Calamari EL, Camacho DM, Fadel CW, Bein A, Swenor B, Nestor B, Cronce MJ. Tovaglieri A and others. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat Biomed Eng. 2019;3(7):520–531. doi:10.1038/s41551-019-0397-0.
   PubMed Web of Science ®Google Scholar
• Vieira-Silva S, Sabino J, Valles-Colomer M, Falony G, Kathagen G, Caenepeel C, Cleynen I, van der Merwe S, Vermeire S, Raes J. Quantitative microbiome profiling disentangles inflammation- and bile duct obstruction-associated microbiota alterations across PSC/IBD diagnoses. Nat Microbiol. 2019;4(11):1826–1831. doi:10.1038/s41564-019-0483-9.
   PubMed Web of Science ®Google Scholar
• VanDussen KL, Marinshaw JM, Shaikh N, Miyoshi H, Moon C, Tarr PI, Ciorba MA, Stappenbeck TS. Development of an enhanced human gastrointestinal epithelial culture system to facilitate patient-based assays. Gut. 2015;64(6):911–920. doi:10.1136/gutjnl-2013-306651.
   PubMed Web of Science ®Google Scholar
• Johansson ME, Gustafsson JK, Holmén-Larsson J, Jabbar KS, Xia L, Xu H, Ghishan FK, Carvalho FA, Gewirtz AT. Sjövall H and others. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut. 2014;63(2):281–291. doi:10.1136/gutjnl-2012-303207.
   PubMed Web of Science ®Google Scholar
• Sabzevary-Ghahfarokhi M, Shohan M, Shirzad H, Rahimian G, Bagheri N, Soltani A, Deris F, Ghatreh-Samani M, Razmara E. The expression analysis of Fra-1 gene and IL-11 protein in Iranian patients with ulcerative colitis. BMC Immunol. 2018;19(1):17. doi:10.1186/s12865-018-0257-9.
   PubMedGoogle Scholar
• Urosevic J, Nebreda AR, Gomis RR. MAPK signaling control of colon cancer metastasis. Cell Cycle. 2014;13(17):2641–2642. doi:10.4161/15384101.2014.946374.
   PubMed Web of Science ®Google Scholar
• Kaminska B. MAPK signalling pathways as molecular targets for anti-inflammatory therapy–from molecular mechanisms to therapeutic benefits. Biochim Biophys Acta. 2005;1754(1–2):253–262. doi:10.1016/j.bbapap.2005.08.017.
   PubMed Web of Science ®Google Scholar
• Coskun M, Olsen J, Seidelin JB, Nielsen OH. MAP kinases in inflammatory bowel disease. Clin Chim Acta. 2011;412(7–8):513–520. doi:10.1016/j.cca.2010.12.020.
   PubMed Web of Science ®Google Scholar
• Mitsuyama K, Suzuki A, Tomiyasu N, Tsuruta O, Kitazaki S, Takeda T, Satoh Y, Bennett BL, Toyonaga A, Sata M. Pro-inflammatory signaling by Jun-N-terminal kinase in inflammatory bowel disease. Int J Mol Med. 2006;17:449–455.
   PubMed Web of Science ®Google Scholar
• Yang L, Yan Y. Protein kinases are potential targets to treat inflammatory bowel disease. World J Gastrointest Pharmacol Ther. 2014;5(4):209–217. doi:10.4292/wjgpt.v5.i4.209.
   PubMedGoogle Scholar
• Salas A, Hernandez-Rocha C, Duijvestein M, Faubion W, McGovern D, Vermeire S, Vetrano S, Vande Casteele N. JAK-STAT pathway targeting for the treatment of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol. 2020;17(6):323–337. doi:10.1038/s41575-020-0273-0.
   PubMed Web of Science ®Google Scholar
• Gu L, Ge Z, Wang Y, Shen M, Zhao P. Activating transcription factor 3 promotes intestinal epithelial cell apoptosis in Crohn’s disease. Pathol Res Pract. 2018;214(6):862–870. doi:10.1016/j.prp.2018.04.013.
   PubMed Web of Science ®Google Scholar
• Xiao L, Rao JN, Cao S, Liu L, Chung HK, Zhang Y, Zhang J, Liu Y, Gorospe M, Wang JY. Long noncoding RNA SPRY4-IT1 regulates intestinal epithelial barrier function by modulating the expression levels of tight junction proteins. Mol Biol Cell. 2016;27(4):617–626. doi:10.1091/mbc.E15-10-0703.
   PubMed Web of Science ®Google Scholar
• Koch S, Nava P, Addis C, Kim W, Denning TL, Li L, Parkos CA, Nusrat A. The Wnt antagonist Dkk1 regulates intestinal epithelial homeostasis and wound repair. Gastroenterology. 2011;141(1):259–68, 268.e1–8. doi:10.1053/j.gastro.2011.03.043.
   Web of Science ®Google Scholar
• Schmidt J, Stoffels B, Moore BA, Chanthaphavong RS, Mazie AR, Buchholz BM, Bauer AJ. Proinflammatory role of leukocyte-derived Egr-1 in the development of murine postoperative ileus. Gastroenterology. 2008;135(3):926–36, 936.e1–2. doi:10.1053/j.gastro.2008.05.079.
   Web of Science ®Google Scholar
• Silverman ES, De Sanctis GT, Boyce J, Maclean JA, Jiao A, Green FH, Grasemann H, Faunce D, Fitzmaurice G, Shi GP. The transcription factor early growth-response factor 1 modulates tumor necrosis factor-alpha, immunoglobulin E, and airway responsiveness in mice. Am J Respir Crit Care Med. 2001;163(3 Pt 1):778–785. doi:10.1164/ajrccm.163.3.2003123.
   PubMed Web of Science ®Google Scholar
• McMahon SB, Monroe JG. The role of early growth response gene 1 (egr-1) in regulation of the immune response. J Leukoc Biol. 1996;60(2):159–166. doi:10.1002/jlb.60.2.159.
   PubMed Web of Science ®Google Scholar
• Wang B, Guo H, Yu H, Chen Y, Xu H, Zhao G. The role of the transcription factor EGR1 in cancer. Front Oncol. 2021;11:642547.
   PubMedGoogle Scholar
• Dong XY, Wu MX, Zhang HM, Lyu H, Qian JM, Yang H. Association between matrix Gla protein and ulcerative colitis according to DNA microarray data. Gastroenterol Rep. 2020;8(1):66–75. doi:10.1093/gastro/goz038.
   Google Scholar
• Macpherson AJ, Chester KA, Robson L, Bjarnason I, Malcolm AD, Peters TJ. Increased expression of c-myc proto-oncogene in biopsies of ulcerative colitis and Crohn’s colitis. Gut. 1992;33(5):651–656. doi:10.1136/gut.33.5.651.
   PubMed Web of Science ®Google Scholar
• Roy PK, Rashid F, Bragg J, Ibdah JA. Role of the JNK signal transduction pathway in inflammatory bowel disease. World J Gastroenterol. 2008;14(2):200–202. doi:10.3748/wjg.14.200.
   PubMed Web of Science ®Google Scholar
• Maaser C, Sturm A, Vavricka SR, Kucharzik T, Fiorino G, Annese V, Calabrese E, Baumgart DC, Bettenworth D, Borralho Nunes P. ECCO-ESGAR guideline for diagnostic assessment in IBD Part 1: initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis. 2019;13(2):144–164. doi:10.1093/ecco-jcc/jjy113.
   PubMed Web of Science ®Google Scholar
• Vermeire S, Joossens M, Verbeke K, Wang J, Machiels K, Sabino J, Ferrante M, Van Assche G, Rutgeerts P, Raes J. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohns Colitis. 2016;10(4):387–394. doi:10.1093/ecco-jcc/jjv203.
   PubMed Web of Science ®Google Scholar
• Vandeputte D, Kathagen G, D’hoe K, Vieira-Silva S, Valles-Colomer M, Sabino J, Wang J, Tito RY, De Commer L, Darzi Y. Quantitative microbiome profiling links gut community variation to microbial load. Nature. 2017;551(7681):507–511. doi:10.1038/nature24460.
   PubMed Web of Science ®Google Scholar
• Vancamelbeke M, Laeremans T, Vanhove W, Arnauts K, Ramalho AS, Farré R, Cleynen I, Ferrante M, Vermeire S. Butyrate does not protect against inflammation-induced loss of epithelial barrier function and cytokine production in primary cell monolayers from patients with ulcerative colitis. J Crohns Colitis. 2019;13(10):1351–1361. doi:10.1093/ecco-jcc/jjz064.
   PubMed Web of Science ®Google Scholar
• Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F, Aken BL, Barrell D, Zadissa A, Searle S. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 2012;22(9):1760–1774. doi:10.1101/gr.135350.111.
   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
• Krämer A, Green J, Pollard J, Tugendreich S. Causal analysis approaches in ingenuity pathway analysis. Bioinformatics. 2014;30(4):523–530. doi:10.1093/bioinformatics/btt703.
   PubMed Web of Science ®Google Scholar
• Yu G, Wang LG, Han Y, He QY. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012;16(5):284–287. doi:10.1089/omi.2011.0118.
   PubMed Web of Science ®Google Scholar
• Yu G, He QY. ReactomePA: an R/Bioconductor package for reactome pathway analysis and visualization. Mol Biosyst. 2016;12(2):477–479. doi:10.1039/C5MB00663E.
   PubMedGoogle Scholar