2,119
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Mitochondrial dysfunction-associated microbiota establishes a transmissible refractory response to anti-TNF therapy during ulcerative colitis

ORCID Icon, ORCID Icon, , ORCID Icon, , ORCID Icon, , , ORCID Icon, ORCID Icon, , , ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon show all
Article: 2266626 | Received 08 Mar 2023, Accepted 29 Sep 2023, Published online: 16 Oct 2023

References

  • Gisbert JP, Chaparro M. Primary failure to an anti-TNF agent in inflammatory bowel disease: switch (to a second anti-TNF agent) or swap (for another mechanism of action)? J Clin Med. 2021;10(22):5318. doi:10.3390/jcm10225318.
  • Gerriets V, Goyal A, Khaddour K. Tumor necrosis factor inhibitors. Florida: StatPearls. Treasure Island (FL); 2022.
  • Haberman Y, Karns R, Dexheimer PJ, Schirmer M, Somekh J, Jurickova I, Braun T, Novak E, Bauman L, Collins MH, et al. Ulcerative colitis mucosal transcriptomes reveal mitochondriopathy and personalized mechanisms underlying disease severity and treatment response. Nat Commun. 2019;10(1):38. doi:10.1038/s41467-018-07841-3.
  • Mottawea W, Chiang CK, Muhlbauer M, Starr AE, Butcher J, Abujamel T, Deeke SA, Brandel A, Zhou H, Shokralla S, et al. Altered intestinal microbiota–host mitochondria crosstalk in new onset Crohn’s disease. Nat Commun. 2016;7(1):13419. doi:10.1038/ncomms13419.
  • Peloquin JM, Goel G, Villablanca EJ, Xavier RJ. Mechanisms of pediatric inflammatory bowel disease. Annu Rev Immunol. 2016;34(1):31–16. doi:10.1146/annurev-immunol-032414-112151.
  • Hatle KM, Gummadidala P, Navasa N, Bernardo E, Dodge J, Silverstrim B, Fortner K, Burg E, Suratt BT, Hammer J, et al. MCJ/DnaJC15, an endogenous mitochondrial repressor of the respiratory chain that controls metabolic alterations. Mol Cell Biol. 2013;33:2302–2314. doi:10.1128/MCB.00189-13.
  • Schusdziarra C, Blamowska M, Azem A, Hell K. Methylation-controlled J-protein MCJ acts in the import of proteins into human mitochondria. Hum Mol Genet. 2013;22:1348–1357. doi:10.1093/hmg/dds541.
  • Navasa N, Martin I, Iglesias-Pedraz JM, Beraza N, Atondo E, Izadi H, Ayaz F, Fernandez-Alvarez S, Hatle K, Som A, Dienz, O., et al. Regulation of oxidative stress by methylation-controlled J protein controls macrophage responses to inflammatory insults. J Infect Dis. 2015;211(1):135–145. doi:10.1093/infdis/jiu389.
  • Pascual-Itoiz MA, Pena-Cearra A, Martin-Ruiz I, Lavin JL, Simo C, Rodriguez H, Atondo E, Flores JM, Carreras-Gonzalez A, Tomas-Cortazar J, et al. The mitochondrial negative regulator MCJ modulates the interplay between microbiota and the host during ulcerative colitis. Sci Rep. 2020;10(1):572. doi:10.1038/s41598-019-57348-0.
  • Pena-Cearra A, Pascual-Itoiz MA, Lavin JL, Fuertes M, Martin-Ruiz I, Castelo J, Palacios A, Barriales D, Fullaondo A, Aransay AM, et al. Mitochondrial complex I dysfunction alters the balance of soluble and membrane-bound TNF during chronic experimental colitis. Sci Rep. 2022;12(1):9977. doi:10.1038/s41598-022-13480-y.
  • Lloyd-Price J, Arze C, Ananthakrishnan AN, Schirmer M, Avila-Pacheco J, Poon TW, Andrews E, Ajami NJ, Bonham KS, Brislawn CJ, et al. Multi-omics of the gut microbial ecosystem in inflammatory bowel diseases. Nature. 2019;569(7758):655–662. doi:10.1038/s41586-019-1237-9.
  • Peña-Cearra A, Song, D, Castelo, J, Palacios, A, Lavin, JL, Azkargorta, M, Elortza, F, Fuertes, M, Pascual-Itoiz, MA, Barriales, D, Martin-Ruiz, I, Fullaondo, A, Aransay, AM, Rodriguez, H, Palm, NW, Anguita, J, Abecia, L. Mitochondrial dysfunction promotes microbial composition that negatively impacts on ulcerative colitis development and progression. npj Biofilms and Microbes. 2023;9(74):0709–2023. doi:10.1038/s41522-023-00443-y37805634.
  • Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576–589. doi:10.1016/j.molcel.2010.05.004.
  • West NR, Hegazy AN, Owens BMJ, Bullers SJ, Linggi B, Buonocore S, Coccia M, Gortz D, This S, Stockenhuber K, et al. Oncostatin M drives intestinal inflammation and predicts response to tumor necrosis factor–neutralizing therapy in patients with inflammatory bowel disease. Nat Med. 2017;23(5):579–589. doi:10.1038/nm.4307.
  • Czarnewski P, Parigi SM, Sorini C, Diaz OE, Das S, Gagliani N, Villablanca EJ. Conserved transcriptomic profile between mouse and human colitis allows unsupervised patient stratification. Nat Commun. 2019;10(1):2892. doi:10.1038/s41467-019-10769-x.
  • Smith PD, Janoff EN, Mosteller-Barnum M, Merger M, Orenstein JM, Kearney JF, Graham MF. Isolation and purification of CD14-negative mucosal macrophages from normal human small intestine. J Immunol Methods. 1997;202(1):1–11. doi:10.1016/s0022-1759(96)00204-9.
  • Castro-Dopico T, Dennison TW, Ferdinand JR, Mathews RJ, Fleming A, Clift D, Stewart BJ, Jing C, Strongili K, Labzin LI, et al. Anti-commensal IgG drives intestinal inflammation and type 17 immunity in ulcerative colitis. Immunity. 2019;50(4):1099–1114 e1010. doi:10.1016/j.immuni.2019.02.006.
  • Ohtsuka Y, Lee J, Stamm DS, Sanderson IR. MIP-2 secreted by epithelial cells increases neutrophil and lymphocyte recruitment in the mouse intestine. Gut. 2001;49(4):526–533. doi:10.1136/gut.49.4.526.
  • Hall AB, Yassour M, Sauk J, Garner A, Jiang X, Arthur T, Lagoudas GK, Vatanen T, Fornelos N, Wilson R, et al. A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients. Genome Med. 2017;9(1):103. doi:10.1186/s13073-017-0490-5.
  • Dovrolis N, Michalopoulos G, Theodoropoulos GE, Arvanitidis K, Kolios G, Sechi LA, Eliopoulos AG, Gazouli M. The interplay between mucosal microbiota composition and host gene-expression is linked with infliximab response in inflammatory bowel diseases. Microorganisms. 2020;8(3):438. doi:10.3390/microorganisms8030438.
  • Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature. 2009;461(7268):1282–1286. doi:10.1038/nature08530.
  • Zhai R, Xue X, Zhang L, Yang X, Zhao L, Zhang C. Strain-specific anti-inflammatory properties of two Akkermansia muciniphila strains on chronic colitis in mice. Front Cell Infect Microbiol. 2019;9:239. doi:10.3389/fcimb.2019.00239.
  • Png CW, Linden SK, Gilshenan KS, Zoetendal EG, McSweeney CS, Sly LI, McGuckin MA, Florin TH. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105(11):2420–2428. doi:10.1038/ajg.2010.281.
  • Wang B, Chen X, Chen Z, Xiao H, Dong J, Li Y, Zeng X, Liu J, Wan G, Fan S, et al. Stable colonization of Akkermansia muciniphila educates host intestinal microecology and immunity to battle against inflammatory intestinal diseases. Experimental & Molecular Medicine. 2023;55(1):55–68. doi:10.1038/s12276-022-00911-z.
  • Koelink PJ, Bloemendaal FM, Li B, Westera L, Vogels EWM, van Roest M, Gloudemans AK, van ’t Wout AB, Korf H, Vermeire S, et al. Anti-TNF therapy in IBD exerts its therapeutic effect through macrophage IL-10 signalling. Gut. 2020;69(6):1053–1063. doi:10.1136/gutjnl-2019-318264.
  • Rajca S, Grondin V, Louis E, Vernier-Massouille G, Grimaud JC, Bouhnik Y, Laharie D, Dupas JL, Pillant H, Picon L, et al. Alterations in the intestinal microbiome (dysbiosis) as a predictor of relapse after infliximab withdrawal in Crohn’s disease. Inflamm Bowel Dis. 2014;20:978–986. doi:10.1097/MIB.0000000000000036.
  • Camuesco D, Comalada M, Rodriguez-Cabezas ME, Nieto A, Lorente MD, Concha A, Zarzuelo A, Galvez J. The intestinal anti-inflammatory effect of quercitrin is associated with an inhibition in iNOS expression. Br J Pharmacol. 2004;143(7):908–918. doi:10.1038/sj.bjp.0705941.
  • Lopetuso LR, Petito V, Cufino V, Arena V, Stigliano E, Gerardi V, Gaetani E, Poscia A, Amato A, Cammarota G, et al. Locally injected infliximab ameliorates murine DSS colitis: differences in serum and intestinal levels of drug between healthy and colitic mice. Dig Liver Dis. 2013;45:1017–1021. doi:10.1016/j.dld.2013.06.007.
  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21. doi:10.1093/bioinformatics/bts635.
  • Liao Y, Smyth GK, Shi W. The subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41:e108. doi:10.1093/nar/gkt214.
  • 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.
  • Huang da W, BT S, RA L. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57. doi:10.1038/nprot.2008.211.
  • Chen J, Bardes EE, Aronow BJ, Jegga AG. ToppGene suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res. 2009;37(Web Server):W305–311. doi:10.1093/nar/gkp427.
  • Kaimal V, Bardes EE, Tabar SC, Jegga AG, Aronow BJ. ToppCluster: a multiple gene list feature analyzer for comparative enrichment clustering and network-based dissection of biological systems. Nucleic Acids Res. 2010;38:W96–102. doi:10.1093/nar/gkq418.
  • Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T. A travel guide to Cytoscape plugins. Nat Methods. 2012;9(11):1069–1076. doi:10.1038/nmeth.2212.
  • Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pages F, Trajanoski Z, Galon J. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25(8):1091–1093. doi:10.1093/bioinformatics/btp101.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using Real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335–336. doi:10.1038/nmeth.f.303.
  • Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460–2461. doi:10.1093/bioinformatics/btq461.
  • McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012;6(3):610–618. doi:10.1038/ismej.2011.139.