Intestinal epithelium-specific MyD88 signaling impacts host susceptibility to infectious colitis by promoting protective goblet cell and antimicrobial responses

Infection and Immunity

Volumn 82, Issue 9, 2014, Pages 3753-3763

  Bhinder, Ganive ^a   Stahl, Martin ^a   Sham, Ho Pan ^a,b   Crowley, Shauna M ^a   Morampudi, Vijay ^a   Dalwadi, Udit ^a   Ma, Caixia ^a   Jacobson, Kevan ^a   Vallance, Bruce A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUCIN 2; MYELOID DIFFERENTIATION FACTOR 88;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL PROTECTION; CITROBACTER RODENTIUM; COLITIS; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE SEVERITY; GOBLET CELL; HOST RESISTANCE; HOST SUSCEPTIBILITY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTESTINE EPITHELIUM; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SIGNAL TRANSDUCTION; TISSUE INJURY; WILD TYPE;

ANIMALS; ANTI-INFECTIVE AGENTS; CITROBACTER RODENTIUM; COLITIS; ENTEROBACTERIACEAE INFECTIONS; EPITHELIAL CELLS; GASTROENTERITIS; GASTROINTESTINAL TRACT; GOBLET CELLS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION;

EID: 84906071028     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02045-14     Document Type: Article

References (31)

1. Mandeville KL, Krabshuis J, Ladep NG, Mulder CJ, Quigley EM, Khan SA. 2009. Gastroenterology in developing countries: issues and advances. World J. Gastroenterol. 15:2839-2854. http://dx.doi.org/10.3748/wjg.15.2839.
2. Ohl ME, Miller SI. 2001. Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52:259-274. http://dx.doi.org/10.1146/annurev.med.52.1.259.
3. Akira S, Takeda K. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511. http://dx.doi.org/10.1038/nri1391.
4. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118:229-241. http://dx.doi.org/10.1016/j.cell.2004.07.002.
5. Gibson DL, Ma C, Bergstrom KSB, Huang JT, Man C, Vallance BA. 2008. MyD88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10:618-631. http://dx.doi.org/10.1111/j.1462-5822.2007.01071.x.
6. Lebeis SL, Bommarius B, Parkos CA, Sherman MA, Kalman D. 2007. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J. Immunol. 179:566-577. http://dx.doi.org/10.4049/jimmunol.179.1.566.
7. Araki A, Kanai T, Ishikura T, Makita S, Uraushihara K, Iiyama R, Totsuka T, Takeda K, Akira S, Watanabe M. 2005. MyD88-deficient mice develop severe intestinal inflammation in dextran sodium sulfate colitis. J. Gastroenterol. 40:16-23. http://dx.doi.org/10.1007/s00535-004-1492-9.
8. Malvin NP, Seno H, Stappenbeck TS. 2012. Colonic epithelial response to injury requires Myd88 signaling in myeloid cells. Mucosal Immunol. 5:194-206. http://dx.doi.org/10.1038/mi.2011.65.
9. Kirkland D, Benson A, Mirpuri J, Pifer R, Hou B, DeFranco AL, Yarovinsky F. 2012. B cell-intrinsic MyD88 signaling prevents the lethal dissemination of commensal bacteria during colonic damage. Immunity 36:228-238. http://dx.doi.org/10.1016/j.immuni.2011.11.019.
10. Asquith MJ, Boulard O, Powrie F, Maloy KJ. 2010. Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease. Gastroenterology 139:519-529. http://dx.doi.org/10.1053/j.gastro.2010.04.045.
11. Brandl K, Sun L, Neppl C, Siggs OM, Le Gall SM, Tomisato W, Li X, Du X, Maennel DN, Blobel CP, Beutler B. 2010. MyD88 signaling in nonhematopoietic cells protects mice against induced colitis by regulating specific EGF receptor ligands. Proc. Natl. Acad. Sci. U. S. A. 107:19967-19972. http://dx.doi.org/10.1073/pnas.1014669107.
12. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. 2005. Citrobacter rodentium of mice and man. Cell Microbiol. 7:1697-1706. http://dx.doi.org/10.1111/j.1462-5822.2005.00625.x.
13. Goto Y, Kiyono H. 2012. Epithelial barrier: an interface for the crosscommunication between gut flora and immune system. Immunol. Rev. 245:147-163. http://dx.doi.org/10.1111/j.1600-065X.2011.01078.x.
14. Khan MA, Steiner TS, Sham HP, Bergstrom KSB, Huang JT, Assi K, Salh B, Tai IT, Li X, Vallance BA. 2010. The single IgG IL-1-related receptor controls TLR responses in differentiated human intestinal epithelial cells. J. Immunol. 184:2305-2313. http://dx.doi.org/10.4049/jimmunol.0900021.
15. Sham HP, Yu EY, Gulen MF, Bhinder G, Stahl M, Chan JM, Brewster L, Morampudi V, Gibson DL, Hughes MR, McNagny KM, Li X, Vallance BA. 2013. SIGIRR, a negative regulator of TLR/IL-1R signalling promotes microbiota dependent resistance to colonization by enteric bacterial pathogens. PLoS Pathog. 9(8):e1003539. http://dx.doi.org/10.1371/journal.ppat.1003539.
16. Frantz AL, Rogier EW, Weber CR, Shen L, Cohen DA, Fenton LA, Bruno MEC, Katzel CS. 2012. Targeted deletion of MyD88 in intestinal epithelial cells results in compromised antibacterial immunity associated with downregulation of polymeric immunoglobulin receptor, mucin-2, and antibacterial peptides. Mucosal Immunol. 5:501-512. http://dx.doi.org/10.1038/mi.2012.23.
17. Chatfield SN, Strahan K, Pickard D, Charles IG, Hormaeche CE, Dougan G. 1992. Evaluation of Salmonella typhimurium strains harbouring defined mutations in htrA and aroA in the murine salmonellosis model. Microb. Pathog. 12:145-151. http://dx.doi.org/10.1016/0882-4010 (92)90117-7.
18. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, Russell SL, Vallance BA, Finlay BB. 2011. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect. Immun. 79:1536-1545. http://dx.doi.org/10.1128/IAI.01104-10.
19. Layton A, McKay L, Williams D, Garrett V, Gentry R, Sayler G. 2006. Development of bacteroides 16S rRNA gene TaqMan-based real-time PCR assays for estimation of total, human, and bovine fecal pollution in water. Appl. Environ. Microbiol. 72:4214-4224. http://dx.doi.org/10.1128/AEM.01036-05.
20. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. 2008. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett. Appl. Microbiol. 47:367-373. http://dx.doi.org/10.1111/j.1472-765X.2008.02408.x.
21. Bacchetti De Gregoris T, Aldred N, Clare AS, Burgess JG. 2011. Improvement of phylum-and class-specific primers for real-time PCR quantification of bacterial taxa. J. Microbiol. Methods 86:351-356. http://dx.doi.org/10.1016/j.mimet.2011.06.010.
22. Fierer N, Jackson JA, Vilgalys R, Jackson RB. 2005. Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 71:4117-4120. http://dx.doi.org/10.1128/AEM.71.7.4117-4120.2005.
23. Hirota SA, Ng J, Lueng A, Khajah M, Parhar K, Li Y, Lam V, Potentier MS, Ng K, Bawa M, McCafferty DM, Rioux KP, Ghosh S, Xavier RJ, Colgan SP, Tschopp J, Muruve D, MacDonald JA, Beck PL. 2011. NLRP3 inflammasome plays a key role in the regulation of intestinal homeostasis. Inflamm. Bowel Dis. 17:1359-1372. http://dx.doi.org/10.1002/ibd.21478.
24. Valdez Y, Grassl GA, Guttman JA, Coburn B, Gros P, Vallance BA, Finlay BB. 2009. Nramp1 drives an accelerated inflammatory response during Salmonella-induced colitis in mice. Cell Microbiol. 11:351-362. http://dx.doi.org/10.1111/j.1462-5822.2008.01258.x.
25. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M, Pfeffer K, Rüssman H, Hardt WD. 2003. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect. Immun. 71:2839-2858. http://dx.doi.org/10.1128/IAI.71.5.2839-2858.2003.
26. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, Ley R, Wakeland EK, Hooper LV. 2011. The antibacterial lectin RegIII-γ promotes the spatial segregation of microbiota and host in the intestine. Science 334:255-258. http://dx.doi.org/10.1126/science.1209791.
27. Hogan SP, Seidu L, Blanchard C, Groschwitz K, Mishra A, Karow ML, Ahrens R, Artis D, Murphy AJ, Valenzuela DM, Yanopoulos G, Rothenberg ME. 2006. Resistin-like molecule beta regulates innate colonic function: barrier integrity and inflammation susceptibility. J. Allergy Clin. Immunol. 118:257-268. http://dx.doi.org/10.1016/j.jaci.2006.04.039.
28. Zarepour M, Bhullar K, Montero M, Ma C, Huang T, Velcich A, Xia L, Vallance BA. 2013. The mucin Muc2 limits pathogen burdens and epithelial barrier dysfunction during Salmonella enterica serovar Typhimurium colitis. Infect. Immun. 81:3672-3683. http://dx.doi.org/10.1128/IAI.00854-13.
29. Melmed G, Thomas LS, Lee N, Tesfay SY, Lukasek K, Michelsen KS, Zhou Y, Hu B, Arditi M, Abreu MT. 2003. Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J. Immunol. 170:1406-1415. http://dx.doi.org/10.4049/jimmunol.170.3.1406.
30. Otte JM, Cario E, Podolsky DK. 2004. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126:1054-1070. http://dx.doi.org/10.1053/j.gastro.2004.01.007.
31. Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK. 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J. Immunol. 164:966-972. http://dx.doi.org/10.4049/jimmunol.164.2.966.