Distinct immune signatures in the colon of Crohn's disease and ankylosing spondylitis patients in the absence of inflammation

Immunology and Cell Biology

Volumn 94, Issue 5, 2016, Pages 421-429

  Dunn, Elliott T J ^a   Taylor, Edward S ^a   Stebbings, Simon ^a   Schultz, Michael ^a   Butt, A Grant ^a   Kemp, Roslyn A ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 22;

ADULT; AGED; ANKYLOSING SPONDYLITIS; ARTICLE; BATH ANKYLOSING SPONDYLITIS DISEASE ACTIVITY INDEX; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CLINICAL ARTICLE; COHORT ANALYSIS; COLONOSCOPY; COMPARATIVE STUDY; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; DESCENDING COLON; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNE SIGNATURE; IMMUNOLOGICAL PARAMETERS; INFLAMMATORY DISEASE; INTESTINE BIOPSY; MALE; PHENOTYPE; PILOT STUDY; PROTEIN BLOOD LEVEL; RECTUM; REGULATORY T LYMPHOCYTE; SIGMOID; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TERMINAL ILEUM; TRANSVERSE COLON; YOUNG ADULT; ADOLESCENT; CASE CONTROL STUDY; COLON; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE COUNT; LYMPHOCYTE SUBPOPULATION; MIDDLE AGED; PATHOLOGY;

ADOLESCENT; ADULT; AGED; CASE-CONTROL STUDIES; COLON; CROHN DISEASE; FEMALE; HUMANS; INFLAMMATION; LYMPHOCYTE COUNT; LYMPHOCYTE SUBSETS; MALE; MIDDLE AGED; PHENOTYPE; SPONDYLITIS, ANKYLOSING; T-LYMPHOCYTES;

EID: 84954349406     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2015.112     Document Type: Article

References (54)

1. Gasche C, Scholmerich J, Brynskov J, D'Haens G, Hanauer SB, Irvine EJ, et al. A simple classification of Crohn's disease: report of the Working Party for the World Congresses of Gastroenterology, Vienna 1998. Inflamm Bowel Dis 2000; 6: 8-15
2. Danoy P, Pryce K, Hadler J, Bradbury LA, Farrar C, Pointon J, et al. Association of variants at 1q32 and STAT3 with ankylosing spondylitis suggests genetic overlap with Crohn's disease. PLoS Genet 2010; 6: e1001195
3. Stebbings S, Jenks K, Treharne GJ, Garcia JA, Schultz M, Highton J, et al. Validation of the Dudley Inflammatory Bowel Symptom Questionnaire for the assessment of bowel symptoms in axial SpA: prevalence of clinically relevant bowel symptoms and association with disease activity. Rheumatology (Oxford) 2012; 51: 858-865
4. Barrett JC, Hansoul S, Nicolae DL, Cho JH, Duerr RH, Rioux JD, et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat Genet 2008; 40: 955-962
5. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 2012; 491: 119-124
6. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448: 427-434
7. Cho JH. The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 2008; 8: 458-466
8. Graham DB, Xavier RJ. From genetics of inflammatory bowel disease towards mechanistic insights. Trends Immunol 2013; 34: 371-378
9. Shale M, Schiering C, Powrie F. CD4(+) T-cell subsets in intestinal inflammation. Immunol Rev 2013; 252: 164-182
10. Parronchi P, Romagnani P, Annunziato F, Sampognaro S, Becchio A, Giannarini L, et al. Type 1 T-helper cell predominance and interleukin-12 expression in the gut of patients with Crohn's disease. Am J Pathol 1997; 150: 823-832
11. Fuss IJ, Neurath M, Boirivant M, Klein JS, de la Motte C, Strong SA, et al. Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol 1996; 157: 1261-1270
12. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, et al. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003; 52: 65-70
13. Maul J, Loddenkemper C, Mundt P, Berg E, Giese T, Stallmach A, et al. Peripheral and intestinal regulatory CD4+ CD25(high) T cells in inflammatory bowel disease. Gastroenterology 2005; 128: 1868-1878
14. Leung JM, Davenport M, Wolff MJ, Wiens KE, Abidi WM, Poles MA, et al. IL-22-producing CD4+ cells are depleted in actively inflamed colitis tissue. Mucosal Immunol 2014; 7: 124-133
15. Sugimoto K, Ogawa A, Mizoguchi E, Shimomura Y, Andoh A, Bhan AK, et al. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 2008; 118: 534-544
16. Vainer B, Nielsen OH, Hendel J, Horn T, Kirman I. Colonic expression and synthesis of interleukin 13 and interleukin 15 in inflammatory bowel disease. Cytokine 2000; 12: 1531-1536
17. Kucharzik T, Lugering N, Weigelt H, Adolf M, Domschke W, Stoll R. Immunoregulatory properties of IL-13 in patients with inflammatory bowel disease; comparison with IL-4 and IL-10. Clin Exp Immunol 1996; 104: 483-490
18. Smith JA. Update on ankylosing spondylitis: current concepts in pathogenesis. Curr Allergy Asthma Rep 2015; 15: 489
19. Sherlock JP, Joyce-Shaikh B, Turner SP, Chao CC, Sathe M, Grein J, et al. IL-23 induces spondyloarthropathy by acting on ROR-gammat+ CD3+CD4-CD8-entheseal resident T cells. Nat Med 2012; 18: 1069-1076
20. Zhou L, Chong MM, Littman DR. Plasticity of CD4+ T cell lineage differentiation. Immunity 2009; 30: 646-655
21. Murphy KM, Stockinger B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat Immunol 2010; 11: 674-680
22. Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8: 247-258
23. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13: 843-850
24. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. Multiple-cytokineproducing antiviral CD4 T cells are functionally superior to single-cytokineproducing cells. J Virol 2007; 81: 8468-8476
25. Wallace KL, Zheng LB, Kanazawa Y, Shih DQ. Immunopathology of inflammatory bowel disease. World J Gastroenterol 2014; 20: 6-21
26. Hovhannisyan Z, Treatman J, Littman DR, Mayer L. Characterization of interleukin-17-producing regulatory T cells in inflamed intestinal mucosa from patients with inflammatory bowel diseases. Gastroenterology 2011; 140: 957-965
27. Girardin A, McCall J, Black MA, Edwards F, Phillips V, Taylor ES, et al. Inflammatory and regulatory T cells contribute to a unique immune microenvironment in tumor tissue of colorectal cancer patients. Int J Cancer 2013; 132: 1842-1850
28. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol 2003; 3: 521-533
29. Xu XR, Liu CQ, Feng BS, Liu ZJ. Dysregulation of mucosal immune response in pathogenesis of inflammatory bowel disease. World J Gastroenterol 2014; 20: 3255-3264
30. Geremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev 2014; 13: 3-10
31. Mielants H, Veys EM, De Vos M, Cuvelier C, Goemaere S, De Clercq L, et al. The evolution of spondyloarthropathies in relation to gut histology. I. Clinical aspects. J Rheumatol 1995; 22: 2266-2272
32. Barbi J, Pardoll D, Pan F. Treg functional stability and its responsiveness to the microenvironment. Immunol Rev 2014; 259: 115-139
33. Brakenhoff LK, van der Heijde DM, Hommes DW, Huizinga TW, Fidder HH. The jointgut axis in inflammatory bowel diseases. J Crohns Colitis 2010; 4: 257-268
34. Ergin A, Syrbe U, Scheer R, Thiel A, Adam T, Bussow K, et al. Impaired peripheral Th1 CD4+ T cell response to Escherichia coli proteins in patients with Crohn's disease and ankylosing spondylitis. J Clin Immunol 2011; 31: 998-1009
35. Eastaff-Leung N, Mabarrack N, Barbour A, Cummins A, Barry S. Foxp3+ regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease. J Clin Immunol 2010; 30: 80-89
36. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005; 201: 723-735
37. Dejaco C, Duftner C, Grubeck-Loebenstein B, Schirmer M. Imbalance of regulatory T cells in human autoimmune diseases. Immunology 2006; 117: 289-300
38. Koenen HJ, Smeets RL, Vink PM, van Rijssen E, Boots AM, Joosten I. Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 2008; 112: 2340-2352
39. Liu F, Wang F, Wang CC, Li N, Li SF. Expression of IL-2 and IL-11 and its significance in patients with ankylosing spondylitis. Asian Pac J Trop Med 2013; 6: 76-78
40. Bal A, Unlu E, Bahar G, Aydog E, Eksioglu E, Yorgancioglu R. Comparison of serum IL-1 beta, sIL-2R, IL-6, and TNF-Alpha levels with disease activity parameters in ankylosing spondylitis. Clin Rheumatol 2007; 26: 211-215
41. Fahey LM, Wilson EB, Elsaesser H, Fistonich CD, McGavern DB, Brooks DG. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J Exp Med 2011; 208: 987-999
42. Rutz S, Eidenschenk C, Ouyang W. IL-22, not simply a Th17 cytokine. Immunol Rev 2013; 252: 116-132
43. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27: 485-517
44. Kang YH, Seigel B, Bengsch B, Fleming VM, Billerbeck E, Simmons R, et al. CD161(+) CD4(+) T cells are enriched in the liver during chronic hepatitis and associated with cosecretion of IL-22 and IFN-gamma. Front Immunol 2012; 3: 346
45. Dyring-Andersen B, Skov L, Lovendorf MB, Bzorek M, Sondergaard K, Lauritsen JP, et al. CD4(+) T cells producing interleukin (IL)-17, IL-22 and interferon-gamma are major effector T cells in nickel allergy. Contact Dermatitis 2013; 68: 339-347
46. Gill T, Asquith M, Rosenbaum JT, Colbert RA. The intestinal microbiome in spondyloarthritis. Curr Opin Rheumatol 2015; 27: 319-325
47. Aujla SJ, Chan YR, Zheng M, Fei M, Askew DJ, Pociask DA, et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 2008; 14: 275-281
48. Kemp R, Dunn E, Schultz M. Immunomodulators in inflammatory bowel disease: an emerging role for biologic agents. BioDrugs 2013; 27: 585-590
49. Duhen R, Glatigny S, Arbelaez CA, Blair TC, Oukka M, Bettelli E. Cutting edge: the pathogenicity of IFN-gamma-producing Th17 cells is independent of T-bet. J Immunol 2013; 190: 4478-4482
50. Franke A, McGovern DP, Barrett JC, Wang K, Radford-Smith GL, Ahmad T, et al. Genome-wide meta-Analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010; 42: 1118-1125
51. Rivas MA, Beaudoin M, Gardet A, Stevens C, Sharma Y, Zhang CK, et al. Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease. Nat Genet 2011; 43: 1066-1073
52. Marchiando AM, Ramanan D, Ding Y, Gomez LE, Hubbard-Lucey VM, Maurer K, et al. A deficiency in the autophagy gene Atg16L1 enhances resistance to enteric bacterial infection. Cell Host Microbe 2013; 14: 216-224
53. Jung T, Schauer U, Heusser C, Neumann C, Rieger C. Detection of intracellular cytokines by flow cytometry. J Immunol Methods 1993; 159: 197-207
54. Lee JA, Spidlen J, Boyce K, Cai J, Crosbie N, Dalphin M, et al. MIFlowCyt: the minimum information about a flow cytometry experiment. Cytometry A 2008; 73: 926-930