IL-22 Upregulates Epithelial Claudin-2 to Drive Diarrhea and Enteric Pathogen Clearance

Cell Host and Microbe

Volumn 21, Issue 6, 2017, Pages 671-681.e4

  Tsai, Pei Yun ^b   Zhang, Bingkun ^a,b   He, Wei Qi ^b,c   Zha, Juan Min ^b,c,d   Odenwald, Matthew A ^b   Singh, Gurminder ^b,f   Tamura, Atsushi ^e   Shen, Le ^b   Sailer, Anne ^b   Yeruva, Sunil ^b,f   Kuo, Wei Ting ^f   Fu, Yang Xin ^b,g   Tsukita, Sachiko ^e   Turner, Jerrold R ^b,f  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF CHICAGO   (United States)

^c SOOCHOW UNIVERSITY   (China)

^d THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^e OSAKA UNIVERSITY   (Japan)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

^g UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

bacterial infection; colitis; diarrhea; enteric infection; innate defense; permeability; tight junction

Indexed keywords

CLAUDIN 2; CREATININE; F ACTIN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; UVOMORULIN; CYTOKINE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-22; SODIUM; WATER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL SHEDDING; CITROBACTER RODENTIUM; CITROBACTER RODENTIUM INFECTION; COLITIS; COLON CELL; COLON EPITHELIUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DIARRHEA; DISEASE SEVERITY; ENTEROBACTERIACEAE INFECTION; HOST RESISTANCE; INTESTINE MUCOSA PERMEABILITY; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; OSMOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIGHT JUNCTION; TISSUE INJURY; WATER CONTENT; WATER TRANSPORT; ANIMAL; C57BL MOUSE; CELL MEMBRANE PERMEABILITY; DISEASE MODEL; EPITHELIUM; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; UPREGULATION;

ANIMALS; CELL MEMBRANE PERMEABILITY; CITROBACTER RODENTIUM; CLAUDIN-2; COLITIS; CYTOKINES; DIARRHEA; DISEASE MODELS, ANIMAL; ENTEROBACTERIACEAE INFECTIONS; EPITHELIUM; IMMUNITY, INNATE; INTERLEUKINS; INTESTINAL MUCOSA; INTESTINES; MICE; MICE, INBRED C57BL; SODIUM; TIGHT JUNCTIONS; UP-REGULATION; WATER;

EID: 85020701318     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2017.05.009     Document Type: Article

References (32)

1. Ahmad, R., Chaturvedi, R., Olivares-Villagómez, D., Habib, T., Asim, M., Shivesh, P., Polk, D.B., Wilson, K.T., Washington, M.K., Van Kaer, L., et al. Targeted colonic claudin-2 expression renders resistance to epithelial injury, induces immune suppression, and protects from colitis. Mucosal Immunol. 7 (2014), 1340–1353.
2. Anderson, J.M., Van Itallie, C.M., Physiology and function of the tight junction. Cold Spring Harb. Perspect. Biol., 1, 2009, a002584.
3. Basu, R., O'Quinn, D.B., Silberger, D.J., Schoeb, T.R., Fouser, L., Ouyang, W., Hatton, R.D., Weaver, C.T., Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37 (2012), 1061–1075.
4. Clayburgh, D.R., Barrett, T.A., Tang, Y., Meddings, J.B., Van Eldik, L.J., Watterson, D.M., Clarke, L.L., Mrsny, R.J., Turner, J.R., Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J. Clin. Invest. 115 (2005), 2702–2715.
5. Davison, W.C., A bacteriological and clinical consideration of bacillary dysentery in adults and children. Medicine 1 (1922), 389–510.
6. Deng, W., de Hoog, C.L., Yu, H.B., Li, Y., Croxen, M.A., Thomas, N.A., Puente, J.L., Foster, L.J., Finlay, B.B., A comprehensive proteomic analysis of the type III secretome of Citrobacter rodentium. J. Biol. Chem. 285 (2010), 6790–6800.
7. DuPont, H.L., Hornick, R.B., Adverse effect of lomotil therapy in shigellosis. JAMA 226 (1973), 1525–1528.
8. Giacomin, P.R., Moy, R.H., Noti, M., Osborne, L.C., Siracusa, M.C., Alenghat, T., Liu, B., McCorkell, K.A., Troy, A.E., Rak, G.D., et al. Epithelial-intrinsic IKKα expression regulates group 3 innate lymphoid cell responses and antibacterial immunity. J. Exp. Med. 212 (2015), 1513–1528.
9. Guttman, J.A., Li, Y., Wickham, M.E., Deng, W., Vogl, A.W., Finlay, B.B., Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell. Microbiol. 8 (2006), 634–645.
10. Holmes, J.L., Van Itallie, C.M., Rasmussen, J.E., Anderson, J.M., Claudin profiling in the mouse during postnatal intestinal development and along the gastrointestinal tract reveals complex expression patterns. Gene Expr. Patterns 6 (2006), 581–588.
11. Keely, S., Kelly, C.J., Weissmueller, T., Burgess, A., Wagner, B.D., Robertson, C.E., Harris, J.K., Colgan, S.P., Activated fluid transport regulates bacterial-epithelial interactions and significantly shifts the murine colonic microbiome. Gut Microbes 3 (2012), 250–260.
12. Mankertz, J., Amasheh, M., Krug, S.M., Fromm, A., Amasheh, S., Hillenbrand, B., Tavalali, S., Fromm, M., Schulzke, J.D., TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res. 336 (2009), 67–77.
13. Nik, A.M., Carlsson, P., Separation of intact intestinal epithelium from mesenchyme. Biotechniques 55 (2013), 42–44.
14. Nishida, M., Yoshida, M., Nishiumi, S., Furuse, M., Azuma, T., Claudin-2 regulates colorectal inflammation via myosin light chain kinase-dependent signaling. Dig. Dis. Sci. 58 (2013), 1546–1559.
15. Pham, T.A., Clare, S., Goulding, D., Arasteh, J.M., Stares, M.D., Browne, H.P., Keane, J.A., Page, A.J., Kumasaka, N., Kane, L., et al., Sanger Mouse Genetics Project. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe 16 (2014), 504–516.
16. Pickert, G., Neufert, C., Leppkes, M., Zheng, Y., Wittkopf, N., Warntjen, M., Lehr, H.A., Hirth, S., Weigmann, B., Wirtz, S., et al. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206 (2009), 1465–1472.
17. Pinto, D., Robine, S., Jaisser, F., El Marjou, F.E., Louvard, D., Regulatory sequences of the mouse villin gene that efficiently drive transgenic expression in immature and differentiated epithelial cells of small and large intestines. J. Biol. Chem. 274 (1999), 6476–6482.
18. Qi, W., Joshi, S., Weber, C.R., Wali, R.K., Roy, H.K., Savkovic, S.D., Polyethylene glycol diminishes pathological effects of Citrobacter rodentium infection by blocking bacterial attachment to the colonic epithelia. Gut Microbes 2 (2011), 267–273.
19. Raleigh, D.R., Boe, D.M., Yu, D., Weber, C.R., Marchiando, A.M., Bradford, E.M., Wang, Y., Wu, L., Schneeberger, E.E., Shen, L., Turner, J.R., Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J. Cell Biol. 193 (2011), 565–582.
20. Rankin, L.C., Girard-Madoux, M.J., Seillet, C., Mielke, L.A., Kerdiles, Y., Fenis, A., Wieduwild, E., Putoczki, T., Mondot, S., Lantz, O., et al. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nat. Immunol. 17 (2016), 179–186.
21. Rosen, M.J., Chaturvedi, R., Washington, M.K., Kuhnhein, L.A., Moore, P.D., Coggeshall, S.S., McDonough, E.M., Weitkamp, J.H., Singh, A.B., Coburn, L.A., et al. STAT6 deficiency ameliorates severity of oxazolone colitis by decreasing expression of claudin-2 and Th2-inducing cytokines. J. Immunol. 190 (2013), 1849–1858.
22. Rosenthal, R., Günzel, D., Krug, S.M., Schulzke, J.D., Fromm, M., Yu, A.S., Claudin-2-mediated cation and water transport share a common pore. Acta Physiol. (Oxf.) 219 (2017), 521–536.
23. Sato, T., Stange, D.E., Ferrante, M., Vries, R.G., Van Es, J.H., Van den Brink, S., Van Houdt, W.J., Pronk, A., Van Gorp, J., Siersema, P.D., Clevers, H., Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141 (2011), 1762–1772.
24. Sun, R., Urban, J.F. Jr., Notari, L., Vanuytsel, T., Madden, K.B., Bohl, J.A., Ramalingam, T.R., Wynn, T.A., Zhao, A., Shea-Donohue, T., Interleukin-13 receptor α1-dependent responses in the intestine are critical to parasite clearance. Infect. Immun. 84 (2016), 1032–1044.
25. Suzuki, T., Yoshinaga, N., Tanabe, S., Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J. Biol. Chem. 286 (2011), 31263–31271.
26. Thiagarajah, J.R., Chang, J., Goettel, J.A., Verkman, A.S., Lencer, W.I., Aquaporin-3 mediates hydrogen peroxide-dependent responses to environmental stress in colonic epithelia. Proc. Natl. Acad. Sci. USA 114 (2017), 568–573.
27. Turner, J.R., Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9 (2009), 799–809.
28. Wada, M., Tamura, A., Takahashi, N., Tsukita, S., Loss of claudins 2 and 15 from mice causes defects in paracellular Na+ flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology 144 (2013), 369–380.
29. Weber, C.R., Raleigh, D.R., Su, L., Shen, L., Sullivan, E.A., Wang, Y., Turner, J.R., Epithelial myosin light chain kinase activation induces mucosal interleukin-13 expression to alter tight junction ion selectivity. J. Biol. Chem. 285 (2010), 12037–12046.
30. Xue, M., Zhao, J., Ying, L., Fu, F., Li, L., Ma, Y., Shi, H., Zhang, J., Feng, L., Liu, P., IL-22 suppresses the infection of porcine enteric coronaviruses and rotavirus by activating STAT3 signal pathway. Antiviral Res. 142 (2017), 68–75.
31. Yang, B., Song, Y., Zhao, D., Verkman, A.S., Phenotype analysis of aquaporin-8 null mice. Am. J. Physiol. Cell Physiol. 288 (2005), C1161–C1170.
32. Zheng, Y., Valdez, P.A., Danilenko, D.M., Hu, Y., Sa, S.M., Gong, Q., Abbas, A.R., Modrusan, Z., Ghilardi, N., de Sauvage, F.J., Ouyang, W., Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008), 282–289.