CCL20/CCR6-mediated migration of regulatory T cells to the Helicobacter pylori-infected human gastric mucosa

Gut

Volumn 63, Issue 10, 2014, Pages 1550-1559

  Cook, Katherine W ^a   Letley, Darren P ^a   Ingram, Richard J M ^a   Staples, Emily ^a   Skjoldmose, Helle ^a   Atherton, John C ^a   Robinson, Karen ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; ALPHA INTEGRIN E; BETA7 INTEGRIN; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; L SELECTIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CCL20 PROTEIN, HUMAN; CCR6 PROTEIN, HUMAN; CHEMOKINE;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LYMPHOCYTE MIGRATION; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; UPREGULATION; ADOLESCENT; ANIMAL; CD8+ T LYMPHOCYTE; CELL LINE; CHEMOTAXIS; FLOW CYTOMETRY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MUCOSAL IMMUNOLOGY; NEUTROPHIL CHEMOTAXIS; PATHOGENICITY; PEPTIC ULCER; PHYSIOLOGY; STOMACH MUCOSA; T LYMPHOCYTES; UNITED KINGDOM; VERY ELDERLY; YOUNG ADULT;

CHEMOTAXIS; HELICOBACTER PYLORI; MUCOSAL IMMUNOLOGY; T LYMPHOCYTES;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CHEMOKINE CCL20; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; FEMALE; FLOW CYTOMETRY; GASTRIC MUCOSA; GREAT BRITAIN; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MALE; MICE; MIDDLE AGED; PEPTIC ULCER; RECEPTORS, CCR6; T-LYMPHOCYTES, REGULATORY; YOUNG ADULT;

EID: 84908556963     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-306253     Document Type: Article

References (47)

1. Blaser MJ, Atherton JC. Helicobacter pylori persistence: biology and disease. J Clin Invest 2004;113:321-33.
2. Atherton JC, Blaser MJ. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 2009;119:2475-87.
3. Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2002;2:28-37.
4. Tegtmeyer N, Wessler S, Backert S. Role of the cag-pathogenicity island encoded type IV secretion system in Helicobacter pylori pathogenesis. FEBS J 2011;278:1190-202.
5. Peek RM Jr, Miller GG, Tham KT, et al. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest 1995;73:760-70.
6. Viala J, Chaput C, Boneca IG, et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 2004;5:1166-74.
7. Bamford KB, Fan X, Crowe SE, et al. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998;114:482-92.
8. Rad R, Ballhorn W, Voland P, et al. Extracellular and intracellular pattern recognition receptors cooperate in the recognition of Helicobacter pylori. Gastroenterology 2009;136:2247-57.
9. Robinson K, Kenefeck R, Pidgeon EL, et al. Helicobacter pylori-induced peptic ulcer disease is associated with inadequate regulatory T cell responses. Gut 2008;57:1375-85.
10. Lundgren A, Stromberg E, Sjoling A, et al. Mucosal FOXP3-expressing CD4+ CD25high regulatory T cells in Helicobacter pylori-infected patients. Infect Immun 2005;73:523-31.
11. Rad R, Brenner L, Bauer S, et al. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 2006;131:525-37.
12. Raghavan S, Fredriksson M, Svennerholm AM, et al. Absence of CD4+CD25+ regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pylori-infected mice. Clin Exp Immunol 2003;132:393-400.
13. th International Congress of Mucosal Immunology; 2011, Paris, France. http://www.socmucimm.org/images/icmi2011/abstract%20supplement%20-%20chronological%207-18-2011.pdf
14. Eikawa S, Ohue Y, Kitaoka K, et al. Enrichment of Foxp3+ CD4 regulatory T cells in migrated T cells to IL-6- and IL-8-expressing tumors through predominant induction of CXCR1 by IL-6. J Immunol 2010;185:6734-40.
15. Gobert M, Treilleux I, Bendriss-Vermare N, et al. Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res 2009;69:2000-9.
16. Dobaczewski M, Xia Y, Bujak M, et al. CCR5 signaling suppresses inflammation and reduces adverse remodeling of the infarcted heart, mediating recruitment of regulatory T cells. Am J Pathol 2010;176:2177-87.
17. Yamaoka Y, Kita M, Kodama T, et al. Chemokines in the gastric mucosa in Helicobacter pylori infection. Gut 1998;42:609-17.
18. Eck M, Schmausser B, Scheller K, et al. CXC chemokines Gro(alpha)/IL-8 and IP-10/MIG in Helicobacter pylori gastritis. Clin Exp Immunol 2000;122:192-9.
19. Lundgren A, Trollmo C, Edebo A, et al. Helicobacter pylori-specific CD4+ T cells home to and accumulate in the human Helicobacter pylori-infected gastric mucosa. Infect Immun 2005;73:5612-19.
20. Wu YY, Tsai HF, Lin WC, et al. Upregulation of CCL20 and recruitment of CCR6+ gastric infiltrating lymphocytes in Helicobacter pylori gastritis. Infect Immun 2007;75:4357-63.
21. Enarsson K, Lundgren A, Kindlund B, et al. Function and recruitment of mucosal regulatory T cells in human chronic Helicobacter pylori infection and gastric adenocarcinoma. Clin Immunol 2006;121:358-68.
22. Siewert C, Menning A, Dudda J, et al. Induction of organ-selective CD4+ regulatory T cell homing. Eur J Immunol 2007;37:978-89.
23. Argent RH, Thomas RJ, Aviles-Jimenez F, et al. Toxigenic Helicobacter pylori infection precedes gastric hypochlorhydria in cancer relatives, and H. pylori virulence evolves in these families. Clin Cancer Res 2008;14:2227-35.
24. Staples E, Ingram RJ, Atherton JC, et al. Optimising the quantification of cytokines present at low concentrations in small human mucosal tissue samples using Luminex assays. J Immunol Methods 2013;394:1-9.
25. Argent RH, Thomas RJ, Letley DP, et al. Functional association between the Helicobacter pylori virulence factors VacA and CagA. J Med Microbiol 2008;57(Pt 2):145-50.
26. Crabtree JE, Ferrero RL, Kusters JG. The mouse colonizing Helicobacter pylori strain SS1 may lack a functional cag pathogenicity island. Helicobacter 2002;7:139-40; author reply 40-1.
27. Patel SR, Smith K, Letley DP, et al. Helicobacter pylori down-regulates expression of human beta-defensin 1 in the gastric mucosa in a type IV secretion dependent fashion. Cell Microbiol 2013;15:2080-92.
28. Haribhai D, Lin W, Relland LM, et al. Regulatory T cells dynamically control the primary immune response to foreign antigen. J Immunol 2007;178:2961-72.
29. Robinson K, Loughlin MF, Potter R, et al. Host adaptation and immune modulation are mediated by homologous recombination in Helicobacter pylori. J Infect Dis 2005;191:579-87.
30. Yamazaki T, Yang XO, Chung Y, et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 2008;181:8391-401.
31. Kim TG, Byamba D, Wu WH, et al. Statins inhibit chemotactic interaction between CCL20 and CCR6 in vitro: possible relevance to psoriasis treatment. Exp Dermatol 2011;20:855-7.
32. Chaput C, Labigne A, Boneca IG. Characterization of Helicobacter pylori lytic transglycosylases Slt and MltD. J Bacteriol 2007;189:422-9.
33. Yoshida A, Isomoto H, Hisatsune J, et al. Enhanced expression of CCL20 in human Helicobacter pylori-associated gastritis. Clin Immunol 2009;130:290-7.
34. Schutyser E, Struyf S, Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev 2003;14:409-26.
35. Rhee SH, Keates AC, Moyer MP, et al. MEK is a key modulator for TLR5-induced interleukin-8 and MIP3alpha gene expression in non-transformed human colonic epithelial cells. J Biol Chem 2004;279:25179-88.
36. Allison CC, Kufer TA, Kremmer E, et al. Helicobacter pylori induces MAPK phosphorylation and AP-1 activation via a NOD1-dependent mechanism. J Immunol 2009;183:8099-109.
37. Kido M, Tanaka J, Aoki N, et al. Helicobacter pylori promotes the production of thymic stromal lymphopoietin by gastric epithelial cells and induces dendritic cell-mediated inflammatory Th2 responses. Infect Immun 2010;78:108-14.
38. Campbell DJ, Koch MA. Phenotypical and functional specialization of FOXP3(+) regulatory T cells. Nat Rev Immunol 2011;11:119-30.
39. Hart AL, Ng SC, Mann E, et al. Homing of immune cells: role in homeostasis and intestinal inflammation. Inflamm Bowel Dis 2010;16:1969-77.
40. Williams IR. CCR6 and CCL20: partners in intestinal immunity and lymphorganogenesis. Ann N Y Acad Sci 2006;1072:52-61.
41. Serrano C, Wright SW, Bimczok D, et al. Downregulated Th17 responses are associated with reduced gastritis in Helicobacter pylori-infected children. Mucosal Immunol 2013;6:950-9.
42. Comerford I, Bunting M, Fenix K, et al. An immune paradox: how can the same chemokine axis regulate both immune tolerance and activation?: CCR6/CCL20: a chemokine axis balancing immunological tolerance and inflammation in autoimmune disease. Bioessays 2010;32:1067-76.
43. Lee AY, Eri R, Lyons AB, et al. CC chemokine ligand 20 and its cognate receptor CCR6 in mucosal T cell immunology and inflammatory bowel disease: odd couple or axis of evil? Front Immunol 2013;4:194.
44. Kaser A, Ludwiczek O, Holzmann S, et al. Increased expression of CCL20 in human inflammatory bowel disease. J Clin Immunol 2004;24:74-85.
45. Kitamura K, Farber JM, Kelsall BL. CCR6 marks regulatory T cells as a colon-tropic, IL-10-producing phenotype. J Immunol 2010;185:3295-304.
46. Sonnenberg A, Genta RM. Low prevalence of Helicobacter pylori infection among patients with inflammatory bowel disease. Aliment Pharmacol Ther 2012;35:469-76.
47. Luther J, Dave M, Higgins PD, et al. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis 2010;16:1077-84.