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RESEARCH PAPER

Exosomes transfer miRNAs from cell-to-cell to inhibit autophagy during infection with Crohn’s disease-associated adherent-invasive E. coli

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References

  • Palmela C, Chevarin C, Xu Z, Torres J, Sevrin G, Hirten R, Barnich N, Ng SC, Colombel J-F. Adherent-invasive Escherichia coli in inflammatory bowel disease. Gut. 2018;67:574–587.
  • Carrière J, Darfeuille-Michaud A, Nguyen HTT. Infectious etiopathogenesis of Crohn’s disease. World J Gastroenterol. 2014;20:12102–12117. doi:10.3748/wjg.v20.i34.12102.
  • O’Brien CL, Bringer M-A, Holt KE, Gordon DM, Dubois AL, Barnich N, Darfeuille-Michaud A, Pavli P. Comparative genomics of Crohn’s disease-associated adherent-invasive Escherichia coli. Gut. 2017;66:1382–1389.
  • Martinez-Medina M, Aldeguer X, Lopez-Siles M, González-Huix F, López-Oliu C, Dahbi G, Blanco JE, Blanco J, Garcia-Gil JL, Darfeuille-Michaud A. Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E.coli (AIEC) in Crohn’s disease. Inflamm Bowel Dis. 2009;15:872–882. doi:10.1002/ibd.20860.
  • Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser A-L, Barnich N, Bringer M-A, Swidsinski A, Beaugerie L, Colombel J-F. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127:412–421. doi:10.1053/j.gastro.2004.04.061.
  • Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM. Enhanced Escherichia coli adherence and invasion in Crohn’s disease and colon cancer. Gastroenterology. 2004;127:80–93. doi:10.1053/j.gastro.2004.03.054.
  • Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel J-F. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology. 1998;115:1405–1413.
  • Nguyen HTT, Dalmasso G, Müller S, Carrière J, Seibold F, Darfeuille-Michaud A. Crohn’s disease-associated adherent-invasive Escherichia coli modulate levels of microRNAs in intestinal epithelial cells to reduce autophagy. Gastroenterology. 2014;146:508–519. doi:10.1053/j.gastro.2013.10.021.
  • Bretin A, Carrière J, Dalmasso G, Bergougnoux A, B’chir W, Maurin AC, Müller S, Seibold F, Barnich N, Bruhat A, et al. Activation of the EIF2AK4-EIF2A/eIF2α-ATF4 pathway triggers autophagy response to Crohn disease-associated adherent-invasive Escherichia coli infection. Autophagy. 2016;12:770–783. doi:10.1080/15548627.2016.1156823.
  • Glasser AL, Boudeau J, Barnich N, Perruchot MH, Colombel JF, Darfeuille-Michaud A. Adherent invasive Escherichia coli strains from patients with Crohn’s disease survive and replicate within macrophages without inducing host cell death. Infect Immun. 2001;69:5529–5537. doi:10.1128/IAI.69.9.5529-5537.2001.
  • Lapaquette P, Bringer M-A, Darfeuille-Michaud A. Defects in autophagy favour adherent-invasive Escherichia coli persistence within macrophages leading to increased pro-inflammatory response. Cell Microbiol. 2012;14:791–807. doi:10.1111/j.1462-5822.2012.01768.x.
  • Vazeille E, Buisson A, Bringer MA, Goutte M, Ouchchane L, Hugot JP, de Vallée A, Barnich N, Bommelaer G, Darfeuille-Michaud A. Monocyte-derived macrophages from Crohn’s disease patients are impaired in the ability to control intracellular adherent-invasive Escherichia coli and exhibit disordered cytokine secretion profile. J Crohns Colitis. 2015;9:410–420. doi:10.1093/ecco-jcc/jjv053.
  • Bretin A, Lucas C, Larabi A, Dalmasso G, Billard E, Barnich N, Bonnet R, Nguyen HTT. AIEC infection triggers modification of gut microbiota composition in genetically predisposed mice, contributing to intestinal inflammation. Sci Rep. 2018;8:12301. doi:10.1038/s41598-018-30055-y.
  • Carvalho FA, Barnich N, Sivignon A, Darcha C, Chan CHF, Stanners CP, Darfeuille-Michaud A. Crohn’s disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. J Exp Med. 2009;206:2179–2189. doi:10.1084/jem.20090741.
  • Larabi A, Barnich N, Nguyen HTT. New insights into the interplay between autophagy, gut microbiota and inflammatory responses in IBD. Autophagy. 2019:1–14.
  • Nguyen HTT, Lapaquette P, Bringer M-A D-MA. Autophagy and Crohn’s disease. J Innate Immun. 2013;5:434–443. doi:10.1159/000345129.
  • Brest P, Lapaquette P, Souidi M, Lebrigand K, Cesaro A, Vouret-Craviari V, Mari B, Barbry P, Mosnier J-F, Hébuterne X, et al. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn’s disease. Nat Genet. 2011;43:242–245. doi:10.1038/ng.762.
  • Dalmasso G, Nguyen HTT, Faïs T, Massier S, Barnich N, Delmas J, Bonnet R. Crohn’s disease-associated adherent-invasive Escherichia coli manipulate host autophagy by impairing SUMOylation. Cells. 2019;8:35. doi:10.3390/cells8010035.
  • Lapaquette P, Glasser A-L, Huett A, Xavier RJ, Darfeuille-Michaud A. Crohn’s disease-associated adherent-invasive E.coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell Microbiol. 2010;12:99–113. doi:10.1111/j.1462-5822.2009.01381.x.
  • Carrière J, Barnich N, Nguyen HTT. Exosomes: From Functions in Host-Pathogen Interactions and Immunity to Diagnostic and Therapeutic Opportunities. In: Nilius B., de Tombe P., Gudermann T., Jahn R., Lill R., Petersen O. (eds) Reviews of Physiology, Biochemistry and Pharmacology, Vol. 172. Cham: Springer; 2016. ISBN 978-3-319-49901-7. Online ISBN 978-3-319-49902-4. https://doi-org.proxy.insermbiblio.inist.fr/10.1007/112_2016_7
  • Carrière J, Bretin A, Darfeuille-Michaud A, Barnich N, Nguyen HTT. Exosomes released from cells infected with Crohn’s disease–associated adherent-invasive Escherichia coli activate host innate immune responses and enhance bacterial intracellular replication. Inflamm Bowel Dis. 2016;22:516–528.
  • Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659. doi:10.1038/ncb1596.
  • Singh PP, Li L, Schorey JS. Exosomal RNA from Mycobacterium tuberculosis-infected cells is functional in recipient macrophages. Traffic. 2015;16:555–571. doi:10.1111/tra.12278.
  • Zhou C, Tan L, Sun Y, Qiu X, Liao Y, Song C, Liu W, Nair V, Ding C. Exosomes carry microRNAs into neighboring cells to promote diffusive infection of newcastle disease virus. Viruses. 2019;11:527. doi:10.3390/v11060527.
  • Alexander M, Hu R, Runtsch MC, Kagele DA, Mosbruger TL, Tolmachova T, Seabra MC, Round JL, Ward DM, O’Connell RM. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun. 2015;6. doi:10.1038/ncomms8321.
  • Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, Baty CJ, Gibson GA, Erdos G, Wang Z, et al. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood. 2012;119:756–766. doi:10.1182/blood-2011-02-338004.
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Arozena AA, Adachi H, Adams CM, Adams PD, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
  • Zhang W, Jiang X, Bao J, Wang Y, Liu H, Tang L. Exosomes in pathogen infections: a bridge to deliver molecules and link functions. Front Immunol. 2018;9:1–12. doi:10.3389/fimmu.2018.00001.
  • Abrami L, Brandi L, Moayeri M, Brown MJ, Krantz BA, Leppla SH. van der Goot FG. Hijacking multivesicular bodies enables long-term and exosome-mediated long-distance action of anthrax toxin. Cell Rep. 2013;5:986–996. doi:10.1016/j.celrep.2013.10.019.
  • Shimoda A, Ueda K, Nishiumi S, Murata-Kamiya N, Mukai S, Sawada S, Azuma T, Hatakeyama M, Akiyoshi K. Exosomes as nanocarriers for systemic delivery of the Helicobacter pylori virulence factor CagA. Sci Rep. 2016;6:18346. doi:10.1038/srep18346.
  • Chen Y, Wang X, Yu Y, Xiao Y, Huang J, Yao Z, Chen X, Zhou T, Li P, Xu C. Serum exosomes of chronic gastritis patients infected with Helicobacter pylori mediate IL-1α expression via IL-6 trans-signalling in gastric epithelial cells. Clin Exp Immunol. 2018;194:339–349. doi:10.1111/cei.13200.
  • Cheng Y, Schorey JS. Extracellular vesicles deliver Mycobacterium RNA to promote host immunity and bacterial killing. EMBO Rep. 2019;20:e46613. doi:10.15252/embr.201846613.
  • Walters SB, Kieckbusch J, Nagalingam G, Swain A, Latham SL, Grau GER, Britton WJ, Combes V, Saunders BM. Microparticles from mycobacteria-infected macrophages promote inflammation and cellular migration. J Immunol. 2013;190:669–677. doi:10.4049/jimmunol.1201856.
  • Hare NJ, Chan B, Chan E, Kaufman KL, Britton WJ, Saunders BM. Microparticles released from Mycobacterium tuberculosis-infected human macrophages contain increased levels of the type I interferon inducible proteins including ISG15. Proteomics. 2015;15:3020–3029. doi:10.1002/pmic.201400610.
  • Li L, Cheng Y, Emrich S, Schorey J. Activation of endothelial cells by extracellular vesicles derived from Mycobacterium tuberculosis infected macrophages or mice. PLoS One. 2018;13:e0198337. doi:10.1371/journal.pone.0198337.
  • Fu Y, Zhang L, Zhang F, Tang T, Zhou Q, Feng C, Jin Y, Wu Z. Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection. PLoS Pathog. 2017;13:e1006611. doi:10.1371/journal.ppat.1006611.
  • Maemura T, Fukuyama S, Sugita Y, Lopes TJS, Nakao T, Noda T, Kawaoka Y. Lung-derived exosomal miR-483-3p regulates the innate immune response to Influenza virus infection. J Infect Dis. 2018;217:1372–1382. doi:10.1093/infdis/jiy035.
  • Jiang K, Yang J, Guo S, Zhao G, Wu H, Deng G. Peripheral circulating exosome-mediated delivery of miR-155 as a novel mechanism for acute lung inflammation. Mol Ther. 2019;27:1–14. doi:10.1016/j.ymthe.2019.07.003.
  • Wang J, Deng Z, Wang Z, Wu J, Gu T, Jiang Y, Li G. MicroRNA-155 in exosomes secreted from Helicobacter pylori infection macrophages immunomodulates inflammatory response. Am J Transl Res. 2016;8:3700–3709.
  • Alipoor SD, Mortaz E, Tabarsi P, Farnia P, Mirsaeidi M, Garssen J, Movassaghi M, Adcock IM. Bovis bacillus calmette–guerin (BCG) infection induces exosomal miRNA release by human macrophages. J Transl Med. 2017;15:105. doi:10.1186/s12967-017-1205-9.
  • Mitsuhashi S, Feldbrügge L, Csizmadia E, Mitsuhashi M, Robson SC, Moss AC. Luminal extracellular vesicles (EVs) in inflammatory bowel disease (IBD) exhibit proinflammatory effects on epithelial cells and macrophages. Inflamm Bowel Dis. 2016;22:1587–1595. doi:10.1097/MIB.0000000000000840.
  • Zhang X, Deeke SA, Ning Z, Starr AE, Butcher J, Li J, Mayne J, Cheng K, Liao B, Li L, et al. Metaproteomics reveals associations between microbiome and intestinal extracellular vesicle proteins in pediatric inflammatory bowel disease. Nat Commun. 2018;9:2873. doi:10.1038/s41467-018-05357-4.
  • Rasko DA, Rosovitz MJ, Myers GSA, MongodinEF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, et al. The pangenome structure of Escherichia coli: comparative genomic analysis of e. coli commensal and pathogenic isolates. J Bacteriol. 2008;190:6881–6893. doi:10.1128/JB.00619-08.

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