Interleukin-13-mediated paneth cell degranulation and antimicrobial peptide release

Journal of Innate Immunity

Volumn 6, Issue 4, 2014, Pages 530-541

  Stockinger, Silvia ^a,b   Albers, Thorben ^a   Duerr, Claudia U ^a,e   Ménard, Sandrine ^c   Pütsep, Katrin ^d   Andersson, Mats ^d   Hornef, Mathias W ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^d KAROLINSKA INSTITUTE   (Sweden)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Antimicrobial peptide; Interleukin 13; Intestinal crypts; Intestine; Paneth cell

Indexed keywords

CARBACHOL; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 15; INTERLEUKIN 22; INTERLEUKIN 28; INTERLEUKIN 4; MURAMYL DIPEPTIDE; MUSCARINIC RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN KINASE B; STAT6 PROTEIN; ANTIMICROBIAL CATIONIC PEPTIDE; INTERLEUKIN 13 RECEPTOR; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; CPG OLIGODEOXYNUCLEOTIDE; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ANTIGEN RETRIEVAL; ANTIMICROBIAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DEGRANULATION; ENZYME PHOSPHORYLATION; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; INTESTINE FLORA; MASS SPECTROMETRY; MAST CELL; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANETH CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANIMAL; C3H MOUSE; CELL CULTURE; DRUG EFFECTS; GENETICS; IMMUNOLOGY; METABOLISM; MUCOSAL IMMUNITY; SIGNAL TRANSDUCTION; SMALL INTESTINE; UPREGULATION; HOMEOSTASIS; HOST RESISTANCE; OLIGOMERIZATION; PROTEIN SECRETION;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CARBACHOL; CELL DEGRANULATION; CELLS, CULTURED; IMMUNITY, MUCOSAL; INTERLEUKIN-13; INTERLEUKIN-4; INTESTINE, SMALL; MICE; MICE, INBRED C3H; PANETH CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, INTERLEUKIN-13; RECEPTORS, MUSCARINIC; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84902831916     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000357644     Document Type: Article

References (56)

1. Bevins CL, Salzman NH: Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011; 9: 356-368.
2. Selsted ME, Miller SI, Henschen AH, Ouel-lette AJ: Enteric defensins: antibiotic peptide components of intestinal host defense. J Cell Biol 1992; 118:929-936.
3. Ouellette AJ, Lualdi JC: A novel mouse gene family coding for cationic, cysteine-rich pep-tides: regulation in small intestine and cells of myeloid origin. J Biol Chem 1990; 265:9831-9837.
4. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, Ley R, Wakeland EK, Hooper LV: The antibacterial lectin RegIIIγ promotes the spatial segregation of microbiota and host in the intestine. Science 2011; 334:255-258.
5. Linzmeier RM, Ganz T: Human defensin gene copy number polymorphisms: comprehensive analysis of independent variation in α-and β-defensin regions at 8p22-p23. Ge-nomics 2005; 86:423-430.
6. Amid C, Rehaume LM, Brown KL, Gilbert JG, Dougan G, Hancock RE, Harrow JL: Manual annotation and analysis of the defensin gene cluster in the C57BL/6J mouse reference genome. BMC Genomics 2009; 10:606.
7. Andersson ML, Karlsson-Sjöberg JM, Pütsep KL: CRS-peptides: unique defense peptides of mouse Paneth cells. Mucosal Immunol 2012; 5:367-376.
8. Fernandez MI, Regnault B, Mulet C, Tanguy M, Jay P, Sansonetti PJ, Pédron T: Maturation of Paneth cells induces the refractory state of newborn mice to Shigella infection. J Immunol 2008; 180:4924-4930.
9. Wilson CL, Ouellette AJ, Satchell DP, Ayabe T, López-Boado YS, Stratman JL, Hultgren SJ, Matrisian LM, Parks WC: Regulation of intestinal α-defensin activation by the metallopro-teinase matrilysin in innate host defense. Science 1999; 286:113-117.
10. Salzman NH, Ghosh D, Huttner KM, Pater-son Y, Bevins CL: Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 2003; 422: 522-526.
11. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjöberg J, Amir E, Teggatz P, Barman M, Hayward M, Eastwood D, Stoel M, Zhou Y, Sodergren E, Weinstock GM, Bevins CL, Williams CB, Bos NA: Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010; 11:76-83.
12. Vaishnava S, Behrendt CL, Ismail AS, Eck-mann L, Hooper LV: Paneth cells directly sense gut commensals and maintain homeo-stasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 2008; 105: 20858-20863.
13. Wehkamp J, Harder J, Weichenthal M, Schwab M, Schäffeler E, Schlee M, Herrlinger KR, Stallmach A, Noack F, Fritz P, Schröder JM, Bevins CL, Fellermann K, Stange EF: NOD2 (CARD15) mutations in Crohn's disease are associated with diminished mucosal α-defensin expression. Gut 2004; 53:1658-1664.
14. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaef-feler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr, Fellermann K, Ganz T, Stange EF, Bevins CL: Reduced Paneth cell α-defensins in ileal Crohn's disease. Proc Natl Acad Sci USA 2005; 102:18129-18134.
15. Wehkamp J, Wang G, Kübler I, Nuding S, Gregorieff A, Schnabel A, Kays RJ, Feller-mann K, Burk O, Schwab M, Clevers H, Bev-ins CL, Stange EF: The Paneth cell α-defensin deficiency of ileal Crohn's disease is linked to Wnt/Tcf-4. J Immunol 2007; 179:3109-3118.
16. Bevins CL, Stange EF, Wehkamp J: Decreased Paneth cell defensin expression in ileal Crohn's disease is independent of inflammation, but linked to the NOD2 1007fs genotype. Gut 2009; 58:882-883.
17. Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J, Lennerz JK, Kishi C, Kc W, Carrero JA, Hunt S, Stone CD, Brunt EM, Xavier RJ, Sleckman BP, Li E, Mizushima N, Stappen-beck TS, Virgin HW 4th: A key role for au-tophagy and the autophagy gene Atg16l1 in mouse and human intestinal Paneth cells. Nature 2008; 456:259-263.
18. Günther C, Martini E, Wittkopf N, Amann K, Weigmann B, Neumann H, Waldner MJ, He-drick SM, Tenzer S, Neurath MF, Becker C: Caspase-8 regulates TNF-α-induced epithelial necroptosis and terminal ileitis. Nature 2011; 477:335-339.
19. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis EE, Higgins DE, Schreiber S, Glimcher LH, Blumberg RS: XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008; 134: 743-756.
20. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ: Secretion of micro-bicidal α-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 2000; 1: 113-118.
21. Menendez A, Willing BP, Montero M, Wlo-darska M, So CC, Bhinder G, Vallance BA, Finlay BB: Bacterial stimulation of the TLR-MyD88 pathway modulates the homeostatic expression of ileal Paneth cell α-defensins. J Innate Immun 2013; 5:39-49.
22. Satoh Y: Atropine inhibits the degranulation of Paneth cells in ex-germ-free mice. Cell Tissue Res 1988; 253:397-402.
23. Rumio C, Sommariva M, Sfondrini L, Palazzo M, Morelli D, Viganò L, De Cecco L, Ta-gliabue E, Balsari A: Induction of Paneth cell degranulation by orally administered Tolllike receptor ligands. J Cell Physiol 2012; 227: 1107-1113.
24. Satoh Y, Habara Y, Ono K, Kanno T: Carba-mylcholine-and catecholamine-induced in-tracellular calcium dynamics of epithelial cells in mouse ileal crypts. Gastroenterology 1995; 108:1345-1356.
25. Tanabe H, Ayabe T, Bainbridge B, Guina T, Ernst RK, Darveau RP, Miller SI, Ouellette AJ: Mouse Paneth cell secretory responses to cell surface glycolipids of virulent and attenuated pathogenic bacteria. Infect Immun 2005; 73: 2312-2320.
26. Rumio C, Besusso D, Palazzo M, Selleri S, Sfondrini L, Dubini F, Ménard S, Balsari A: Degranulation of Paneth cells via Toll-like receptor 9. Am J Pathol 2004; 165:373-381.
27. Lotz M, Gütle D, Walther S, Ménard S, Bog-dan C, Hornef MW: Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med 2006; 203:973-984.
28. Putsep K, Axelsson LG, Boman A, Midtvedt T, Normark S, Boman HG, Andersson M: Germ-free and colonized mice generate the same products from enteric prodefensins. J Biol Chem 2000; 275:40478-40482.
29. Karlsson J, Pütsep K, Chu H, Kays RJ, Bevins CL, Andersson M: Regional variations in Pa-neth cell antimicrobial peptide expression along the mouse intestinal tract. BMC Immunol 2008; 9:37.
30. Urban JF Jr, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M, Fin-kelman FD: IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasil-iensis. Immunity 1998; 8:255-264.
31. Pott J, Mahlakõiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, Staeheli P, Hornef MW: IFN-a; determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci USA 2011; 108:7944-7949.
32. + innate lymphoid cells control intestinal inflammation by recruiting inflammatory monocytes. Immunity 2012; 37:108-121.
33. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, Ouyang W: Inter-leukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14:282-289.
34. Linge HM, Collin M, Nordenfelt P, Mörgelin M, Malmsten M, Egesten A: The human CXC chemokine granulocyte chemotactic protein 2 (GCP-2)/CXCL6 possesses membrane-disrupting properties and is antibacterial. Antimicrob Agents Chemother 2008; 52: 2599-2607.
35. Lotz M, König T, Ménard S, Gütle D, Bogdan C, Hornef MW: Cytokine-mediated control of lipopolysaccharide-induced activation of small intestinal epithelial cells. Immunology 2007; 122:306-315.
36. Ceponis PJ, Botelho F, Richards CD, McKay DM: Interleukins 4 and 13 increase intestinal epithelial permeability by a phosphatidylino-sitol 3-kinase pathway. Lack of evidence for STAT 6 involvement. J Biol Chem 2000; 275: 29132-29137.
37. Ali K, Camps M, Pearce WP, Ji H, Rückle T, Kuehn N, Pasquali C, Chabert C, Rommel C, Vanhaesebroeck B: Isoform-specific functions of phosphoinositide 3-kinases: p110δ but not p110γ promotes optimal allergic responses in vivo. J Immunol 2008; 180:2538-2544.
38. Pigeau GM, Kolic J, Ball BJ, Hoppa MB, Wang YW, Rückle T, Woo M, Manning Fox JE, MacDonald PE: Insulin granule recruitment and exocytosis is dependent on p110γ in in-sulinoma and human β-cells. Diabetes 2009; 58:2084-2092.
39. Endo D, Gon Y, Nunomura S, Yamashita K, Hashimoto S, Ra C: PI3Kγ differentially regulates FcepsilonRI-mediated degranulation and migration of mast cells by and toward antigen. Int Arch Allergy Immunol 2009; 149: 66-72.
40. Wynn TA: IL-13 effector functions. Annu Rev Immunol 2003; 21:425-456.
41. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H: Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011; 469:415-418.
42. Kobayashi KS, Chamaillard M, Ogura Y, Henegariu O, Inohara N, Nuñez G, Flavell RA: Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005; 307:731-734.
43. Petnicki-Ocwieja T, Hrncir T, Liu YJ, Biswas A, Hudcovic T, Tlaskalova-Hogenova H, Ko-bayashi KS: Nod2 is required for the regulation of commensal microbiota in the intestine. Proc Natl Acad Sci USA 2009; 106: 15813-15818.
44. Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM: Type 2 immunity is controlled by IL-4/IL-13 expression in hemato-poietic non-eosinophil cells of the innate immune system. J Exp Med 2006; 203:1435-1446.
45. Mjösberg JM, Trifari S, Crellin NK, Peters CP, van Drunen CM, Piet B, Fokkens WJ, Cupedo T, Spits H: Human IL-25-and IL-33-respon-sive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161. Nat Immunol 2011; 12:1055-1062.
46. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, Langford TK, Bucks C, Kane CM, Fallon PG, Pannell R, Jolin HE, McKenzie AN: Nuo-cytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 2010; 464:1367-1370.
47. Mannon P, Reinisch W: Interleukin 13 and its role in gut defence and inflammation. Gut 2012; 61:1765-1773.
48. Kamal M, Wakelin D, Ouellette AJ, Smith A, Podolsky DK, Mahida YR: Mucosal T cells regulate Paneth and intermediate cell numbers in the small intestine of T. spiralis-infected mice. Clin Exp Immunol 2001; 126:117-125.
49. Kamal M, Dehlawi MS, Brunet LR, Wakelin D: Paneth and intermediate cell hyperplasia induced in mice by helminth infections. Para-sitology 2002; 125:275-281.
50. Dehlawi MS, Mahida YR, Hughes K, Wakelin D: Effects of Trichinella spiralis infection on intestinal pathology in mice lacking interleu-kin-4 (IL-4) or intestinal trefoil factor (ITF/TFF3). Parasitol Int 2006; 55:207-211.
51. Steenwinckel V, Louahed J, Lemaire MM, Sommereyns C, Warnier G, McKenzie A, Brombacher F, Van Snick J, Renauld JC: IL-9 promotes IL-13-dependent Paneth cell hy-perplasia and up-regulation of innate immunity mediators in intestinal mucosa. J Immunol 2009; 182:4737-4743.
52. Meyer-Hoffert U, Hornef MW, Henriques-Normark B, Axelsson LG, Midtvedt T, Pütsep K, Andersson M: Secreted enteric antimicrobial activity localises to the mucus surface layer. Gut 2008; 57:764-771.
53. H17 cells express a functional IL-13 receptor and IL-13 attenuates IL-17A production. J Allergy Clin Immunol 2011; 127:1006-1013.
54. Reddy A, Fried B: The use of Trichuris suis and other helminth therapies to treat Crohn's disease. Parasitol Res 2007; 100:921-927.
55. Grzeskowiak Ł, Collado MC, Mangani C, Maleta K, Laitinen K, Ashorn P, Isolauri E, Sal-minen S: Distinct gut microbiota in southeastern African and northern European infants. J Pediatr Gastroenterol Nutr 2012; 54:812-816.
56. Okada H, Kuhn C, Feillet H, Bach JF: The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol 2010; 160:1-9.