4,762
Views
77
CrossRef citations to date
0
Altmetric
Research Paper

Butyrate mediates anti-inflammatory effects of Faecalibacterium prausnitzii in intestinal epithelial cells through Dact3

, , , , ORCID Icon, ORCID Icon, , & ORCID Icon show all
Article: 1826748 | Received 18 May 2020, Accepted 09 Sep 2020, Published online: 15 Oct 2020

References

  • Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature. 2011;474:307–317.
  • Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med. 2009;361:2066–2078. doi:10.1056/NEJMra0804647.
  • Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Doré J, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15(8):1183–1189. doi:10.1002/ibd.20903.
  • Miquel S, Martin R, Bridonneau C, Robert V, Sokol H, Bermudez-Humaran LG, Thomas M, Langella P. Ecology and metabolism of the beneficial intestinal commensal bacterium Faecalibacterium prausnitzii. Gut Microbes. 2014;5(2):146–151. doi:10.4161/gmic.27651.
  • Miquel S, Martin R, Rossi O, Bermudez-Humaran LG, Chatel JM, Sokol H, Thomas M, Wells JM, Langella P. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013;16(3):255–261. doi:10.1016/j.mib.2013.06.003.
  • Martin R, Miquel S, Ulmer J, Kechaou N, Langella P, Bermudez-Humaran LG. Role of commensal and probiotic bacteria in human health: a focus on inflammatory bowel disease. Microb Cell Fact. 2013;12:71. doi:10.1186/1475-2859-12-71.
  • Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran 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 U S A. 2008;105(43):16731–16736. doi:10.1073/pnas.0804812105.
  • Martin R, Chain F, Miquel S, Lu J, Gratadoux -J-J, Sokol H, Verdu EF, Bercik P, Bermúdez-Humarán LG, Langella P, et al. The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm Bowel Dis. 2014;20(3):417–430. doi:10.1097/01.MIB.0000440815.76627.64.
  • Martin R, Miquel S, Chain F, Natividad JM, Jury J, Lu J, Sokol H, Theodorou V, Bercik P, Verdu EF, et al. Faecalibacterium prausnitzii prevents physiological damages in a chronic low-grade inflammation murine model. BMC Microbiol. 2015;15(1):67. doi:10.1186/s12866-015-0400-1.
  • Martin R, Bermudez-Humaran LG, Langella P. Searching for the bacterial effector: the example of the multi-skilled commensal bacterium faecal bacterium prausnitzii. Front Microbiol. 2018;9:346. doi:10.3389/fmicb.2018.00346.
  • Leonel AJ, Alvarez-Leite JI. Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care. 2012;15(5):474–479. doi:10.1097/MCO.0b013e32835665fa.
  • Miquel S, Leclerc M, Martin R, Chain F, Lenoir M, Raguideau S, Hudault S, Bridonneau C, Northen T, Bowen B, et al. Identification of metabolic signatures linked to anti-inflammatory effects of Faecalibacterium prausnitzii. MBio. 2015;6(2). doi:10.1128/mBio.00300-15.
  • Quevrain E, Maubert MA, Michon C, Chain F, Marquant R, Tailhades J, Miquel S, Carlier L, Bermúdez-Humarán LG, Pigneur B, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2016 Mar;65(3):415-425. doi:10.1136/gutjnl-2014-307649.
  • Fisher DA, Kivimae S, Hoshino J, Suriben R, Martin P-M, Baxter N, Cheyette BNR. Three Dact gene family members are expressed during embryonic development and in the adult brains of mice. Developmental Dynamics. 2006;235(9):2620–2630. doi:10.1002/dvdy.20917.
  • Kim H, Jung BJ, Jung JH, Kim JY, Chung SK, Chung DK. Lactobacillus plantarum lipoteichoic acid alleviates TNF-alpha-induced inflammation in the HT-29 intestinal epithelial cell line. Mol Cells. 2012;33:479–486. doi:10.1007/s10059-012-2266-5.
  • Kechaou N, Chain F, Gratadoux -J-J, Blugeon S, Bertho N, Chevalier C, Le Goffic R, Courau S, Molimard P, Chatel JM, et al. Identification of one novel candidate probiotic Lactobacillus plantarum strain active against influenza virus infection in mice by a large-scale screening. Appl Environ Microbiol. 2013;79:1491–1499. doi:10.1128/AEM.03075-12.
  • Eckmann L, Jung HC, Schurer-Maly C, Panja A, Morzycka-Wroblewska E, Kagnoff MF. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology. 1993;105:1689–1697. doi:10.1016/0016-5085(93)91064-O.
  • Gross V, Andus T, Daig R, Aschenbrenner E, Scholmerich J, Falk W. Regulation of interleukin-8 production in a human colon epithelial cell line (HT-29). Gastroenterology. 1995;108:653–661. doi:10.1016/0016-5085(95)90436-0.
  • Andoh A, Fujiyama Y, Sumiyoshi K, Sakumoto H, Okabe H, Bamba T. Tumour necrosis factor-alpha up-regulates decay-accelerating factor gene expression in human intestinal epithelial cells. Immunology. 1997;90:358–363. doi:10.1111/j.1365-2567.1997.00358.x.
  • van Rijn SJ, Riemers FM, van den Heuvel D, Wolfswinkel J, Hofland L, Meij BP, Penning LC. Expression stability of reference genes for quantitative RT-PCR of healthy and diseased pituitary tissue samples varies between humans, mice, and dogs. Mol Neurobiol. 2014;49:893–899.
  • Jiang X, Tan J, Li JS, Kivimaee S, Yang XJ, Zhuang L, Lee PL, Chan MTW, Stanton LW, Liu ET, et al. DACT3 is an epigenetic regulator of Wnt/beta-catenin signaling in colorectal cancer and is a therapeutic target of histone modifications. Cancer Cell. 2008;13:529–541. doi:10.1016/j.ccr.2008.04.019.
  • Duncan SH, Barcenilla A, Stewart CS, Pryde SE, Flint HJ. Acetate utilization and butyryl coenzyme A (CoA): acetate-CoA-transferase in butyrate-producing bacteria from the human large intestine. Appl Environ Microbiol. 2002;68:5186–5190. doi:10.1128/AEM.68.10.5186-5190.2002.
  • Urdaci MC, Sanchez B. Some immunomodulatory effects of probiotic bacteria might be due to porcine neutrophil elastase inhibitor, a serpin present in MRS broth. Immunol Lett. 2009;122:99–100. doi:10.1016/j.imlet.2008.11.004.
  • Hoffmann TW, Pham H-P, Bridonneau C, Aubry C, Lamas B, Martin-Gallausiaux C, Moroldo M, Rainteau D, Lapaque N, Six A, et al. Microorganisms linked to inflammatory bowel disease-associated dysbiosis differentially impact host physiology in gnotobiotic mice. Isme J. 2016;10(2):460–477. doi:10.1038/ismej.2015.127.
  • Laval L, Martin R, Natividad JN, Chain F, Miquel S, Desclee de Maredsous C, Capronnier S, Sokol H, Verdu EF, van Hylckama Vlieg J, et al. Lactobacillus rhamnosus CNCM I-3690 and the commensal bacterium Faecalibacterium prausnitzii A2-165 exhibit similar protective effects to induced barrier hyper-permeability in mice. Gut Microbes. 2015;6:1–9. doi:10.4161/19490976.2014.990784.
  • Duncan SH, Hold GL, Harmsen HJM, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;52:2141–2146.
  • Mandal A, Waxman J. Retinoic acid negatively regulates dact3b expression in the hindbrain of zebrafish embryos. Gene Expression Patterns. 2014;16:122–129. doi:10.1016/j.gep.2014.09.003.
  • Xue H, Xiao ZC, Zhang J, Wen J, Wang Y, Chang Z, Zhao J, Gao X, Du J, Chen Y-G, et al. Disruption of the Dapper3 gene aggravates ureteral obstruction-mediated renal fibrosis by amplifying Wnt/beta-catenin signaling. J Biol Chem. 2013;288:15006–15014. doi:10.1074/jbc.M113.458448.
  • Beltran AS, Russo A, Lara H, Fan C, Lizardi PM, Blancafort P. Suppression of breast tumor growth and metastasis by an engineered transcription factor. PLoS One. 2011;6(9):e24595. doi:10.1371/journal.pone.0024595.
  • Li H, Bitler BG, Vathipadiekal V, Maradeo ME, Slifker M, Creasy CL, Tummino PJ, Cairns P, Birrer MJ, Zhang R, et al. ALDH1A1 is a novel EZH2 target gene in epithelial ovarian cancer identified by genome-wide approaches. Cancer Prev Res. 2012;5(3):484–491. doi:10.1158/1940-6207.CAPR-11-0414.
  • Xi SC, Yang MC, Tao YG, Xu H, Shan JG, Inchauste S, Zhang M, Mercedes L, Hong JA, Rao M, et al. Cigarette smoke induces C/EBP-beta-mediated activation of miR-31 in normal human respiratory epithelia and lung cancer cells. PLoS One. 2010;5(10):e13764. doi:10.1371/journal.pone.0013764.
  • Neta G, Brenner AV, Sturgis EM, Pfeiffer RM, Hutchinson AA, Aschebrook-Kilfoy B, Yeager M, Xu L, Wheeler W, Abend M, et al. Common genetic variants related to genomic integrity and risk of papillary thyroid cancer. Carcinogenesis. 2011;32(8):1231–1237. doi:10.1093/carcin/bgr100.
  • Fung KYC, Kerr C, Henderson S, Ilka P, Shaw J, Buckley MJ, Lockett T, Head R, Cosgrove L. Mechanisms associated with acquisition of resistance to butyrate-induced apoptosis in colorectal cancer cells using gene expression analysis. J Proteomics Genomics Res. 2014;1:16–30. doi:10.14302/.2326-0793.jpgr-14-598.
  • Bocker U, Nebe T, Herweck F, Holt L, Panja A, Jobin C, Rossol S, Sartor R, Singer MV. Butyrate modulates intestinal epithelial cell-mediated neutrophil migration. Clin Exp Immunol. 2003;131(1):53–60. doi:10.1046/j.1365-2249.2003.02056.x.
  • Lakhdari O, Tap J, Beguet-Crespel F, Le Roux K, de Wouters T, Cultrone A, Nepelska M, Lefèvre F, Doré J, Blottière HM, et al. Identification of NF-kappaB modulation capabilities within human intestinal commensal bacteria. J Biomed Biotechnol. 2011;2011:282356. doi:10.1155/2011/282356.
  • Yin L, Laevsky G, Giardina C. Butyrate suppression of colonocyte NF-kappa B activation and cellular proteasome activity. J Biol Chem. 2001;276:44641–44646.
  • Cuiv PO, Smith WJ, Pottenger S, Burman S, Shanahan ER, Morrison M. Isolation of genetically tractable most-wanted bacteria by metaparental mating. Sci Rep. 2015;5:13282. doi:10.1038/srep13282.
  • Cheyette BNR, Waxman JS, Miller JR, Takemaru KI, Sheldahl LC, Khlebtsova N, Fox EP, Earnest T, Moon RT. Dapper, a dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. Developmental Cell. 2002;2:449–461. doi:10.1016/S1534-5807(02)00140-5.
  • Amar J, Chabo C, Waget A, Klopp P, Vachoux C, Bermudez-Humaran LG, Smirnova N, Bergé M, Sulpice T, Lahtinen S, et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med. 2011;3:559–572. doi:10.1002/emmm.201100159.
  • Benbouziane B, Ribelles P, Aubry C, Martin R, Kharrat P, Riazi A, Langella P, Bermúdez-Humarán LG. Development of a stress-inducible controlled expression (SICE) system in Lactococcus lactis for the production and delivery of therapeutic molecules at mucosal surfaces. J Biotechnol. 2013;168(2):120–129. doi:10.1016/j.jbiotec.2013.04.019.
  • Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34:374+.
  • Matouskova P, Bartikova H, Bousova I, Hanusova V, Szotakova B, Skalova L, Hribal ML. Reference genes for real-time PCR quantification of messenger RNAs and MicroRNAs in mouse model of obesity. PLoS One. 2014;9(1):e86033. doi:10.1371/journal.pone.0086033.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods. 2001;25:402–408. doi:10.1006/meth.2001.1262.
  • Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 2002;30:36e–36. doi:10.1093/nar/30.9.e36.