Downregulated Th17 responses are associated with reduced gastritis in Helicobacter pylori-infected children

Mucosal Immunology

Volumn 6, Issue 5, 2013, Pages 950-959

  Serrano, C ^a   Wright, S W ^b   Bimczok, D ^b   Shaffer, C L ^c,d   Cover, T L ^c,d   Venegas, A ^a   Salazar, M G ^e   Smythies, L E ^b   Harris, P R ^a   Smith, P D ^b,f  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b University of Alabama   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e University of Alabama at Birmingham   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3;

ADOLESCENT; ADULT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CAGA GENE; CELL ACTIVATION; CELL COUNT; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DOWN REGULATION; FEMALE; GASTRITIS; GENE FREQUENCY; GENOTYPE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; LAMINA PROPRIA; MALE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH MUCOSA; TH17 CELL; VACA GENE;

ADOLESCENT; ADULT; CHILD; DISEASE PROGRESSION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GASTRIC MUCOSA; GASTRITIS; GENE EXPRESSION REGULATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INTERLEUKIN-10; INTERLEUKIN-17; MALE; MIDDLE AGED; NEUTROPHILS; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; VIRULENCE FACTORS;

EID: 84875320712     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2012.133     Document Type: Article

References (51)

1. Mohammadi,M., Czinn, S., Redline, R. & Nedrud, J. Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotye and promote a delayed-type hypersensitivity response in the stomachs of mice. J. Immunol. 156, 4729-4738 (1996
2. Smythies, L.E.,Waites, K.B., Lindsey, R.J., Harris, P.R., Ghiara, P. & Smith, P.D. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-g, gene-deficient mice. J. Immunol. 165, 1022-1029 (2000
3. Mattapallil, J.J., Dandekar, S., Canfield, D.R. & Solnick, J.V. A predominant Th1 type of immune response is induced early during acute Helicobacter pylori infection in rhesus macaques. Gastroenterology 118, 307-315 (2000
4. Karttunen, R., Karttunen, T., Ekre, H-P.T. & MacDonald, T.T. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut 36, 341-345 (1995
5. Haeberle, H.A. et al. Differential stimulation of interleukin-12 (IL-12) and IL-10 by live and killed Helicobacter pylori in vitro and association of IL-12 production with g interferon-producing T cells in the human gastric mucosa. Infect. Immun. 65, 4229-4235 (1997
6. D'Elios, M.M. et al. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J. Immunol. 158, 962-967 (1997
7. Bamford, K.B. et al. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 114, 482-492 (1998
8. Harris, P.R. et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 134, 491-499 (2008
9. Guiraldes, E. et al. Proinflammatory cytokine expression in gastric tissue from children with Helicobacter pylori-Associated gastritis. J. Pediatr. Gastroenterol. Nutr. 33, 127-132 (2001
10. Whitney, A.E., Guarner, J., Hutwagner, L. & Gold, B.D. Helicobacter pylori gastritis in children and adults: Comparative histopathologic study. Ann. Diagn. Pathol. 4, 279-285 (2000
11. Lundgren, A. et al. Mucosal FOXP3-expressing CD4+ CD25high regulatory T cells in Helicobacter pylori-infected patients. Infect. Immun. 73 523-531 (2005
12. Robinson, K. et al. Helicobacter pylori-induced peptic ulcer disease is associated with inadequate regulatory T cell responses. Gut 57, 1375-1385 (2008
13. Raghavan, S., Fredriksson, M., Svennerholm, A.M., Holmgren, J. & Suri-Payer, E. 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. 132, 393-400 (2003
14. Rad, R. et al. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 131, 525-537 (2006
15. Alam,M.S. et al.CD73 is expressed by human regulatory T helper cells and suppresses proinflammatory cytokine production and Helicobacter felisinduced gastritis in mice. J. Infect. Dis. 199, 494-504 (2009
16. Shiomi, S. et al. IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Helicobacter 13, 518-524 (2008
17. Algood, H.M., Gallo-Romero, J., Wilson, K.T., Peek, R.M. Jr & Cover, T.L. Host response to Helicobacter pylori infection before initiation of the adaptive immune response. FEMS Immunol. Med. Microbiol. 51, 577-586 (2007
18. Kao, J.Y. et al. Helicobacter pylori immune escape is mediated by dendritic cell-induced Treg skewing and Th17 suppression in mice. Gastroenterology 138, 1046-1054 (2010
19. Fox, J.G. & Wang, T.C. Inflammation, atrophy, and gastric cancer. J. Clin. Invest. 117, 60-69 (2007
20. Falush, D. et al. Traces of human migrations in Helicobacter pylori populations. Science 299, 1582-1585 (2003
21. Linz, B. et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445, 915-918 (2007
22. Caruso, R. et al. IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol. 38, 470-478 (2008
23. Kraft, C. et al. Genomic changes during chronic Helicobacter pylori infection. J. Bacteriol. 188, 249-254 (2006
24. Cruz-Coke, R.&Moreno, R.S. Genetic epidemiology of single gene defects in Chile. J. Med. Genet. 31, 702-706 (1994
25. Medina, E.L. & Kaempffer, A.M.R. Elementos de Salud Publica. Biblioteca Digital. Universidad de Chile2011). Section 5.2.6
26. National Administration Department of Statistics (DANE). Government of Columbia (2007
27. de Sablet, T. et al. Phylogeographic origin of Helicobacter pylori is a determinant of gastric cancer risk. Gut 60, 1189-1195 (2011
28. Basso, D. et al. Clinical relevance of Helicobacter pylori cagA and vacA gene polymorphisms. Gastroenterology 135, 91-99 (2008
29. Blaser,M.J. et al. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55, 2111-2115 (1995
30. Mangan, P.R. et al. Transforming growth factor-b induces development of the T(H)17 lineage. Nature 441, 231-234 (2006
31. Weaver, C.T., Hatton, R.D., Mangan, P.R. & Harrington, L.E. IL-17 family cytokines and the expanding diversity of effector Tcell lineages. Annu. Rev. Immunol. 25, 821-852 (2007
32. Ouyang, W., Kolls, J.K. & Zheng, Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467 (2008
33. Bodger, K., Bromelow, K., Wyatt, J.I. & Heatley, R.V. Interleukin 10 in Helicobacter pylori associated gastritis: Immunohistochemical localisation and in vitro effects on cytokine secretion. J. Clin. Pathol. 54, 285-292 (2001
34. Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238 (2006
35. Quintana, F.J. et al. Control of Treg and TH17 cell differentiation by the aryl hydrocarbon receptor. Nature 453, 65-71 (2008
36. Mucida, D. et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260 (2007
37. Ivanov, I.I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349 (2008
38. Zhang, M., Liu, M., Luther, J. & Kao, J.Y. Helicobacter pylori directs tolerogenic programming of dendritic cells. Gut Microbes 1, 325-329 (2010
39. Bimczok, D. et al. Human primary gastric dendritic cells induce a Th1 response to H. pylori. Mucosal Immunol. 3, 260-269 (2010
40. Bimczok, D., Grams, J.M., Stahl, R.D., Waites, K.B., Smythies, L.E. & Smith, P.D. Stromal regulation of human gastric dendritic cells restricts the Th1 response to Helicobacter pylori. Gastroenterology 141, 929-938 (2011
41. Smythies, L.E. et al. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115, 66-75 (2005
42. Smythies, L.E. et al. Inflammation anergy in human intestinal macrophages is due to Smad-induced IkBa expression and NF-kB inactivation. J. Biol. Chem. 285, 19593-19604 (2010
43. DeLyria, E.S., Redline, R.W. & Blanchard, T.G. Vaccination of mice against H pylori induces a strong Th-17 response and immunity that is neutrophil dependent. Gastroenterology 136, 247-256 (2009
44. Velin, D. et al. Interleukin-17 is a critical mediator of vaccine-induced reduction of Helicobacter infection in the mouse model. Gastroenterology 136, 2237-2246 (2009
45. Hitzler, I., Oertli, M., Becher, B., Agger, E.M. & Muller, A. Dendritic cells prevent rather than promote immunity conferred by a helicobacter vaccine using a mycobacterial adjuvant. Gastroenterology 141, 186-196 (2011
46. Dixon, M.F., Genta, R.M., Yardley, J.H. & Correa, P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am. J. Surg. Pathol. 20, 1161-1181 (1996
47. van Doorn, L.J. et al. Expanding allelic diversity of Helicobacter pylori vacA. J. Clin. Microbiol. 36, 2597-2603 (1998
48. Sicinschi, L.A., Correa, P., Bravo, L.E. & Schneider, B.G. A positive assay for identification of cagA negative strains of Helicobacter pylori. J. Microbiol. Methods 55, 625-633 (2003
49. Rudi, J. et al. Diversity of Helicobacter pylori vacA and cagA genes and relationship to VacA and CagA protein expression, cytotoxin production, and associated diseases. J. Clin. Microbiol. 36, 944-948 (1998
50. Achtman, M. et al. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol. 32, 459-470 (1999
51. Tamura, K., Dudley, J., Nei, M. & Kumar, S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599 (2007