Commensal Microbiota-induced microRNA modulates intestinal epithelial permeability through the small GTPase ARF4

Journal of Biological Chemistry

Volumn 292, Issue 37, 2017, Pages 15426-15433

  Nakata, Kazuaki ^a   Sugi, Yutaka ^a   Narabayashi, Hikari ^a   Kobayakawa, Tetsuro ^a   Nakanishi, Yusuke ^a   Tsuda, Masato ^a   Hosono, Akira ^a   Kaminogawa, Shuichi ^a   Hanazawa, Shigemasa ^a   Takahashi, Kyoko ^a  

^a NIHON UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELL DEATH; MAMMALS;

ADP-RIBOSYLATION FACTORS; EPITHELIAL BARRIER; EPITHELIAL CELLS; EPITHELIAL PERMEABILITY; INTESTINAL EPITHELIAL CELLS; INTESTINAL INFLAMMATION; INTESTINAL TRACT; PROGRAMMED CELL DEATHS;

RNA;

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 4; CLAUDIN 4; INTERLEUKIN 8; MEMBRANE RECEPTOR; MICRORNA; MICRORNA 21; MICRORNA 21 5P; OCCLUDIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROGRAMMED CELL DEATH 4 PROTEIN; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; APOPTOSIS REGULATORY PROTEIN; ARF4 PROTEIN, HUMAN; ARF4 PROTEIN, MOUSE; MIRN-21 MICRORNA, MOUSE; PDCD4 PROTEIN, MOUSE; PTEN PROTEIN, MOUSE; RNA BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CACO-2 CELL LINE; COMMENSAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HT-29 CELL LINE; HUMAN; HUMAN CELL; INTESTINAL EPITHELIAL PERMEABILITY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE MUCOSA PERMEABILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSEPITHELIAL RESISTANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; ENZYMOLOGY; GENETICS; GERMFREE ANIMAL; INTESTINE MUCOSA; LARGE INTESTINE; METABOLISM; MICROBIOLOGY; PERMEABILITY; PHYSIOLOGY; PROCEDURES; PROTEOMICS; RNA INTERFERENCE; TUMOR CELL LINE; UPREGULATION;

ADP-RIBOSYLATION FACTORS; ANIMALS; APOPTOSIS REGULATORY PROTEINS; CACO-2 CELLS; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; GASTROINTESTINAL MICROBIOME; GERM-FREE LIFE; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; INTESTINE, LARGE; MICE, INBRED BALB C; MICRORNAS; PERMEABILITY; PROTEOMICS; PTEN PHOSPHOHYDROLASE; RNA INTERFERENCE; RNA-BINDING PROTEINS; UP-REGULATION;

EID: 85029583880     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.788596     Document Type: Article

References (33)

1. Bäckhed, F., Ley, R. E., Sonnenburg, J. L., Peterson, D. A., and Gordon, J. I. (2005) Host-bacterial mutualism in the human intestine. Science 307, 1915–1920
2. Tlaskalová-Hogenová, H., Stěpánková, R., Kozáková, H., Hudcovic, T., Vannucci, L., Tučková;, L., Rossmann, P., Hrnčí, T., Kverka, M., Zákostel-ská, Z., Klimečová, K., Pibylová, J., Bártová, J., Sanchez, D., Fundová, P., et al. (2011) The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8, 110 –120
3. Heller, F., Florian, P., Bojarski, C., Richter, J., Christ, M., Hillenbrand, B., Mankertz, J., Gitter, A. H., Bürgel, N., Fromm, M., Zeitz, M., Fuss, I., Strober, W., and Schulzke, J. D. (2005) Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 129, 550 –564
4. Pruteanu, M., Hyland, N. P., Clarke, D. J., Kiely, B., and Shanahan, F. (2011) Degradation of the extracellular matrix components by bacterial-derived metalloproteases: implications for inflammatory bowel diseases. Inflamm. Bowel Dis. 17, 1189 –1200
5. Pruteanu, M., and Shanahan, F. (2013) Digestion of epithelial tight junction proteins by the commensal Clostridium perfringens. Am. J. Physiol. Gastrointest. Liver Physiol. 305, G740 –G748
6. 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, M. N., Artis, D., Walker, M. D., Hornstein, E., et al. (2011) Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat. Immunol. 12, 239 –246
7. Dalmasso, G., Nguyen, H. T., Yan, Y., Laroui, H., Charania, M. A., Ayya-durai, S., Sitaraman, S. V., and Merlin, D. (2011) Microbiota modulate host gene expression via microRNAs. PLoS ONE 6, e19293
8. Singh, N., Shirdel, E. A., Waldron, L., Zhang, R. H., Jurisica, I., and Comelli, E. M. (2012) The murine caecal microRNA signature depends on the presence of the endogenous microbiota. Int. J. Biol. Sci. 8, 171–186
9. Takahashi, K., Sugi, Y., Hosono, A., and Kaminogawa, S. (2009) Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. J. Immunol. 183, 6522– 6529
10. Asangani, I. A., Rasheed, S. A., Nikolova, D. A., Leupold, J. H., Colburn, N. H., Post, S., and Allgayer, H. (2008) MicroRNA-21 (miR-21) post-tran-scriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27, 2128 –2136
11. Meng, F., Henson, R., Wehbe-Janek, H., Ghoshal, K., Jacob, S. T., and Patel, T. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133, 647–658
12. Sayed, D., Rane, S., Lypowy, J., He, M., Chen, I. Y., Vashistha, H., Yan, L., Malhotra, A., Vatner, D., and Abdellatif, M. (2008) MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol. Biol. Cell 19, 3272–3282
13. Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., Gal-uppo, P., Just, S., Rottbauer, W., Frantz, S., Castoldi, M., Soutschek, J., Koteliansky, V., Rosenwald, A., Basson, M. A., et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456, 980 –984
14. Bitomsky, N., Böhm, M., and Klempnauer, K. H. (2004) Transformation suppressor protein Pdcd4 interferes with JNK-mediated phosphorylation of c-Jun and recruitment of the coactivator p300 by c-Jun. Oncogene 23, 7484 –7493
15. Hanafusa, H., Torii, S., Yasunaga, T., and Nishida, E. (2002) Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4, 850 – 858
16. Zhou, X., Ren, Y., Moore, L., Mei, M., You, Y., Xu, P., Wang, B., Wang, G., Jia, Z., Pu, P., Zhang, W., and Kang, C. (2010) Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab. Invest. 90, 144 –155
17. Aggarwal, S., Suzuki, T., Taylor, W. L., Bhargava, A., and Rao, R. K. (2011) Contrasting effects of ERK on tight junction integrity in differentiated and under-differentiated Caco-2 cell monolayers. Biochem. J. 433, 51– 63
18. Langlois, M. J., Bergeron, S., Bernatchez, G., Boudreau, F., Saucier, C., Perreault, N., Carrier, J. C., and Rivard, N. (2010) The PTEN phosphatase controls intestinal epithelial cell polarity and barrier function: role in colorectal cancer progression. PLoS ONE 5, e15742
19. Zhang, Y., Wu, S., Ma, J., Xia, Y., Ai, X., and Sun, J. (2015) Bacterial protein AvrA stabilizes intestinal epithelial tight junctions via blockage of the C-Jun N-terminal kinase pathway. Tissue Barriers 3, e972849
20. Lee, J., Park, E. J., Yuki, Y., Ahmad, S., Mizuguchi, K., Ishii, K. J., Shimaoka, M., and Kiyono, H. (2015) Profiles of microRNA networks in intestinal epithelial cells in a mouse model of colitis. Sci. Rep. 5, 18174
21. Sheedy, F. J., Palsson-McDermott, E., Hennessy, E. J., Martin, C., O’Leary, J. J., Ruan, Q., Johnson, D. S., Chen, Y., and O’Neill, L. A. (2010) Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat. Immunol. 11, 141–147
22. Shi, C., Yang, Y., Xia, Y., Okugawa, Y., Yang, J., Liang, Y., Chen, H., Zhang, P., Wang, F., Han, H., Wu, W., Gao, R., Gasche, C., Qin, H., Ma, Y., and Goel, A. (2016) Novel evidence for an oncogenic role of microRNA-21 in colitis-associated colorectal cancer. Gut 65, 1470 –1481
23. Wu, F., Zhang, S., Dassopoulos, T., Harris, M. L., Bayless, T. M., Meltzer, S. J., Brant, S. R., and Kwon, J. H. (2010) Identification of microRNAs associated with ileal and colonic Crohn’s disease. Inflamm. Bowel Dis. 16, 1729 –1738
24. Maudet, C., Mano, M., and Eulalio, A. (2014) MicroRNAs in the interaction between host and bacterial pathogens. FEBS Lett. 588, 4140 – 4147
25. Staedel, C., and Darfeuille, F. (2013) MicroRNAs and bacterial infection. Cell. Microbiol. 15, 1496 –1507
26. Zhang, L., Shen, J., Cheng, J., and Fan, X. (2015) MicroRNA-21 regulates intestinal epithelial tight junction permeability. Cell Biochem. Funct. 33, 235–240
27. Ye, D., Guo, S., Al-Sadi, R., and Ma, T. Y. (2011) MicroRNA regulation of intestinal epithelial tight junction permeability. Gastroenterology 141, 1323–1333
28. Zhou, Q., Costinean, S., Croce, C. M., Brasier, A. R., Merwat, S., Larson, S. A., Basra, S., and Verne, G. N. (2015) MicroRNA 29 targets nuclear factor B-repressing factor and Claudin 1 to increase intestinal permeability. Gastroenterology 148, 158 –169.e8
29. Ohland, C. L., and Macnaughton, W. K. (2010) Probiotic bacteria and intestinal epithelial barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 298, G807–G819
30. Citalán-Madrid, A. F., García-Ponce, A., Vargas-Robles, H., Betanzos, A., and Schnoor, M. (2013) Small GTPases of the Ras superfamily regulate intestinal epithelial homeostasis and barrier function via common and unique mechanisms. Tissue Barriers 1, e26938
31. Smyth, D., McKay, C. M., Gulbransen, B. D., Phan, V. C., Wang, A., and McKay, D. M. (2012) Interferon- signals via an ERK1/2-ARF6 pathway to promote bacterial internalization by gut epithelia. Cell. Microbiol. 14, 1257–1270
32. Sugi, Y., Takahashi, K., Kurihara, K., Nakata, K., Narabayashi, H., Hamamoto, Y., Suzuki, M., Tsuda, M., Hanazawa, S., Hosono, A., and Kaminogawa, S. (2016) Post-transcriptional regulation of Toll-interacting protein in the intestinal epithelium. PLoS ONE 11, e0164858
33. Agarwal, V., Bell, G. W., Nam, J. W., and Bartel, D. P. (2015) Predicting effective microRNA target sites in mammalian mRNAs. Elife 4, e05005