Characterization of gliadin-specific Th17 cells from the mucosa of celiac disease patients

American Journal of Gastroenterology

Volumn 106, Issue 3, 2011, Pages 528-538

  Fernández, Silvia ^a   Molina, Ignacio J ^b   Romero, Pilar ^a   González, Rafael ^c   Pẽa, José ^a,c   Sánchez, Francisco ^c   Reynoso, Fernanda R ^c   Pérez Navero, Juan L ^c   Estevez, Orlando ^c   Ortega, Consuelo ^a   Santamaría, Manuel ^a,c  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD161 ANTIGEN; CD45RO ANTIGEN; CHEMOKINE RECEPTOR CCR6; GLIADIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23 RECEPTOR; RETINOID RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

ADOLESCENT; ARTICLE; CD4+ T LYMPHOCYTE; CELIAC DISEASE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DUODENUM; DUODENUM BIOPSY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRESCHOOL CHILD; PRIORITY JOURNAL; TH17 CELL; UPREGULATION;

ADOLESCENT; CELIAC DISEASE; CHILD; CHILD, PRESCHOOL; CYTOKINES; FEMALE; FLOW CYTOMETRY; GLIADIN; HUMANS; IMMUNOASSAY; INFLAMMATION; INTERFERON REGULATORY FACTORS; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKINS; INTESTINAL MUCOSA; MALE; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; POLYMERASE CHAIN REACTION; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 79952364000     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2010.465     Document Type: Article

References (51)

1. Green PH, Cellier C. Celiac disease. N Engl J Med 2007;357:1731-43.
2. Jabri B, Sollid LM. Mechanisms of disease: immunopathogenesis of celiac disease. Nat Clin Pract Gastroenterol Hepatol 2006;3:516-25. (Pubitemid 44322763)
3. Monteleone I, Monteleone G, Del Vecchio Blanco G et al. Regulation of the T helper cell type 1 transcription factor T-bet in coeliac disease mucosa. Gut 2004;53:1090-5. (Pubitemid 38961960)
4. Frisullo G, Nociti V, Iorio R et al. T-bet and pSTAT-1 expression in PBMC from coeliac disease patients: new markers of disease activity. Clin Exp Immunol 2009;158:106-14.
5. Jabri B, Meresse B. NKG2 receptor-mediated regulation of effector CTL functions in the human tissue microenvironment. Curr Top Microbiol Immunol 2006;298:139-56. (Pubitemid 41491726)
6. Gianfrani C, Levings MK, Sartirana C et al. Gliadin-specific type 1 regulatory T cells from the intestinal mucosa of treated celiac patients inhibit pathogenic T cells. J Immunol 2006;177:4178-86. (Pubitemid 44359953)
7. Forsberg G, Hernell O, Melgar S et al. Paradoxical coexpression of proin- flammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology 2002;123:667-78. (Pubitemid 34977072)
8. Forsberg G, Hernell O, Hammarstrom S et al. Concomitant increase of IL-10 and pro-inflammatory cytokines in intraepithelial lymphocyte subsets in celiac disease. Int Immunol 2007;19:993-1001. (Pubitemid 47386924)
9. Korn T, Mitsdoerffer M, Kuchroo VK. Immunological basis for the development of tissue inflammation and organ-specific autoimmunity in animal models of multiple sclerosis. Results Probl Cell Differ 2010;51:43-74.
10. Korn T, Oukka M, Kuchroo V et al. Th17 cells: effector T cells with inflammatory properties. Semin Immunol 2007;19:362-71. (Pubitemid 351274046)
11. Turner JE, Paust HJ, Steinmetz OM et al. CCR6 recruits regulatory T cells and Th17 cells to the kidney in glomerulonephritis. J Am Soc Nephrol 2010;21:974-85.
12. Ivanov II, McKenzie BS, Zhou L et al. The orphan nuclear receptor RORgammat directs the Differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006;126:1121-33. (Pubitemid 44380299)
13. Wurster AL, Rodgers VL, Satoskar AR et al. Interleukin 21 is a T helper (Th) cell 2 cytokine that specifically inhibits the Differentiation of naive Thcells into interferon gamma-producing Th1 cells. J Exp Med 2002;196:969-77.
14. Wolk K, Kunz S, Witte E et al. IL-22 increases the innate immunity of tissues . Immunity 2004;21:241-54. (Pubitemid 39094053)
15. Zheng Y, Valdez PA, Danilenko DM et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008;14:282-9. (Pubitemid 351347912)
16. Volpe E, Servant N, Zollinger R et al. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nat Immunol 2008;9:650-7. (Pubitemid 351712635)
17. Izcue A, Coombes JL, Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol 2009;27:313-38.
18. Bhagat G, Naiyer AJ, Shah JG et al. Small intestinal CD8TCRgammadeltaNKG2A intraepithelial lymphocytes have attributes of regulatory cells in patients with celiac disease. J Clin Invest 2008;118:281-93.
19. Shull MM, Ormsby I, Kier AB et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992;359:693-9.
20. Powrie F, Carlino J, Leach MW et al. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med 1996;183:2669-74.
21. Korn T, Bettelli E, Oukka M et al. IL-17 and Th17 Cells. Annu Rev Immunol 2009;27:485-517.
22. Ortega C, Fernandez AS, Carrillo JM et al. IL-17-producing CD8+ T lymphocytes from psoriasis skin plaques are cytotoxic effector cells that secrete Th 17-related cytokines. J Leukoc Biol 2009;86:435-43.
23. Castellanos-Rubio A, Santin I, Irastorza I et al. TH17 (and TH1) signatures of intestinal biopsies of CD patients in response to gliadin. Autoimmunity 2009;42:69-73.
24. Monteleone I, Sarra M, Del Vecchio Blanco G et al. Characterization of IL- 17A-producing cells in celiac disease mucosa. J Immunol 2010;184:2211-8.
25. Jabri B, Sollid LM. Tissue-mediated control of immunopathology in coeliac disease. Nat Rev Immunol 2009;9:858-70.
26. Nilsen EM, Jahnsen FL, Lundin KE et al. Gluten induces an intestinal cytokine response strongly dominated by interferon gamma in patients with celiac disease. Gastroenterology 1998;115:551-63. (Pubitemid 28397290)
27. Kan SH, Mancini G, Gallagher G. Identification and characterization of multiple splice forms of the human interleukin-23 receptor alpha chain in mitogen-activated leukocytes. Genes Immun 2008;9:631-9.
28. Cosmi L, De Palma R, Santarlasci V et al. Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor. J Exp Med 2008;205:1903-16.
29. Awasthi A, Riol-Blanco L, Jager A et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol 2009;182:5904-8.
30. Bodd M, Raki M, Tollefsen S et al. HLA-DQ2-restricted gluten-reactive T cells produce IL-21 but not IL-17 or IL-22. Mucosal Immunol 2010;3:594-601.
31. Molberg O, McAdam S, Lundin KE et al. T cells from celiac disease lesions recognize gliadin epitopes deamidated in situ by endogenous tissue transglutaminase . Eur J Immunol 2001;31:1317-23. (Pubitemid 32454680)
32. Ciccocioppo R, Finamore A, Mengheri E et al. Isolation and characterization of circulating tissue transglutaminase-specific T cells in coeliac disease. Int J Immunopathol Pharmacol 2010;23:179-91.
33. Brustle A, Heink S, Huber M et al. The development of inflammatory T(H)- 17 cells requires interferon-regulatory factor 4. Nat Immunol 2007;8:958-66. (Pubitemid 47300010)
34. Liang SC, Tan XY, Luxenberg DP et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006;203:2271-9. (Pubitemid 44498362)
35. Afzali B, Mitchell P, Lechler RI et al. Translational mini-review series on Th 17 cells: induction of interleukin-17 production by regulatory T cells. Clin Exp Immunol 2009;159:120-30.
36. Weaver CT, Hatton RD. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat Rev Immunol 2009;9:883-9.
37. Fina D, Sarra M, Caruso R et al. Interleukin 21 contributes to the mucosal T helper cell type 1 response in coeliac disease. Gut 2008;57:887-92. (Pubitemid 351919521)
38. Sanjabi S, Zenewicz LA, Kamanaka M et al. Anti-inflammatory and proinflammatory roles of TGF-beta, IL-10, and IL-22 in immunity and autoimmunity . Curr Opin Pharmacol 2009;9:447-53.
39. Weiss B, Wolk K, Grunberg BH et al. Cloning of murine IL-22 receptor alpha 2 and comparison with its human counterpart. Genes Immun 2004;5:330-6. (Pubitemid 39139758)
40. Zenewicz LA, Yancopoulos GD, Valenzuela DM et al. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007;27:647-59. (Pubitemid 47615503)
41. Sugimoto K, Ogawa A, Mizoguchi E et al. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 2008;118:534-44. (Pubitemid 351206544)
42. Zenewicz LA, Yancopoulos GD, Valenzuela DM et al. Innate and adaptive interleukin-22 protects mice from inflammatory bowel disease. Immunity 2008;29:947-57.
43. Chang H, Hanawa H, Liu H et al. Hydrodynamic-based delivery of an interleukin-22-Ig fusion gene ameliorates experimental autoimmune myocarditis in rats. J Immunol 2006;177:3635-43. (Pubitemid 44359895)
44. Wolk K, Witte E, Hoffmann U et al. IL-22 induces lipopolysaccharide- binding protein in hepatocytes: a potential systemic role of IL-22 in Crohn's disease. J Immunol 2007;178:5973-81. (Pubitemid 46674395)
45. O ' Connor W Jr, Kamanaka M, Booth CJ et al. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat Immunol 2009;10:603-9.
46. Nam JS, Terabe M, Kang MJ et al. Transforming growth factor beta subverts the immune system into directly promoting tumor growth through interleukin- 17. Cancer Res 2008;68:3915-23.
47. Benahmed M, Meresse B, Arnulf B et al. Inhibition of TGF-beta signaling by IL-15: a new role for IL-15 in the loss of immune homeostasis in celiac disease. Gastroenterology 2007;132:994-1008. (Pubitemid 46440858)
48. Ayyoub M, Deknuydt F, Raimbaud I et al. Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage- specific transcription factor RORgamma t. Proc Natl Acad Sci USA 2009;106:8635-40.
49. Leveque L, Deknuydt F, Bioley G et al. Interleukin 2-mediated conversion of ovarian cancer-associated CD4+ regulatory T cells into proinflammatory interleukin 17-producing helper T cells. J Immunother 2009;32:101-8.
50. O ' Connor W Jr, Zenewicz LA, Flavell RA. The dual nature of T(H) 17 cells shift ing the focus to function. Nat Immunol 2010;11:471-6.
51. Cosmi L, Maggi L, Santarlasci V et al. Identification of a novel subset of human circulating memory CD4(+) T cells that produce both IL-17A and IL-4. J Allergy Clin Immunol 2010;125:222-30.