In vitro evaluation of intestinal epithelial TLR activation in preventing food allergic responses

Clinical Immunology

Volumn 154, Issue 2, 2014, Pages 91-99

  de Kivit, Sander ^a   Tobin, Mary C ^a   DeMeo, Mark T ^a   Fox, Susan ^a   Garssen, Johan ^b,c   Forsyth, Christopher B ^a   Keshavarzian, Ali ^a,b   Landay, Alan L ^a,b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c Nutricia Nederland   (Netherlands)

Author keywords

Cytokines; ; Food allergy; ; Intestinal epithelial cells; ; PBMC; ; Toll like receptors

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; FOOD ALLERGEN; GAMMA INTERFERON; IMMUNOGLOBULIN E; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 6; INTERLEUKIN 8; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC REACTION; ARTICLE; ATOPY; CELL ACTIVATION; COCULTURE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; EFFECTOR CELL; EGG; FOOD ALLERGY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; MICROENVIRONMENT; MILK; MONOLAYER CULTURE; PEANUT; PERIPHERAL BLOOD MONONUCLEAR CELL; PERMEABILITY BARRIER; PRIORITY JOURNAL; TH1 TH2 BALANCE;

CYTOKINES;; FOOD ALLERGY;; INTESTINAL EPITHELIAL CELLS;; PBMC;; TOLL-LIKE RECEPTORS;

ADULT; AGED; CELL LINE, TUMOR; COCULTURE TECHNIQUES; EPITHELIAL CELLS; FEMALE; FOOD HYPERSENSITIVITY; GENE EXPRESSION REGULATION; HUMANS; INTESTINAL MUCOSA; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; TOLL-LIKE RECEPTORS; YOUNG ADULT;

EID: 84905247909     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2014.07.002     Document Type: Article

References (48)

1. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., Belkaid Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 2007, 204:1775-1785.
2. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 2007, 204:1757-1764.
3. + dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008, 205:2139-2149.
4. Noval Rivas M., Burton O.T., Wise P., Zhang Y.Q., Hobson S.A., Garcia Lloret M., Chehoud C., Kuczynski J., DeSantis T., Warrington J., Hyde E.R., Petrosino J.F., Gerber G.K., Bry L., Oettgen H.C., Mazmanian S.K., Chatila T.A. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J. Allergy Clin. Immunol. 2013, 131:201-212.
5. Bjorksten B., Sepp E., Julge K., Voor T., Mikelsaar M. Allergy development and the intestinal microflora during the first year of life. J. Allergy Clin. Immunol. 2001, 108:516-520.
6. Murray C.S., Tannock G.W., Simon M.A., Harmsen H.J., Welling G.W., Custovic A., Woodcock A. Fecal microbiota in sensitized wheezy and non-sensitized non-wheezy children: a nested case-control study. Clin. Exp. Allergy 2005, 35:741-745.
7. Penders J., Thijs C., van den Brandt P.A., Kummeling I., Snijders B., Stelma F., Adams H., van Ree R., Stobberingh E.E. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut 2007, 56:661-667.
8. Ling Z., Li Z., Liu X., Cheng Y., Luo Y., Tong X., Yuan L., Wang Y., Sun J., Li L., Xiang C. Altered fecal microbiota composition associated with food allergy in infants. Appl. Environ. Microbiol. 2014, 80:2546-2554.
9. de Kivit S., Tobin M.C., Forsyth C.B., Keshavarzian A., Landay A.L. Regulation of intestinal immune responses through TLR activation: implications for pro- and prebiotics. Front. Immunol. 2014, 5:60.
10. Cario E., Gerken G., Podolsky D.K. Toll-like receptor 2 enhances ZO-1-associated intestinal epithelial barrier integrity via protein kinase C. Gastroenterology 2004, 127:224-238.
11. O'Hara J.R., Feener T.D., Fischer C.D., Buret A.G. Campylobacter jejuni disrupts protective Toll-like receptor 9 signaling in colonic epithelial cells and increases the severity of dextran sulfate sodium-induced colitis in mice. Infect. Immun. 2012, 80:1563-1571.
12. Lee J., Mo J.H., Katakura K., Alkalay I., Rucker A.N., Liu Y.T., Lee H.K., Shen C., Cojocaru G., Shenouda S., Kagnoff M., Eckmann L., Ben-Neriah Y., Raz E. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell Biol. 2006, 8:1327-1336.
13. h1-polarized regulatory or inflammatory type effector response in vitro. Immunobiology 2011, 216:518-527.
14. Li X., Wang C., Nie J., Lv D., Wang T., Xu Y. Toll-like receptor 4 increases intestinal permeability through up-regulation of membrane PKC activity in alcoholic steatohepatitis. Alcohol 2013, 47:459-465.
15. Frolova L., Drastich P., Rossmann P., Klimesova K., Tlaskalova-Hogenova H. Expression of Toll-like receptor 2 (TLR2), TLR4, and CD14 in biopsy samples of patients with inflammatory bowel diseases: upregulated expression of TLR2 in terminal ileum of patients with ulcerative colitis. J. Histochem. Cytochem. 2008, 56:267-274.
16. Cario E., Podolsky D.K. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 2000, 68:7010-7017.
17. Kalliomaki M., Satokari R., Lahteenoja H., Vahamiko S., Gronlund J., Routi T., Salminen S. Expression of microbiota, Toll-like receptors, and their regulators in the small intestinal mucosa in celiac disease. J. Pediatr. Gastroenterol. Nutr. 2012, 54:727-732.
18. Prescott S.L., Noakes P., Chow B.W., Breckler L., Thornton C.A., Hollams E.M., Ali M., van den Biggelaar A.H., Tulic M.K. Presymptomatic differences in Toll-like receptor function in infants who have allergy. J. Allergy Clin. Immunol. 2008, 122:391-399. (399 e1-5).
19. Westerholm-Ormio M., Vaarala O., Tiittanen M., Savilahti E. Infiltration of Foxp3- and Toll-like receptor-4-positive cells in the intestines of children with food allergy. J. Pediatr. Gastroenterol. Nutr. 2010, 50:367-376.
20. Pochard P., Vickery B., Berin M.C., Grishin A., Sampson H.A., Caplan M., Bottomly K. Targeting Toll-like receptors on dendritic cells modifies the T(H)2 response to peanut allergens in vitro. J. Allergy Clin. Immunol. 2010, 126:92-97. (e5).
21. h2-response in BALB/c mice. Eur. J. Pharm. Biopharm. 2013, 85:656-664.
22. Zhong Y., Huang J., Tang W., Chen B., Cai W. Effects of probiotics, probiotic DNA and the CpG oligodeoxynucleotides on ovalbumin-sensitized Brown-Norway rats via TLR9/NF-kappaB pathway. FEMS Immunol. Med. Microbiol. 2012, 66:71-82.
23. h1 responses to peanut antigens: modulation of sensitization and utility in a truncated immunotherapy regimen in mice. Mol. Nutr. Food Res. 2013, 57:906-915.
24. Zhu F.G., Kandimalla E.R., Yu D., Agrawal S. Oral administration of a synthetic agonist of Toll-like receptor 9 potently modulates peanut-induced allergy in mice. J. Allergy Clin. Immunol. 2007, 120:631-637.
25. Jarvinen K.M., Konstantinou G.N., Pilapil M., Arrieta M.C., Noone S., Sampson H.A., Meddings J., Nowak-Wegrzyn A. Intestinal permeability in children with food allergy on specific elimination diets. Pediatr. Allergy Immunol. 2013, 24:589-595.
26. Ventura M.T., Polimeno L., Amoruso A.C., Gatti F., Annoscia E., Marinaro M., Di Leo E., Matino M.G., Buquicchio R., Bonini S., Tursi A., Francavilla A. Intestinal permeability in patients with adverse reactions to food. Dig. Liver Dis. 2006, 38:732-736.
27. Cueto-Sola M., Bailon E., Utrilla P., Rodriguez-Ruiz J., Garrido-Mesa N., Zarzuelo A., Xaus J., Galvez J., Comalada M. Active colitis exacerbates immune response to internalized food antigens in mice. Int. Arch. Allergy Immunol. 2013, 162:214-224.
28. Turcanu V., Maleki S.J., Lack G. Characterization of lymphocyte responses to peanuts in normal children, peanut-allergic children, and allergic children who acquired tolerance to peanuts. J. Clin. Invest. 2003, 111:1065-1072.
29. h2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005, 129:550-564.
30. Prasad S., Mingrino R., Kaukinen K., Hayes K.L., Powell R.M., MacDonald T.T., Collins J.E. Inflammatory processes have differential effects on claudins 2, 3 and 4 in colonic epithelial cells. Lab. Invest. 2005, 85:1139-1162.
31. Liu X., Yang G., Geng X.R., Cao Y., Li N., Ma L., Chen S., Yang P.C., Liu Z. Microbial products induce claudin-2 to compromise gut epithelial barrier function. PLoS One 2013, 8:e68547.
32. Abreu M.T., Arnold E.T., Thomas L.S., Gonsky R., Zhou Y., Hu B., Arditi M. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J. Biol. Chem. 2002, 277:20431-20437.
33. Singh J.C., Cruickshank S.M., Newton D.J., Wakenshaw L., Graham A., Lan J., Lodge J.P., Felsburg P.J., Carding S.R. Toll-like receptor-mediated responses of primary intestinal epithelial cells during the development of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288:G514-G524.
34. Ewaschuk J.B., Backer J.L., Churchill T.A., Obermeier F., Krause D.O., Madsen K.L. Surface expression of Toll-like receptor 9 is upregulated on intestinal epithelial cells in response to pathogenic bacterial DNA. Infect. Immun. 2007, 75:2572-2579.
35. Sodhi C., Levy R., Gill R., Neal M.D., Richardson W., Branca M., Russo A., Prindle T., Billiar T.R., Hackam D.J. DNA attenuates enterocyte Toll-like receptor 4-mediated intestinal mucosal injury after remote trauma. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G862-G873.
36. Patel R.M., Myers L.S., Kurundkar A.R., Maheshwari A., Nusrat A., Lin P.W. Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am. J. Pathol. 2012, 180:626-635.
37. Salvati V.M., Mazzarella G., Gianfrani C., Levings M.K., Stefanile R., De Giulio B., Iaquinto G., Giardullo N., Auricchio S., Roncarolo M.G., Troncone R. Recombinant human interleukin 10 suppresses gliadin dependent T cell activation in ex vivo cultured coeliac intestinal mucosa. Gut 2005, 54:46-53.
38. Cheng J., Kalliomaki M., Heilig H.G., Palva A., Lahteenoja H., de Vos W.M., Salojarvi J., Satokari R. Duodenal microbiota composition and mucosal homeostasis in pediatric celiac disease. BMC Gastroenterol. 2013, 13:113.
39. Bouladoux N., Hall J.A., Grainger J.R., dos Santos L.M., Kann M.G., Nagarajan V., Verthelyi D., Belkaid Y. Regulatory role of suppressive motifs from commensal DNA. Mucosal Immunol. 2012, 5:623-634.
40. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., Akira S. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
41. Campeau J.L., Salim S.Y., Albert E.J., Hotte N., Madsen K.L. Intestinal epithelial cells modulate antigen-presenting cell responses to bacterial DNA. Infect. Immun. 2012, 80:2632-2644.
42. Kant R., de Vos W.M., Palva A., Satokari R. Immunostimulatory CpG motifs in the genomes of gut bacteria and their role in human health and disease. J. Med. Microbiol. 2014, 63:293-308.
43. Ghadimi D., Vrese M., Heller K.J., Schrezenmeir J. Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integrity of polarized intestinal epithelial cells. Inflamm. Bowel Dis. 2010, 16:410-427.
44. de Kivit S., Kraneveld A.D., Knippels L.M., van Kooyk Y., Garssen J., Willemsen L.E. Intestinal epithelium-derived galectin-9 is involved in the immunomodulating effects of nondigestible oligosaccharides. J. Innate Immun. 2013, 5:625-638.
45. Iliev I.D., Tohno M., Kurosaki D., Shimosato T., He F., Hosoda M., Saito T., Kitazawa H. Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from Lactobacillus rhamnosus GG DNA potentially suppresses OVA-specific IgE production in mice. Scand. J. Immunol. 2008, 67:370-376.
46. h2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunobiology 2008, 213:677-692.
47. Lee W.I., Yao T.C., Yeh K.W., Chen L.C., Ou L.S., Huang J.L. Stronger Toll-like receptor 1/2, 4, and 7/8 but less 9 responses in peripheral blood mononuclear cells in non-infectious exacerbated asthmatic children. Immunobiology 2013, 218:192-200.
48. Bonnegarde-Bernard A., Jee J., Fial M.J., Aeffner F., Cormet-Boyaka E., Davis I.C., Lin M., Tome D., Karin M., Sun Y., Boyaka P.N. IKKbeta in intestinal epithelial cells regulates allergen-specific IgA and allergic inflammation at distant mucosal sites. Mucosal Immunol. 2014, 7:257-267.