Helicobacter pylori induces in-vivo expansion of human regulatory T cells through stimulating interleukin-1β production by dendritic cells

Clinical and Experimental Immunology

Volumn 170, Issue 3, 2012, Pages 300-309

  Mitchell, P J ^a   Afzali, B ^a   Fazekasova, H ^a   Chen, D ^a   Ali, N ^a   Powell, N ^a   Lord, G M ^a   Lechler, R I ^a   Lombardi, G ^a  

^a GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Helicobacter pylori; Human; Interleukin 1; Regulatory T cells; Suppression

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CARCINOGENESIS; CELL DIVISION; CELL EXPANSION; CHRONIC GASTRITIS; CYTOKINE PRODUCTION; DENDRITIC CELL; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STOMACH BIOPSY; STOMACH MUCOSA;

DENDRITIC CELLS; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84868255022     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2012.04659.x     Document Type: Article

References (57)

1. Logan R, Walker M. ABC of the upper gastrointestinal tract. Epidemiology and diagnosis of Helicobacter pylori infection. BMJ 2001; 323:920-922.
2. Murray LJ, Bamford KB, O'Reilly DP, McCrum EE, Evans AE. Helicobacter pylori infection: relation with cardiovascular risk factors, ischaemic heart disease, and social class. Br Heart J 1995; 74:497-501.
3. Dhalla F, da Silva SP, Lucas M, Travis S, Chapel H. Review of gastric cancer risk factors in patients with common variable immunodeficiency disorders, resulting in a proposal for a surveillance programme. Clin Exp Immunol 2011; 165:1-7.
4. Harris A, Misiewicz JJ. ABC of the upper gastrointestinal tract. Management of Helicobacter pylori infection. BMJ 2001; 323:1047-1050.
5. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002; 347:1175-1186.
6. Schmausser B, Andrulis M, Endrich S etal. Expression and subcellular distribution of Toll-like receptors TLR-4, TLR-5 and TLR-9 on the gastric epithelium in Helicobacter pylori infection. Clin Exp Immunol 2004; 136:521-526.
7. Maeda S, Akanuma M, Mitsuno Y etal. Distinct mechanism of Helicobacter pylori-mediated NF-kappa B activation between gastric cancer cells and monocytic cells. J Biol Chem 2001; 276:44856-44864.
8. Nishi T, Okazaki K, Kawasaki K etal. Involvement of myeloid dendritic cells in the development of gastric secondary lymphoid follicles in Helicobacter pylori-infected neonatally thymectomized BALB/c mice. Infect Immun 2003; 71:2153-2162.
9. Ninomiya T, Matsui H, Akbar SM, Murakami H, Onji M. Localization and characterisation of antigen-presenting dendritic cells in the gastric mucosa of murine and human autoimmune gastritis. Eur J Clin Invest 2000; 30:350-358.
10. Mitchell P, Germain C, Fiori PL, Khamri W etal. Chronic exposure to Helicobacter pylori impairs dendritic cell function and inhibits Th1 development. Infect Immun 2007; 75:810-819.
11. Bamford KB, Fan X, Crowe SE etal. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998; 114:482-492.
12. Karttunen R, Karttunen T, Ekre HP, MacDonald TT. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut 1995; 36:482-492.
13. Khamri W, Walker MM, Clark P etal. Helicobacter pylori stimulates dendritic cells to induce interleukin-17 expression from CD4+ T lymphocytes. Infect Immun 2010; 78:845-853.
14. Mizuno T, Ando T, Nobata K etal. Interleukin-17 levels in Helicobacter pylori-infected gastric mucosa and pathologic sequelae of colonization. World J Gastroenterol 2005; 11:6305-6311.
15. Sakaguch IS, Miyara M, Costantino CM, Hafler DA. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10:490-500.
16. Coffer PJ, Burgering BM. Forkhead-box transcription factors and their role in the immune system. Nat Rev Immunol 2004; 11:889-899.
17. Belkaid Y, Rouse B. Natural regulatory T cells in infectious disease. Nat Immunol 2005; 6:353-360.
18. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420:502-507.
19. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 2003; 197:111-119.
20. Lundgren A, Suri-Payer E, Enarsson K, Svennerholm AM, Lundin BS. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect Immun 2003; 71:1755-1762.
21. Lundgren A, Strömberg E, Sjöling A etal. Mucosal FOXP3-expressing CD4+ CD25high regulatory T cells in Helicobacter pylori-infected patients. Infect Immun 2005; 73:523-531.
22. Yamazaki S, Iyoda T, Tarbell K etal. Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J Exp Med 2003; 198:235-247.
23. Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol 2004; 172:2778-2784.
24. O'Sullivan BJ, Thomas HE, Pai S etal. IL-1 beta breaks tolerance through expansion of CD25+ effector T cells. J Immunol 2006; 176:7278-7287.
25. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003; 299:1033-1036.
26. Kubo T, Hatton RD, Oliver J, Liu X, Elson CO, Weaver CT. Regulatory T cell suppression and anergy are differentially regulated by proinflammatory cytokines produced by TLR-activated dendritic cells. J Immunol 2004; 173:7249-7258.
27. Valencia X, Stephens G, Goldbach-Mansky R, Wilson M, Shevach EM, Lipsky PE. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 2006; 108:253-261.
28. King IL, Segal BM. Cutting edge: IL-12 induces CD4+CD25- T cell activation in the presence of T regulatory cells. J Immunol 2005; 175:641-645.
29. Scott K, Manunta M, Germain C etal. Qualitatively distinct patterns of cytokines are released by human dendritic cells in response to different pathogens. Immunology 2005; 116:245-254.
30. Veerapathran A, Pidala J, Beato F, Yu X, Anasetti C. Ex vivo expansion of human Tregs specific for alloantigens presented. Blood 2011; 118:5671-5680.
31. Schulz O, Edwards AD, Schito M etal. CD40 triggering of heterodimeric IL-12 p70 production by dendritic cells in vivo requires a microbial priming signal. Immunity 2000; 4:453-462.
32. Wilson KT, Crabtree JE. Immunology of Helicobacter pylori: insights into the failure of the immune response and perspectives on vaccine studies. Gastroenterology 2007; 133:288-308.
33. Necchi V, Candusso ME, Tava F etal. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology 2007; 132:1009-1023.
34. Cooke CL, Huff JL, Solnick JV. The role of genome diversity and immune evasion in persistent infection with Helicobacter pylori. FEMS Immunol Med Microbiol 2005; 45:11-23.
35. Algood HM, Cover TL. Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin Microbiol Rev 2006; 19:597-613.
36. Kabir S. The role of interleukin-17 in the Helicobacter pylori induced infection and immunity. Helicobacter 2011; 16:1-8.
37. Baldwin AS. Series introduction: the transcription factor NF-kappaB and human disease. J Clin Invest 2001; 107:3-6.
38. Wallace JL, Cucala M, Mugridge K, Parente L. Secretagogue-specific effects of interleukin-1 on gastric acid secretion. Am J Physiol 1991; 261:559-564.
39. Kondo S, Shinomura Y, Kanayama S etal. Interleukin-1 beta inhibits gastric histamine secretion and synthesis in the rat. Am J Physiol 1994; 267:966-971.
40. Huang FY, Chan AO, Rashid A, Wong DK, Cho CH, Yuen MF. Helicobacter pylori induces promoter methylation of E-cadherin via interleukin-1β activation of nitric oxide production in gastric cancer cells. Cancer 2012. Epub ahead of print.
41. Zambon CF, Basso D, Navaglia F etal. Helicobacter pylori virulence genes and host IL-1RN and IL-1beta genes interplay in favouring the development of peptic ulcer and intestinal metaplasia. Cytokine 2002; 18:242-251.
42. Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 2003; 197:403-411.
43. Peng G, Guo Z, Kiniwa Y etal. Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science 2005; 309:1380-1384.
44. Liu H, Komai-Koma M, Xu D, Liew FY. Toll-like receptor 2 signaling modulates the functions of CD4+ CD25+ regulatory T cells. Proc Natl Acad Sci U S A 2006; 103:7048-7053.
45. Peek RM Jr, Miller GG, Tham KT etal. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest 1995; 73:760-770.
46. Kondo S, Shinomura Y, Kanayama S etal. Interleukin-1 beta inhibits gastric histamine secretion and synthesis in the rat. Am J Physiol 1994; 267:G966-971.
47. Persson C, Canedo P, Machado JC, El-Omar EM, Forman D. Polymorphisms in inflammatory response genes and their association with gastric cancer: a HuGE systematic review and meta-analyses. Am J Epidemiol 2011; 173:259-270.
48. Sugimoto M, Furuta T, Yamaoka Y. Influence of inflammatory cytokine polymorphisms on eradication rates of Helicobacter pylori. J Gastroenterol Hepatol 2009; 24:1725-1732.
49. Doganci A, Eigenbrod T, Krug N etal. The IL-6R alpha chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. J Clin Invest 2005; 115:313-325.
50. Nadkarni S, Mauri C, Ehrenstein MR, Anti TN. F-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta. J Exp Med 2007; 204:33-39.
51. Afzali B, Mitchell P, Lechler RI, John S, Lombardi G. Translational mini-review series on Th17 cells: induction of interleukin-17 production by regulatory T cells. Clin Exp Immunol 2010; 159:120-130.
52. 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.
53. Oertli M, Sundquist M, Hitzler I etal. DC-derived IL-18 drives Treg differentiation, murine Helicobacter pylori-specific immune tolerance, and asthma protection. J Clin Invest 2012; 112:1082-1096.
54. Kim JM, Kim JS, Yoo DY etal. Stimulation of dendritic cells with Helicobacter pylori vacuolating cytotoxin negatively regulates their maturation via the restoration of E2F1. Clin Exp Immunol 2011; 166:34-45.
55. Drakes ML, Czinn SJ, Blanchard TG. Regulation of murine dendritic cell immune responses by Helicobacter felis antigen. Infect Immun 2006; 74:4624-4633.
56. Kranzer K, Eckhardt A, Aigner M etal. Induction of maturation and cytokine release of human dendritic cells by Helicobacter pylori. Infect Immun 2004; 72:4416-4423.
57. Nishi T, Okazaki K, Kawasaki K etal. Involvement of myeloid dendritic cells in the development of gastric secondary lymphoid follicles in Helicobacter pylori-infected neonatally thymectomized BALB/c mice. Infect Immun 2003; 71:2153-2162.