The intestinal microbiota interferes with the microrna response upon oral listeria infection

mBio

Volumn 4, Issue 6, 2013, Pages

  Archambaud, Cristel ^a,b,c   Sismeiro, Odile ^a   Toedling, Joern ^d,e,f,g   Soubigou, Guillaume ^a   Bécavin, Christophe ^a,b,c   Lechat, Pierre ^a   Lebreton, Alice ^a,b,c   Ciaudo, Constance ^g,h   Cossart, Pascale ^a,b,c  

^a INSTITUT PASTEUR   (France)

^b INSERM   (France)

^c USC 2020   (France)

^d INSTITUT CURIE   (France)

^e INSERM U900   (France)

^f PSL RESEARCH UNIVERSITY   (France)

^g CNRS   (France)

^h ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 143; MICRORNA 148; MICRORNA 192; MICRORNA 194; MICRORNA 200B; MICRORNA 200C; MICRORNA 21; MICRORNA 215; MICRORNA 30D; MICRORNA 378; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENETIC ASSOCIATION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INTERACTIONS WITH RNA; INTESTINE FLORA; LISTERIA MONOCYTOGENES; LISTERIOSIS; MOUSE; MOUTH INFECTION; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY MECHANISM; SEQUENCE ANALYSIS; TRANSCRIPTION REGULATION; ANIMAL; C57BL MOUSE; FEMALE; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; ILEUM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MICROFLORA;

ANIMALS; FEMALE; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; ILEUM; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED C57BL; MICROBIOTA; MICRORNAS; TRANSCRIPTION, GENETIC;

EID: 84891618594     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00707-13     Document Type: Article

References (59)

1. Cossart P. 2011. Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. U. S. A. 108:19484-19491.
2. Stavru F, Archambaud C, Cossart P. 2011. Cell biology and immunology of Listeria monocytogenes infections: novel insights. Immunol. Rev. 240: 160-184.
3. Aubry C, Goulard C, Nahori MA, Cayet N, Decalf J, Sachse M, Boneca IG, Cossart P, Dussurget O. 2011. OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J. Infect. Dis. 204:731-740.
4. Boneca IG, Dussurget O, Cabanes D, Nahori MA, Sousa S, Lecuit M, Psylinakis E, Bouriotis V, Hugot JP, Giovannini M, Coyle A, Bertin J, Namane A, Rousselle JC, Cayet N, Prévost MC, Balloy V, Chignard M, Philpott DJ, Cossart P, Girardin SE. 2007. A critical role for peptidogly can N-deacetylation in Listeria evasion from the host innate immune system. Proc. Natl. Acad. Sci. U. S. A. 104:997-1002.
5. Rae CS, Geissler A, Adamson PC, Portnoy DA. 2011. Mutations of the Listeria monocytogenes peptidoglycan N-deacetylase and O-acetylase result in enhanced lysozyme sensitivity, bacteriolysis, and hyperinduction of innate immune pathways. Infect. Immun. 79:3596-3606.
6. Dortet L, Mostowy S, Cossart P. 2012. Listeria and autophagy escape: involvement of InlK, an internalin-like protein. Autophagy 8:132-134.
7. Dortet L, Mostowy S, Samba-Louaka A, Gouin E, Nahori MA, Wiemer EA, Dussurget O, Cossart P. 2011. Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog. 7:e1002168. doi:10.1371/journal.ppat.1002168.
8. Yoshikawa Y, Ogawa M, Hain T, Yoshida M, Fukumatsu M, Kim M, Mimuro H, Nakagawa I, Yanagawa T, Ishii T, Kakizuka A, Sztul E, Chakraborty T, Sasakawa C. 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 11:1233-1240.
9. Gouin E, Adib-Conquy M, Balestrino D, Nahori MA, Villiers V, Colland F, Dramsi S, Dussurget O, Cossart P. 2010. The Listeria monocytogenes InlC protein interferes with innate immune responses by targeting the I{kappa}B kinase subunit IKK{alpha}. Proc. Natl. Acad. Sci. U. S. A. 107:17333-17338.
10. Carrero JA, Unanue ER. 2012. Mechanisms and immunological effects of apoptosis caused by Listeria monocytogenes. Adv. Immunol. 113:157-174.
11. Hamon MA, Ribet D, Stavru F, Cossart P. 2012. Listeriolysin O: the Swiss army knife of Listeria. Trends Microbiol. 20:360-368.
12. Hawiger J. 2001. Innate immunity and inflammation: a transcriptional paradigm. Immunol. Res. 23:99-109.
13. Gripenland J, Netterling S, Loh E, Tiensuu T, Toledo-Arana A, Johans son J. 2010. RNAs: regulators of bacterial virulence. Nat. Rev. Microbiol. 8:857-866.
14. Toledo-Arana A, Repoila F, Cossart P. 2007. Small noncoding RNAs controlling pathogenesis. Curr. Opin. Microbiol. 10:182-188.
15. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K, Barthelemy M, Vergassola M, Nahori MA, Soubigou G, Régnault B, Coppée JY, Lecuit M, Johansson J, Cossart P. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950-956.
16. Flynt AS, Lai EC. 2008. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9:831-842.
17. Schickel R, Boyerinas B, Park SM, Peter ME. 2008. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27:5959-5974.
18. Xiao C, Rajewsky K. 2009. MicroRNA control in the immune system: basic principles. Cell 136:26-36.
19. Eulalio A, Schulte L, Vogel J. 2012. The mammalian microRNA response to bacterial infections. RNA Biol. 9:742-750.
20. Staedel C, Darfeuille F. 2013. MicroRNAs and bacterial infection. Cell. Microbiol. 15:1496-1507. doi:10.1111/cmi.12159.
21. Staiger D, Korneli C, Lummer M, Navarro L. 2013. Emerging role for RNA-based regulation in plant immunity. New Phytol. 197:394-404.
22. Ivanov II, Honda K. 2012. Intestinal commensal microbes as immune modulators. Cell Host Microbe 12:496-508.
23. Maynard CL, Elson CO, Hatton RD, Weaver CT. 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489: 231-241.
24. Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242-249.
25. Stecher B, Hardt WD. 2008. The role of microbiota in infectious disease. Trends Microbiol. 16:107-114.
26. Biton M, Levin A, Slyper M, Alkalay I, Horwitz E, Mor H, Kredo-Russo S, Avnit-Sagi T, Cojocaru G, Zreik F, Bentwich Z, Poy MN, Artis D, Walker MD, Hornstein E, Pikarsky E, Ben-Neriah Y. 2011. Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 12:239-246.
27. Dalmasso G, Nguyen HT, Yan Y, Laroui H, Charania MA, Ayyadurai S, Sitaraman SV, Merlin D. 2011. Microbiota modulate host gene expression via microRNAs. PLoS One 6:e19293. doi:10.1371/ journal.pone.0019293.
28. Duerr CU, Hornef MW. 2012. The mammalian intestinal epithelium as integral player in the establishment and maintenance of host-microbial homeostasis. Semin. Immunol. 24:25-35.
29. Singh N, Shirdel EA, Waldron L, Zhang RH, Jurisica I, Comelli EM, Archambaud et al. 2012. The murine caecal microRNA signature depends on the presence of the endogenous microbiota. Int. J. Biol Sci 8:171-186.
30. Xue X, Feng T, Yao S, Wolf KJ, Liu CG, Liu X, Elson CO, Cong Y. 2011. Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J. Immunol. 187:5879-5886.
31. Archambaud C, Nahori MA, Soubigou G, Bécavin C, Laval L, Lechat P, Smokvina T, Langella P, Lecuit M, Cossart P. 2012. Impact of lactobacilli on orally acquired listeriosis. Proc. Natl. Acad. Sci. U. S. A. 109: 16684-16689.
32. Smith K, McCoy KD, Macpherson AJ. 2007. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19:59-69.
33. Chen CJ, Servant N, Toedling J, Sarazin A, Marchais A, Duvernois Berthet E, Cognat V, Colot V, Voinnet O, Heard E, Ciaudo C, Barillot E. 2012. ncPRO-seq: a tool for annotation and profiling of ncRNAs in sRNA-seq data. Bioinformatics 28:3147-3149.
34. Lecuit M, Sonnenburg JL, Cossart P, Gordon JI. 2007. Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. J. Biol. Chem. 282: 15065-15072.
35. Nagaraj N, Wisniewski JR, Geiger T, Cox J, Kircher M, Kelso J, Pääbo S, Mann M. 2011. Deep proteome and transcriptome mapping of a human cancer cell line. Mol. Syst. Biol. 7:548. doi:10.1038/msb.2011.81.
36. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
37. Saito T, Saetrom P. 2010. MicroRNAs-targeting and target prediction. N. Biotechnol. 27:243-249.
38. Jiang S, Zhang LF, Zhang HW, Hu S, Lu MH, Liang S, Li B, Li Y, Li D, Wang ED, Liu MF. 2012. A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J. 31: 1985-1998.
39. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. 2002. Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12:735-739.
40. Babak T, Zhang W, Morris Q, Blencowe BJ, Hughes TR. 2004. Probing microRNAs with microarrays: tissue specificity and functional inference. RNA 10:1813-1819.
41. Beuvink I, Kolb FA, Budach W, Garnier A, Lange J, Natt F, Dengler U, Hall J, Filipowicz W, Weiler J. 2007. A novel microarray approach reveals new tissue-specific signatures of known and predicted mammalian microRNAs. Nucleic Acids Res. 35:e52. doi:10.1093/nar/gkm360.
42. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foà R, Schliwka J, Fuchs U, Novosel A, Müller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter HI, Hornung V, Teng G, Hartmann G, Palkovits M, Di Lauro R, Wernet P, Macino G, Rogler CE, Nagle JW, Ju J, Papavasiliou FN, Benzing T, Lichter P, Tam W, Brownstein MJ, Bosio A, Borkhardt A, Russo JJ, Sander C, Zavolan M, Tuschl T. 2007. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401-1414.
43. Takada S, Berezikov E, Yamashita Y, Lagos-Quintana M, Kloosterman WP, Enomoto M, Hatanaka H, Fujiwara S, Watanabe H, Soda M, Choi YL, Plasterk RH, Cuppen E, Mano H. 2006. Mouse microRNA profiles determined with a new and sensitive cloning method. Nucleic Acids Res. 34:e115. doi:10.1093/nar/gkj093.
44. Gaedcke J, Grade M, Camps J, Søkilde R, Kaczkowski B, Schetter AJ, Difilippantonio MJ, Harris CC, Ghadimi BM, Møller S, Beissbarth T, Ried T, Litman T. 2012. The rectal cancer microRNAome-microRNA expression in rectal cancer and matched normal mucosa. Clin. Cancer Res. 18:4919-4930.
45. Hu S, Dong TS, Dalal SR, Wu F, Bissonnette M, Kwon JH, Chang EB. 2011. The microbe-derived short chain fatty acid butyrate targets miRNA-dependent p21 gene expression in human colon cancer. PLoS One 6:e16221. doi:10.1371/journal.pone.0016221.
46. Lu LF, Boldin MP, Chaudhry A, Lin LL, Taganov KD, Hanada T, Yoshimura A, Baltimore D, Rudensky AY. 2010. Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses. Cell 142: 914-929.
47. Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, Bradley A. 2007. Requirement of bic/microRNA-155 for normal immune function. Science 316:608-611.
48. Taganov KD, Boldin MP, Chang KJ, Baltimore D. 2006. NF-kappaB dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103:12481-12486.
49. Artis D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8:411-420.
50. Quinn SR, O'Neill LA. 2011. A trio of microRNAs that control Toll-like receptor signalling. Int. Immunol. 23:421-425.
51. Kleinsteuber K, Heesch K, Schattling S, Kohns M, Sander-Jülch C, Walzl G, Hesseling A, Mayatepek E, Fleischer B, Marx FM, Jacobsen M. 2013. Decreased expression of miR-21, miR-26a, miR-29a, and miR142-3p in CD4() T cells and peripheral blood from tuberculosis patients. PLoS One 8:e61609. doi:10.1371/journal.pone.0061609.
52. Baud J, Varon C, Chabas S, Chambonnier L, Darfeuille F, Staedel C. 2013. Helicobacter pylori initiates a mesenchymal transition through ZEB1 in gastric epithelial cells. PLoS One 8:e60315. doi:10.1371/ journal.pone.0060315.
53. Nguyen TT, Johnsen IB, Knetter CF, Drabløs F, Fitzgerald KA, Lien E, Anthonsen MW. 2010. Differential gene expression downstream of Toll like receptors (TLRs): role of c-Src and activating transcription factor 3 (ATF3). J. Biol. Chem. 285:17011-17019.
54. Ito J, Ito M, Nambu H, Fujikawa T, Tanaka K, Iwaasa H, Tokita S. 2009. Anatomical and histological profiling of orphan G-protein-coupled receptor expression in gastrointestinal tract of C57BL/6J mice. Cell Tissue Res. 338:257-269.
55. Terahara K, Nochi T, Yoshida M, Takahashi Y, Goto Y, Hatai H, Kurokawa S, Jang MH, Kweon MN, Domino SE, Hiroi T, Yuki Y, Tsunetsugu-Yokota Y, Kobayashi K, Kiyono H. 2011. Distinct fucosylation of M cells and epithelial cells by Fut1 and Fut2, respectively, in response to intestinal environmental stress. Biochem. Biophys. Res. Commun. 404:822-828.
56. Doherty GA, Bai A, Hanidziar D, Longhi MS, Lawlor GO, Putheti P, Csizmadia E, Nowak M, Cheifetz AS, Moss AC, Robson SC. 2012. CD73 is a phenotypic marker of effector memory Th17 cells in inflammatory bowel disease. Eur. J. Immunol. 42:3062-3072.
57. Heale BS, Keegan LP, McGurk L, Michlewski G, Brindle J, Stanton CM, Caceres JF, O'Connell MA. 2009. Editing independent effects of ADARs on the miRNA/siRNA pathways. EMBO J. 28:3145-3156.
58. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249-264.
59. Jain N, Thatte J, Braciale T, Ley K, O'Connell M, Lee JK. 2003. Local-pooled-error test for identifying differentially expressed genes with a small number of replicated microarrays. Bioinformatics 19:1945-1951.