Helicobacter pylori stimulates a mixed adaptive immune response with a strong T-regulatory component in human gastric mucosa

Helicobacter

Volumn 12, Issue 3, 2007, Pages 185-192

  Goll, Rasmus ^a,b   Gruber, Franz ^a   Olsen, Trine ^a   Cui, Guanglin ^a   Raschpichler, Gabriele ^b   Buset, Magne ^b   Asfeldt, Anne M ^b   Husebekk, Anne ^a,b   Florholmen, Jon ^a,b  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

Gene expression profiling; Helicobacter pylori; Immunity; Lymphocyte subsets; Mucosal; Polymerase chain reaction

Indexed keywords

CAGA PROTEIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ADULT; AGED; ARTICLE; COMORBIDITY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DUODENUM ULCER; ENDOSCOPY; FEMALE; GASTRITIS; GENE EXPRESSION PROFILING; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; PEPTIC ULCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SAMPLE; STOMACH BIOPSY; STOMACH MUCOSA; TH1 CELL; TH2 CELL;

CYTOKINES; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, MUCOSAL; INTERLEUKIN-10; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH2 CELLS;

HELICOBACTER PYLORI;

EID: 34247843045     PISSN: 10834389     EISSN: 15235378     Source Type: Journal    
DOI: 10.1111/j.1523-5378.2007.00495.x     Document Type: Article

References (45)

1. Blaser MJ. The role of Helicobacter pylori in gastritis and its progression to peptic ulcer disease. Aliment Pharmacol Ther 1995 9 (Suppl. 1): S27 S30.
2. Go MF. Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 2002 16 (Suppl. 1): S3 S15.
3. Yamaoka Y, Kodama T, Kita M, Imanishi J, Kashima K, Graham DY. Relation between clinical presentation, Helicobacter pylori density, interleukin 1beta and 8 production, and cagA status. Gut 1999 45: 804 11.
4. Supajatura V, Ushio H, Wada A, Yahiro K, Okumura K, Ogawa H, Hirayama T, Ra C. Cutting edge: VacA, a vacuolating cytotoxin of Helicobacter pylori, directly activates mast cells for migration and production of proinflammatory cytokines. J Immunol 2002 168: 2603 7.
5. Peek RM Jr., Miller GG, Tham KT, Perez-Perez GI, Zhao X, Atherton JC, Blaser MJ. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest 1995 73: 760 70.
6. Graham DY, Yamaoka Y. Disease-specific Helicobacter Pylori virulence factors: the unfulfilled promise. Helicobacter 2000 5 (Suppl. 1): S3 S9.
7. Ernst PB, Gold BD. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol 2000 54: 615 40.
8. Fan XG, Yakoob J, Fan XJ, Keeling PW. Enhanced T-helper 2 lymphocyte responses: immune mechanism of Helicobacter pylori infection. Ir J Med Sci 1996 165: 37 9.
9. Lohoff M, Rollinghoff M, Sommer F. Helicobacter pylori gastritis: a Th1 mediated disease? J Biotechnol 2000 83: 33 6.
10. D'Elios MM, Manghetti M, De Carli M, Costa F, Baldari CT, Burroni D, Telford JL, Romagnani S, Del Prete G. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J Immunol 1997 158: 962 7.
11. Sommer F, Faller G, Konturek P, Kirchner T, Hahn EG, Zeus J, Rollinghoff M, Lohoff M. Antrum- and corpus mucosa-infiltrating CD4(+) lymphocytes in Helicobacter pylori gastritis display a Th1 phenotype. Infect Immun 1998 66: 5543 6.
12. Bamford KB, Fan X, Crowe SE, Leary JF, Gourley WK, Luthra GK, Brooks EG, Graham DY, Reyes VE, Ernst PB. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998 114: 482 92.
13. Luzza F, Parrello T, Sebkova L, Pensabene L, Imeneo M, Mancuso M, La Vecchia AM, Monteleone G, Strisciuglio P, Pallone F. Expression of proinflammatory and Th1 but not Th2 cytokines is enhanced in gastric mucosa of Helicobacter pylori infected children. Dig Liver Dis 2001 33: 14 20.
14. Valnes K, Brandtzaeg P, Elgjo K, Stave R. Quantitative distribution of immunoglobulin-producing cells in gastric mucosa: relation to chronic gastritis and glandular atrophy. Gut 1986 27: 505 14.
15. Goll R, Husebekk A, Isaksen V, Kauric G, Hansen T, Florholmen J. Increased frequency of antral CD4 T and CD19 B cells in patients with Helicobacter pylori-related peptic ulcer disease. Scand J Immunol 2005 61: 92 7.
16. Ong SP, Duggan A. Eradication of Helicobacter pylori in clinical situations. Clin Exp Med 2004 4: 30 8.
17. Cui G, Olsen T, Christiansen I, Vonen B, Florholmen J, Goll R. Improvement of real-time polymerase chain reaction for quantifying TNF-alpha mRNA expression in inflamed colorectal mucosa: An approach to optimize procedures for clinical use. Scand J Clin Lab Invest 2006 66: 249 59.
18. Goll R, Olsen T, Cui G, Florholmen J. Evaluation of absolute quantitation by nonlinear regression in probe-based real-time PCR. BMC Bioinformatics 2006 7: 107.
19. Blomstergren A, Lundin A, Nilsson C, Engstrand L, Lundeberg J. Comparative analysis of the complete cag pathogenicity island sequence in four Helicobacter pylori isolates. Gene 2004 328: 85 93.
20. Alm RA, Ling LS, Moir DT, et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999 397: 176 80.
21. Tomb JF, White O, Kerlavage AR, et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997 388: 539 47.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T) Method. Methods 2001 25: 402 8.
23. Kassai K, Yoshikawa T, Yoshida N, Hashiramoto A, Kondo M, Murase H. Helicobacter pylori water extract induces interleukin-8 production by gastric epithelial cells. Dig Dis Sci 1999 44: 237 42.
24. Gionchetti P, Vaira D, Campieri M, Holton J, Menegatti M, Belluzzi A, Bertinelli E, Ferretti M, Brignola C, Miglioli M. Enhanced mucosal interleukin-6 and -8 in Helicobacter pylori-positive dyspeptic patients. Am J Gastroenterol 1994 89: 883 7.
25. Lindholm C, Quiding-Jarbrink M, Lonroth H, Hamlet A, Svennerholm AM. Local cytokine response in Helicobacter pylori-infected subjects. Infect Immun 1998 66: 5964 71.
26. Yamaoka Y, Kita M, Kodama T, Sawai N, Kashima K, Imanishi J. Induction of various cytokines and development of severe mucosal inflammation by cagA gene positive Helicobacter pylori strains. Gut 1997 41: 442 51.
27. Lin SN, Ayada K, Zhao Y, et al. Helicobacter pylori heat-shock protein 60 induces production of the pro-inflammatory cytokine IL8 in monocytic cells. J Med Microbiol 2005 54: 225 33.
28. Crabtree JE, Lindley IJ. Mucosal interleukin-8 and Helicobacter pylori-associated gastroduodenal disease. Eur J Gastroenterol Hepatol 1994 6 (Suppl. 1): S33 S38.
29. Lindholm C, Quiding-Jarbrink M, Lonroth H, Svennerholm AM. Induction of chemokine and cytokine responses by Helicobacter pylori in human stomach explants. Scand J Gastroenterol 2001 36: 1022 9.
30. Bauditz J, Ortner M, Bierbaum M, Niedobitek G, Lochs H, Schreiber S. Production of IL-12 in gastritis relates to infection with Helicobacter pylori. Clin Exp Immunol 1999 117: 316 23.
31. Meyer F, Wilson KT, James SP. Modulation of innate cytokine responses by products of Helicobacter pylori. Infect Immun 2000 68: 6265 72.
32. Fera MT, Carbone M, Buda C, Aragona M, Panetta S, Giannone M, La Torre F, Giudice A, Losi E. Correlation between Helicobacter pylori infection and IL-18 mRNA expression in human gastric biopsy specimens. Ann NY Acad Sci 2002 963: 326 8.
33. Itoh T, Wakatsuki Y, Yoshida M, Usui T, Matsunaga Y, Kaneko S, Chiba T, Kita T. The vast majority of gastric T cells are polarized to produce T helper 1 type cytokines upon antigenic stimulation despite the absence of Helicobacter pylori infection. J Gastroenterol 1999 34: 560 70.
34. Mills KH. Regulatory T cells: friend or foe in immunity to infection? Nat Rev Immunol 2004 4: 841 55.
35. Tomita T, Jackson AM, Hida N, Hayat M, Dixon MF, Shimoyama T, Axon AT, Robinson PA, Crabtree JE. Expression of Interleukin-18, a Th1 cytokine, in human gastric mucosa is increased in Helicobacter pylori infection. J Infect Dis 2001 183: 620 7.
36. Bhat N, Gaensbauer J, Peek RM, Bloch K, Tham KT, Blaser MJ, Perez-Perez G. Local and systemic immune and inflammatory responses to Helicobacter pylori strains. Clin Diagn Lab Immunol 2005 12: 1393 400.
37. Hida N, Shimoyama T Jr., Neville P, Dixon MF, Axon AT, Shimoyama T, Sr., Crabtree JE. Increased expression of IL-10 and IL-12 (p40) mRNA in Helicobacter pylori infected gastric mucosa: relation to bacterial cag status and peptic ulceration. J Clin Pathol 1999 52: 658 64.
38. Yamaoka Y, Kita M, Kodama T, Sawai N, Imanishi J. Helicobacter pylori cagA gene and expression of cytokine messenger RNA in gastric mucosa. Gastroenterology 1996 110: 1744 52.
39. Bergman MP, Engering A, Smits HH, van Vliet SJ, van Bodegraven AA, Wirth HP, Kapsenberg ML, Vandenbroucke-Grauls CM, van Kooyk Y, Appelmelk BJ. Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 2004 200: 979 90.
40. Engstrand L, Graham D, Scheynius A, Genta RM, El Zaatari F. Is the sanctuary where Helicobacter pylori avoids antibacterial treatment intracellular? Am J Clin Pathol 1997 108: 504 9.
41. Bjorkholm B, Zhukhovitsky V, Lofman C, Hulten K, Enroth H, Block M, Rigo R, Falk P, Engstrand L. Helicobacter pylori entry into human gastric epithelial cells: a potential determinant of virulence, persistence, and treatment failures. Helicobacter 2000 5: 148 54.
42. Raghavan S, Holmgren J. CD4+CD25+ suppressor T cells regulate pathogen induced inflammation and disease. FEMS Immunol Med Microbiol 2005 44: 121 7.
43. Bodger K, Wyatt JI, Heatley RV. Gastric mucosal secretion of interleukin-10: relations to histopathology, Helicobacter pylori status, and tumour necrosis factor-alpha secretion. Gut 1997 40: 739 44.
44. Holck S, Norgaard A, Bennedsen M, Permin H, Norn S, Andersen LP. Gastric mucosal cytokine responses in Helicobacter pylori-infected patients with gastritis and peptic ulcers. Association with inflammatory parameters and bacteria load. FEMS Immunol Med Microbiol 2003 36: 175 80.
45. Bodger K, Bromelow K, Wyatt JI, Heatley RV. Interleukin 10 in Helicobacter pylori associated gastritis: immunohistochemical localisation and in vitro effects on cytokine secretion. J Clin Pathol 2001 54: 285 92.