Microscopic colitis patients demonstrate a mixed Th17/Tc17 and Th1/Tc1 mucosal cytokine profile

Molecular Immunology

Volumn 55, Issue 3-4, 2013, Pages 355-364

  Kumawat, Ashok Kumar ^a   Strid, Hilja ^a,b   Tysk, Curt ^a,b   Bohr, Johan ^a,b   Hörnquist, Elisabeth Hultgren ^a  

^a ÖREBRO UNIVERSITY   (Sweden)

^b ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Collagenous colitis; Lymphocytic colitis; Microscopic colitis; Mucosal cytokines; T cells

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; TRANSCRIPTION FACTOR T BET; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; COLLAGENOUS COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; FEMALE; HUMAN; INTESTINE BIOPSY; LYMPHOCYTIC COLITIS; MALE; MICROSCOPIC COLITIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; TH1 CELL; TH17 CELL; ULCERATIVE COLITIS; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; CASE-CONTROL STUDIES; COLITIS, COLLAGENOUS; COLITIS, LYMPHOCYTIC; COLITIS, MICROSCOPIC; CYTOKINES; FEMALE; HUMANS; IMMUNITY, MUCOSAL; MALE; MIDDLE AGED; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS; TH17 CELLS; YOUNG ADULT;

EID: 84877608594     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.03.007     Document Type: Article

References (59)

1. Abbas A.K., Murphy K.M., Sher A. Functional diversity of helper T lymphocytes. Nature 1996, 383:787-793.
2. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., et al. Phenotypic and functional features of human Th17 cells. Journal of Experimental Medicine 2007, 204:1849-1861.
3. Bending D., De la Pena H., Veldhoen M., Phillips J.M., Uyttenhove C., Stockinger B., et al. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. Journal of Clinical Investigation 2009, 119:565-572.
4. Boniface K., Blumenschein W.M., Brovont-Porth K., McGeachy M.J., Basham B., Desai B., et al. Human Th17 cells comprise heterogeneous subsets including IFN-gamma-producing cells with distinct properties from the Th1 lineage. Journal of Immunology 2010, 185:679-687.
5. Brand S. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009, 58:1152-1167.
6. Chamoto K., Kosaka A., Tsuji T., Matsuzaki J., Sato T., Takeshima T., et al. Critical role of the Th1/Tc1 circuit for the generation of tumor-specific CTL during tumor eradication in vivo by Th1-cell therapy. Cancer Science 2003, 94:924-928.
7. Ciric B., El-behi M., Cabrera R., Zhang G.X., Rostami A. IL-23 drives pathogenic IL-17-producing CD8+ T cells. Journal of Immunology 2009, 182:5296-5305.
8. Dignass A., Eliakim R., Magro F., Maaser C., Chowers Y., Geboes K., et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis. Part 1. Definitions and diagnosis. Journal of Crohn's and Colitis 2012, 6:965-990.
9. Fina D., Sarra M., Fantini M.C., Rizzo A., Caruso R., Caprioli F., et al. Regulation of gut inflammation and th17 cell response by interleukin-21. Gastroenterology 2008, 134:1038-1048.
10. Fuss I.J. Is the Th1/Th2 paradigm of immune regulation applicable to IBD?. Inflammatory Bowel Diseases 2008, 14(Suppl. 2):S110-S112.
11. Greenbaum D., Colangelo C., Williams K., Gerstein M. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biology 2003, 4:117.
12. Guillot-Delost M., Le Gouvello S., Mesel-Lemoine M., Cherai M., Baillou C., Simon A., et al. Human CD90 identifies Th17/Tc17 T cell subsets that are depleted in HIV-infected patients. Journal of Immunology 2012, 188:981-991.
13. Göranzon C., Kumawat A.K., Hultgren-Hörnqvist E., Tysk C., Eriksson S., Bohr J., et al. Immunohistochemical characterization of lymphocytes in Microscopic Colitis. Journal of Crohn's and Colitis 2013, 10.1016/j.crohns.2013.02.007.
14. Hamada H., Garcia-Hernandez Mde L., Reome J.B., Misra S.K., Strutt T.M., McKinstry K.K., et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. Journal of Immunology 2009, 182:3469-3481.
15. Hirota K., Duarte J.H., Veldhoen M., Hornsby E., Li Y., Cua D.J., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nature Immunology 2011, 12:255-263.
16. Huber M., Heink S., Grothe H., Guralnik A., Reinhard K., Elflein K., et al. A Th17-like developmental process leads to CD8(+) Tc17 cells with reduced cytotoxic activity. European Journal of Immunology 2009, 39:1716-1725.
17. Jarnerot G., Tysk C., Bohr J., Eriksson S. Collagenous colitis and fecal stream diversion. Gastroenterology 1995, 109:449-455.
18. Johrens K., Grunbaum M., Anagnostopoulos I. Differences in the T-bet and GATA-3 expression patterns between lymphocytic colitis and coeliac disease. Virchows Archiv 2010, 457:451-456.
19. Kim C.J., Nazli A., Rojas O.L., Chege D., Alidina Z., Huibner S., et al. A role for mucosal IL-22 production and Th22 cells in HIV-associated mucosal immunopathogenesis. Mucosal Immunology 2012, 5:670-680.
20. Kobayashi T., Okamoto S., Hisamatsu T., Kamada N., Chinen H., Saito R., et al. IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 2008, 57:1682-1689.
21. Kondo T., Takata H., Matsuki F., Takiguchi M. Cutting edge: phenotypic characterization and differentiation of human CD8+ T cells producing IL-17. Journal of Immunology 2009, 182:1794-1798.
22. Kuang D.M., Peng C., Zhao Q., Wu Y., Zhu L.Y., Wang J., et al. Tumor-activated monocytes promote expansion of IL-17-producing CD8+ T cells in hepatocellular carcinoma patients. Journal of Immunology 2010, 185:1544-1549.
23. Kumawat A.K., Strid H., Elgbratt K., Tysk C., Bohr J., Hultgren Hornquist E. Microscopic colitis patients have increased proportions of Ki67(+) proliferating and CD45RO(+) active/memory CD8(+) and CD4(+)8(+) mucosal T cells. Journal of Crohn's and Colitis 2012, September. 10.1016/j.crohns.2012.08.014.
24. Lexberg M.H., Taubner A., Albrecht I., Lepenies I., Richter A., Kamradt T., et al. IFN-gamma and IL-12 synergize to convert in vivo generated Th17 into Th1/Th17 cells. European Journal of Immunology 2010, 40:3017-3027.
25. Liang S.C., Tan X.Y., Luxenberg D.P., Karim R., Dunussi-Joannopoulos K., Collins M., et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. Journal of Experimental Medicine 2006, 203:2271-2279.
26. Lundberg J.O., Herulf M., Olesen M., Bohr J., Tysk C., Wiklund N.P., et al. Increased nitric oxide production in collagenous and lymphocytic colitis. European Journal of Clinical Investigation 1997, 27:869-871.
27. Maloy K.J. The interleukin-23/interleukin-17 axis in intestinal inflammation. Journal of Internal Medicine 2008, 263:584-590.
28. Menconi M.J., Unno N., Smith M., Aguirre D.E., Fink M.P. Nitric oxide donor-induced hyperpermeability of cultured intestinal epithelial monolayers: role of superoxide radical, hydroxyl radical, and peroxynitrite. Biochimica et Biophysica Acta 1998, 1425:189-203.
29. Monteleone G., Monteleone I., Fina D., Vavassori P., Del Vecchio Blanco G., Caruso R., et al. Interleukin-21 enhances T-helper cell type I signaling and interferon-gamma production in Crohn's disease. Gastroenterology 2005, 128:687-694.
30. Monteleone G., Pallone F., Macdonald T.T. Interleukin-21 as a new therapeutic target for immune-mediated diseases. Trends in Pharmacological Sciences 2009, 30:441-447.
31. Morrison P.J., Ballantyne S.J., Kullberg M.C. Interleukin-23 and T helper 17-type responses in intestinal inflammation: from cytokines to T-cell plasticity. Immunology 2011, 133:397-408.
32. Mosnier J.F., Larvol L., Barge J., Dubois S., De La Bigne G., Henin D., et al. Lymphocytic and collagenous colitis: an immunohistochemical study. American Journal of Gastroenterology 1996, 91:709-713.
33. Munch A., Aust D., Bohr J., Bonderup O., Fernandez Banares F., Hjortswang H., et al. Microscopic colitis: current status, present and future challenges: statements of the European Microscopic Colitis Group. Journal of Crohn's and Colitis 2012, 6:932-945.
34. Olesen M., Middelveld R., Bohr J., Tysk C., Lundberg J.O., Eriksson S., et al. Luminal nitric oxide and epithelial expression of inducible and endothelial nitric oxide synthase in collagenous and lymphocytic colitis. Scandinavian Journal of Gastroenterology 2003, 38:66-72.
35. Olsen T., Goll R., Cui G., Husebekk A., Vonen B., Birketvedt G.S., et al. Tissue levels of tumor necrosis factor-alpha correlates with grade of inflammation in untreated ulcerative colitis. Scandinavian Journal of Gastroenterology 2007, 42:1312-1320.
36. Pardi D.S., Kelly C.P. Microscopic colitis. Gastroenterology 2011, 140:1155-1165.
37. Pratt J.M., Petty J., Riba-Garcia I., Robertson D.H., Gaskell S.J., Oliver S.G., et al. Dynamics of protein turnover, a missing dimension in proteomics. Molecular and Cellular Proteomics 2002, 1:579-591.
38. Ross J. mRNA stability in mammalian cells. Microbiological Reviews 1995, 59:423-450.
39. Rovedatti L., Kudo T., Biancheri P., Sarra M., Knowles C.H., Rampton D.S., et al. Differential regulation of interleukin 17 and interferon gamma production in inflammatory bowel disease. Gut 2009, 58:1629-1636.
40. Salas A., Fernandez-Banares F., Casalots J., Gonzalez C., Tarroch X., Forcada P., et al. Subepithelial myofibroblasts and tenascin expression in microscopic colitis. Histopathology 2003, 43:48-54.
41. Saxena A., Desbois S., Carrie N., Lawand M., Mars L.T., Liblau R.S. Tc17 CD8+ T cells potentiate Th1-mediated autoimmune diabetes in a mouse model. Journal of Immunology 2012, 189:3140-3149.
42. Shibahara T., Wilcox J.N., Couse T., Madara J.L. Characterization of epithelial chemoattractants for human intestinal intraepithelial lymphocytes. Gastroenterology 2001, 120:60-70.
43. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nature Immunology 2011, 12:383-390.
44. +-ATPase by interferon gamma down-regulates intestinal epithelial transport and barrier function. Gastroenterology 2001, 120:1393-1403.
45. Tagkalidis P.P., Gibson P.R., Bhathal P.S. Microscopic colitis demonstrates a T helper cell type 1 mucosal cytokine profile. Journal of Clinical Pathology 2007, 60:382-387.
46. Tajima M., Wakita D., Noguchi D., Chamoto K., Yue Z., Fugo K., et al. IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. Journal of Experimental Medicine 2008, 205:1019-1027.
47. Tajima M., Wakita D., Satoh T., Kitamura H., Nishimura T. IL-17/IFN-gamma double producing CD8+ T (Tc17/IFN-gamma) cells: a novel cytotoxic T-cell subset converted from Tc17 cells by IL-12. International Immunology 2011, 23:751-759.
48. Trifari S., Kaplan C.D., Tran E.H., Crellin N.K., Spits H. Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nature Immunology 2009, 10:864-871.
49. Tysk C., Bohr J., Nyhlin N., Wickbom A., Eriksson S. Diagnosis and management of microscopic colitis. World Journal of Gastroenterology 2008, 14:7280-7288.
50. Ung K.A., Gillberg R., Kilander A., Abrahamsson H. Role of bile acids and bile acid binding agents in patients with collagenous colitis. Gut 2000, 46:170-175.
51. Unutmaz D. RORC2: the master of human Th17 cell programming. European Journal of Immunology 2009, 39:1452-1455.
52. Vigren L., Olesen M., Benoni C., Sjoberg K. Are collagenous and lymphocytic colitis different aspects of the same disease. Scandinavian Journal of Gastroenterology 2012, 47:1448-1453.
53. Volpe E., Servant N., Zollinger R., Bogiatzi S.I., Hupe P., Barillot E., et al. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(H)-17 responses. Nature Immunology 2008, 9:650-657.
54. Wagner M., Lampinen M., Sangfelt P., Agnarsdottir M., Carlson M. Budesonide treatment of patients with collagenous colitis restores normal eosinophil and T-cell activity in the colon. Inflammatory Bowel Diseases 2010, 16:1118-1126.
55. Wolff M.J., Leung J.M., Davenport M., Poles M.A., Cho I., Loke P. TH17, TH22 and TREG cells are enriched in the healthy human cecum. PLoS ONE 2012, 7:e41373.
56. Yamamoto-Furusho J.K., Miranda-Perez E., Fonseca-Camarillo G., Sanchez-Munoz F., Dominguez-Lopez A., Barreto-Zuniga R. Colonic epithelial upregulation of interleukin 22 (IL-22) in patients with ulcerative colitis. Inflammatory Bowel Diseases 2010, 16:1823.
57. Yen H.R., Harris T.J., Wada S., Grosso J.F., Getnet D., Goldberg M.V., et al. Tc17 CD8 T cells: functional plasticity and subset diversity. Journal of Immunology 2009, 183:7161-7168.
58. Zahn A., Giese T., Karner M., Braun A., Hinz U., Stremmel W., et al. Transcript levels of different cytokines and chemokines correlate with clinical and endoscopic activity in ulcerative colitis. BMC Gastroenterology 2009, 9:13.
59. Zhuang Y., Peng L.S., Zhao Y.L., Shi Y., Mao X.H., Chen W., et al. CD8(+) T cells that produce interleukin-17 regulate myeloid-derived suppressor cells and are associated with survival time of patients with gastric cancer. Gastroenterology 2012, 143. pp. 951.e8-962.e8.