Goblet Cell Derived RELM-β Recruits CD4+ T Cells during Infectious Colitis to Promote Protective Intestinal Epithelial Cell Proliferation

PLoS Pathogens

Volumn 11, Issue 8, 2015, Pages

  Bergstrom, Kirk S B ^a,e   Morampudi, Vijay ^a   Chan, Justin M ^a   Bhinder, Ganive ^a   Lau, Jennifer ^a   Yang, Hyungjun ^a   Ma, Caixia ^a   Huang, Tina ^a   Ryz, Natasha ^a   Sham, Ho Pan ^a   Zarepour, Maryam ^a   Zaph, Colby ^b   Artis, David ^c   Nair, Meera ^d   Vallance, Bruce A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 22; RESISTIN; HORMONE; RETNLB PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; CD4 T LYMPHOCYTE; CELL MIGRATION ASSAY; CELL PROLIFERATION; CITROBACTER RODENTIUM; COLITIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FECES ANALYSIS; FLOW CYTOMETRY; GOBLET CELL; HOST RESISTANCE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CELL SEPARATION; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; INTESTINE MUCOSA; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SEPARATION; CITROBACTER RODENTIUM; COLITIS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GOBLET CELLS; HORMONES, ECTOPIC; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION;

EID: 84940765092     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005108     Document Type: Article

References (51)

1. Croxen MA, Finlay BB, Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2013;8:26–38.
2. Khan MA, Bouzari S, Ma C, Rosenberger CM, Bergstrom KS, Gibson DL, et al. Flagellin-dependent and-independent inflammatory responses following infection by Enteropathogenic Escherichia coli and Citrobacer rodentium. Infect Immun 2008;76:1410–1422. doi: 10.1128/IAI.01141-07 18227166
3. Michail SK, Halm DR, Abernathy F., Enteropathogenic Escherichia coli: stimulating neutrophil migration across a cultured intestinal epithelium without altering transpetihelial conductance. J Pediatr Gastroenterol Nutr 2003;36:253–260. 12548063
4. Savkovic SD, Koutsouris A, Hecht G, Activation of NF-κB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am J Physiol 1997;273:C1160–1167. 9357759
5. Savkovic SD, Koutsouris A, Hecht G, Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils. Infect Immun 1996;64:4480–4487 8890195
6. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S, Citrobacter rodentium of mice and man. Cell Microbiol 2005;7:1697–1706. 16309456
7. Mundy R, Girard F, FitzGerald AJ, Frankel G, Comparison of colonization dynamics and pathology of mice infected with enteropathogenic Escherichia coli, enterohaemorrhagic E. coli and Citrobacter rodentium. FEMS Microbiol Lett 2006;265:126–132. 17034412
8. Ryz NR, Patterson S, Zhang Y, Ma C, Huang T, Bhinder G, et al. Active vitamin D increases host susceptibility to Citrobacter rodentium induced colitis by suppressing mucosal Th17 responses. Am J Physiol Gastrointest Liver Physiol 2012;303:G1299–311. doi: 10.1152/ajpgi.00320.2012 23019194
9. Basu R, O'Quinn DB, Silberger DJ, Schoeb TR, Fouser L, Ouyang W, et al. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 2012;37:1061–75. doi: 10.1016/j.immuni.2012.08.024 23200827
10. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, Elson CO, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006;441:231–234. 16648837
11. Simmons CP, Clare S, Ghaem-Maghami M, Uren TK, Rankin J, Huett A, et al. Central role for B lymphocytes and CD4+ T cells in immunity to infection by the attaching and effacing pathogen Citrobacter rodentium. Infect Immun 2003;71:5077–86. 12933850
12. Bergstrom KS, Guttman JA, Rumi M, Ma C, Bouzari S, Khan MA, et al. Modulation of intestinal goblet cell function during infection by an attaching and effacing bacterial pathogen. Infect Immun 2008;76: 796–811. 17984203
13. Chan JM, Bhinder G, Sham HP, Ryz N, Huang T, Bergstrom KS, et al. CD4+ T cells drive goblet cell depletion during Citrobacter rodentium infection. Infect Immun 2013;81:4649–58. doi: 10.1128/IAI.00655-13 24101690
14. Paul G, Marchelletta RR, McCole DF, Barrett KE, Interferon-γ alters downstream signaling originating from epidermal growth factor receptor in intestinal epithelial cells: functional consequences for ion transport. J Biol Chem 2012;287:2144–2155. doi: 10.1074/jbc.M111.318139 22069319
15. O'Loughlin EV, Pang GP, Noltorp R, Koina C, Batey R, Clancy R, Interleukin 2 modulates ion secretion and cell proliferation in cultured human small intestinal enterocytes. Gut 2001;49:636–643. 11600465
16. Papapietro O, Teatero S, Thanabalasuriar A, Yuki KE, Diez E, Zhu L, et al. R-spondin 2 signalling mediates susceptiblity to fatal infecitous diarrhoea. Nat commun. 2013;4:1898. doi: 10.1038/ncomms2816 23695692
17. Medzhitov R, Damage control in host-pathogen interactions. Proc Natl Acad Sci USA 2009;106:15525–15526. doi: 10.1073/pnas.0908451106 19805209
18. Gibson DL, Ma C, Rosenberger CM, Bergstrom KS, Valdez Y, Huang JT, et al. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell Microbiol 2008;10:388–403. 17910742
19. Gibson DL, Montero M, Ropeleski MJ, Bergstrom KS, Ma C, Ghosh S, et al. Interleukin-11 reduces TLR4-induced colitis in TLR2-deficient mice and restores intestinal STAT3 signalling. Gastroenterology. 2010;139:1277–1288. doi: 10.1053/j.gastro.2010.06.057 20600022
20. Sham HP, Yu EY, Gulen MF, Bhinder G, Stahl M, Chan JM, et al. SIGIRR, a negative regulator of TLR/IL-1R signalling promotes Microbiota dependent resistance to colonization by enteric bacterial pathogens. PLoS Pathog 2013;9:e1003539. doi: 10.1371/journal.ppat.1003539 23950714
21. Kim YS, Ho SB, Intestinal Goblet Cells and Mucins in Health and Disease: Recent Insights and Progress. Curr Gastroenterol Rep. 2010;12:319–30. doi: 10.1007/s11894-010-0131-2 20703838
22. Johansson ME, Holmen Larsson JM, Hansson GC, The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci USA 2011;108 Suppl1:4659–4665.
23. Bergstrom KS, Kissoon-Singh V, Gibson DL, Ma C, Montero M, Sham HP, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog 2010;6:e1000902. doi: 10.1371/journal.ppat.1000902 20485566
24. Hogan SP, Seidu L, Blanchard C, Groschwitz K, Mishra A, Karow ML, et al. Resistin-like molecule beta regulates innate colonic function: barrier integrity and inflammation susceptibility. J Allergy Clin Immunol 2006;118:257–268. 16815164
25. Artis D, Wang ML, Keilbaugh SA, He W, Brenes M, Swain GP, et al. RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proc Natl Acad Sci USA 2004;101:13596–13600. 15340149
26. Rajala MW, Obici S, Scherer PE, Rossetti L, Adipose-derived resistin and gut-derived resistin-like molecule-beta selectively impair insulin action on glucose production. J Clin Invest 2003;111:225–230. 12531878
27. Steppan CM, Brown EJ, Wright CM, Bhat S, Banerjee RR, Dai CY, et al. A family of tissue-specific resistin-like molecules. Proc Natl Acad Sci USA 2001;98:502–506. 11209052
28. Hergert B, Grambow E, Butschkau A, Vollmar B, Effects of systemic pretreatment with CpG oligodeoxynucleotides on skin wound healing in mice. Wound Repair Regen 2013;21:723–9. doi: 10.1111/wrr.12084 23927054
29. Jang JC, Chen G, Wang SH, Barnes MA, Chung JI, Camberis M, et al. Macrophage-derived human resistin is induced in multiple helminth infections and promotes inflammatory monocytes and increased parasite burden. PLoS Pathog 2015;11:e1004579. doi: 10.1371/journal.ppat.1004579 25568944
30. He W, Wang ML, Jiang HQ, Steppan CM, Shin ME, Thurnheer MC, et al. Bacterial colonization leads to the colonic secretion of RELMbeta/FIZZ2, a novel goblet cell-specific protein. Gastroenterology 2003;125:1388–1397. 14598255
31. Barnes SL, Vidrich A, Wang ML, Wu GD, Cominelli F, Rivera-Nieves J, et al. Resistin-like molecule beta (RELMbeta/FIZZ2) is highly expressed in the ileum of SAMP1/YitFc mice and is associated with initiation of ileitis. J Immunol 2007;179:7012–7020. 17982092
32. McVay LD, Keilbaugh SA, Wong TMH, Kierstein S, Shin ME, Lehrke M, et al. Absence of bacterially induced RELMbeta reduces injury in the dextran sodium sulfate model of colitis. The Journal of Clinical Investigation 2006;116:2914–2923. 17024245
33. Nair MG, Guild KJ, Du Y, Zaph C, Yancopoulos GD, Valenzuela DM, et al. Goblet cell-derived resistin-like molecule beta augments CD4+ T cell production of IFN-gamma and infection-induced intestinal inflammation. J Immunol 2008;181:4709–4715. 18802073
34. Herbert DR, Yang JQ, Hogan SP, Groschwitz K, Khodoun M, Munitz A, et al. Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection. J Exp Med 2009;206:2947–2957. doi: 10.1084/jem.20091268 19995957
35. Bhinder G, Stahl M, Sham HP, Crowley SM, Morampudi V, Dalwadi U, et al. Intestinal epithelium-specific MyD88 signaling impacts host susceptibility to infectious colitis by promoting protective goblet cell and antimicrobial responses. Infect Immun 2014;82:3753–63. doi: 10.1128/IAI.02045-14 24958710
36. Scholzen T, Gerdes J, The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000;182:311–322. 10653597
37. Veitch AM, Kelly P, Zulu IS, Segal I, Farthing MJ, Tropical enteropathy: a T-cell-mediated crypt hyperplastic enteropathy. Eur J Gastroenterol Hepatol 2001;13:1175–1181. 11711773
38. Dickson BC, Streutker CJ, Chetty R, Coeliac disease: an update for pathologists. J Clin Pathol 2006;59:1008–1016. 17021129
39. Kunkel EJ, Butcher EC, Chemokines and the tissue-specific migration of lymphocytes. Immunity 2002;16:1–4. 11825560
40. Mishra A, Wang M, Schlotman J, Nikolaidis NM, DeBrosse CW, Karow ML, et al. Resistin-like molecule-beta is an allergen-induced cytokine with inflammatory and remodeling activity in the murine lung. Am J Physiol Lung Cell Mol Physiol 2007;293:L305–313. 17545488
41. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14:282–9. doi: 10.1038/nm1720 18264109
42. Krimi RB, Kotelevets L, Dubuquoy L, Plaisancié P, Walker F, Lehy T, et al. Resistin-like molecule β regulates intestinal mucous secretion and curtails TNBS-induced colitis in mice. Inflam Bowel Dis 2008;14:931–941.
43. McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, Knoop KA, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 2012;483:345–9. doi: 10.1038/nature10863 22422267
44. Vallance BA, Deng W, Knodler LA, Finlay BB, Mice lacking T and B Lymphocytes develop transient colitis and crypt hyperplasia yet suffer impaired bacterial clearance during Citrobacter rodentium infection. Infect Immun 2002;70:2070–2081. 11895973
45. Cliffe LJ, Humphreys NE, Lane TE, Potten CS, Booth C, Grencis RK, Accelerated intestinal epithelial cell turnover: a new mechanism of parasite expulsion. Science 2005;308:1463–5. 15933199
46. Schneider DS, Ayres JS, Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 2008;8:889–895. doi: 10.1038/nri2432 18927577
47. Shim E, Bang BR, Kang S, Ma J, Otsuka M, Kang J, et al. Activation of p38α in T cells regulates the intestinal host defense against attaching and effacing bacterial infections. J Immunol 2013;191:2764–2770. doi: 10.4049/jimmunol.1300908 23918973
48. Sonnenberg GF, Monticelli LA, Elloso MM, Fouser LA, Artis D, CD4+ lymphoid tissue inducer cells promote innate immunity in the gut. Immunity 2011;34:122–134. doi: 10.1016/j.immuni.2010.12.009 21194981
49. Osborne LC, Joyce KL, Alenghat T, Sonnenberg GF, Giacomin PR, Du Y, et al. Resistin-like molecule α promotes pathogenic Th17 cell responses and bacterial-induced intestinal inflammation. J Immunol 2013;190:2292–300. doi: 10.4049/jimmunol.1200706 23355735
50. Gibson DL, Ma C, Bergstrom KS, Huan JT, Man C, Vallance BA, 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 2008;10:618–631. 17979981
51. Wiles S, Dougan G, Frankel G, Emergence of a 'hyperinfectious' bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell Microbiol 2005;7:1163–1172. 16008583