Skip to main content

Effects of infection with Helicobacter pylori on gastric epithelium

  • Chapter
Helicobacter pylori
  • 74 Accesses

Abstract

There is growing evidence to support a key role for the gastric epithelium in the pathogenesis of Helicobacter pylori-associated gastroduodenal disorders. H. pylori is largely regarded as a non-invasive pathogen, yet is capable of inducing a significant inflammatory response. The concept that the epithelium could play an active role in H. pylori-associated inflammation has been substantiated over the past few years by work from several laboratories (reviewed by others in refs 1 and 2). In these studies gastric epithelial production of interleukin-8 (IL-8), a cytokine with potent neutrophil chemotactic and activating properties3,4, was significantly increased during H. pylori infection5–9. More recent data suggest that other chemokines including members of the C-C family that stimulate lymphocytes and monocytes/macrophages, are also expressed by gastric epithelial cells in response to H. pylori infection. Gastric epithelial cells are also capable of interacting with immune and inflammatory cells through adhesion or immune accessory molecules including Class II MHC, invariant chain (Ii), intracellular adhesion molecule (ICAM)-1, lymphocyte function antigen (LFA)-3, and B7. Expression of such molecules is increased by H. pylori infection with both direct and indirect events involved in the enhanced expression. Together, this information provides a basis to establish potential mechanisms whereby the epithelium can signal immune cells to establish the gastritis associated with H. pylori infection. In turn, immune or inflammatory cells may mediate alterations of the gastric epithelium that occur during H. pylori infection.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Dixon MF. Pathophysiology of Helicobacter pylori infection. Scand J Gastroenterol. 1994;29: 7–10.

    Article  Google Scholar 

  2. Ernst PB, Crowe SE, Reyes VE. The immunopathogenesis of gastroduodenal disease associated with Helicobacter pylori infection. Curr Opin Gastroenterol. 1995; 11:512–18.

    Article  CAS  Google Scholar 

  3. Oppenheim JJ, Zachariae COC, Mukaida N, Matsushima K. Properties of the novel proinflammatory supergene ‘intercrine’ cytokine family. Annu Rev Immunol. 1991;9:617–48.

    Article  PubMed  CAS  Google Scholar 

  4. Bagglioni M, Walz A, Kunkel SL. Neutrophil-activating peptide/interleukin 8, a novel cytokine that activates neutrophils. J Clin Invest. 1989;84:1045–9.

    Article  Google Scholar 

  5. Crabtree JE, Wyatt JI, Trejdosiewicz LK et al. Interleukin-8 expression in Helicobacter pylori infected, normal, and neoplastic gastroduodenal mucosa. J Clin Pathol. 1994;47:61–6.

    Article  PubMed  CAS  Google Scholar 

  6. Moss SF, Legon S, Davies J, Calam J. Cytokine gene expression in Helicobacter pylori associated antral gastritis. Gut. 1995;35:1567–70.

    Article  Google Scholar 

  7. Peek RM, Miller GG, Tham KT et al. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab Invest. 1995;71:760–70.

    Google Scholar 

  8. Fan XG, Chua A, Fan XJ, Keeling PW. Increased gastric production of interleukin-8 and tumour necrosis factor in patients with Helicobacter pylori infection. J Clin Pathol. 1995;48:133–6.

    Article  PubMed  CAS  Google Scholar 

  9. Crabtree JE, Lindley IJD. Mucosal interleukin-8 and Helicobacter pylori-associated gastroduodenal disease. Eur J Gastroenterol Hepatol. 1995;6:S33–8.

    Google Scholar 

  10. Crabtree JE, Peichl P, Wyatt JI, Stachl U, Lindley IJD. Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection. Scand J Immunol. 1993;37:65–70.

    Article  PubMed  CAS  Google Scholar 

  11. Crabtree JE, Farmery SM, Lindley IJD, Figura N, Peichl P, Tompkins DS. CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J Clin Pathol. 1994;47:945–50.

    Article  PubMed  CAS  Google Scholar 

  12. Crowe SE, Alvarez L, Dytoc M et al. Expression of interleukin-8 and CD54 by human gastric epithelium after Helicobacter pylori infection in vitro. Gastroenterology. 1995;108:65–74.

    Article  PubMed  CAS  Google Scholar 

  13. Sharma SA, Tummuru MKR, Miller GG, Blaser MJ. Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro. Infect Immun. 1995;63:1681–7.

    PubMed  CAS  Google Scholar 

  14. Huang J, O’Toole PW, Doig P, Trust TJ. Stimulation of interleukin-8 production in epithelial cell lines by Helicobacter pylori. Infect Immun. 1995;63:1732–8.

    PubMed  CAS  Google Scholar 

  15. Crabtree JE, Xiang Z, Lindley IJD, Tompkins DS, Rappuoli R, Covacci A. Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori. J Clin Pathol. 1995;48:967–9.

    Article  PubMed  CAS  Google Scholar 

  16. Geiser T, Dewald B, Ehrengruber MU, Clark-Lewis I, Baggiolini M. The interleukin-8-related chemotactic cytokines GROα, GROβ, and GRO activate human neutrophil and basophil leukocytes. J Biol Chem. 1993;268:15419–24.

    PubMed  CAS  Google Scholar 

  17. Yamaoka Y, Kita M, Kodama T, Sawai N, Kashima K, Imanishi J. Expression of chemokine mRNA in gastric mucosa with Helicobacter pylori infection. Gastroenterology. 1996; 110: A1049(abstract).

    Article  Google Scholar 

  18. Takizawa H, Azuma A, Aihara M et al. Helicobacter pylori-induced chemokines production in human gastric carcinoma cell lines: effects of rebapimide. Gastroenterology. 1996;110:A272 (abstract).

    Google Scholar 

  19. Jung HC, Kim JM, Song IS, Kim CY. Increased motility of Helicobacter pylori by methyl-cellulose could upregulate the expression of proinflammatory cytokines in human gastric epithelial cells. Gastroenterology. 1996; 110: A146(abstract).

    Google Scholar 

  20. Eckmann L, Jung HC, Schurer-Maly C, Panja A, Morzycka-Wroblewska E, Kagnoff MF. Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology. 1993;105:1689–97.

    PubMed  CAS  Google Scholar 

  21. Jung HC, Eckmann L, Yang S-K et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest. 1995;95:55–65.

    Article  PubMed  CAS  Google Scholar 

  22. Mayer L, Eisenhardt D, Salomon P, Bauer W, Pious R, Piccinini L. Expression of class II molecules on intestinal epithelial cells in humans. Differences between normal and inflammatory bowel disease. Gastroenterology. 1991; 100:3–12.

    PubMed  CAS  Google Scholar 

  23. Engstrand L, Scheynius A, Pathlson C, Grimelius L, Schwan S. Association of Campylobacter pylori with induced expression of class II transplantation antigens on gastric epithelial cells. Infect Immun. 1989;57:827–32.

    PubMed  CAS  Google Scholar 

  24. Vaines K, Huitfeldt HS, Brandtzaeg P. Relation between T cell number and epithelial HLA class II expression quantified by image analysis in normal and inflamed human gastric mucosa. Gut. 1990;31:647–52.

    Article  Google Scholar 

  25. Chiba M, Ishii N, Ishioka T et al. Topographic study of Helicobacter pylori and HLA-DR antigen expression on gastric epithelium. J Gastroenterol. 1995;30:149–55.

    Article  PubMed  CAS  Google Scholar 

  26. Scheynius A, Engstrand L. Gastric epithelial cells in Helicobacter pylori-associated gastritis express HLA-DR but not ICAM-1. Scand J Immunol. 1991;33:237–41.

    Article  PubMed  CAS  Google Scholar 

  27. Sakai K, Takiguchi M, Mori S et al. Expression and function of class II antigens on gastric carcinoma cells and gastric epithelia: differential expression of DR, DQ, and DP antigens. J Natl Cancer Inst. 1987;79:923–32.

    PubMed  CAS  Google Scholar 

  28. Noach LA, Bosma NB, Jansen J, Hoek FJ, van-Deventer SJ, Tytgat GN. Mucosal tumor necrosis factor-alpha, interleukin-1 beta and interleukin-8 production in patients with Helicobacter pylori. Scand J Gastroenterol. 1994;29:425–9.

    Article  PubMed  CAS  Google Scholar 

  29. Karttunen R, Karttunen T, Ekre H-PT, Macdonald TT. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut. 1995;36:341–5.

    Article  PubMed  CAS  Google Scholar 

  30. Yamaoka Y, Kita M, Kodama T, Sawai N, Imanishi J. Helicobacter pylori cagA gene and expression of cytokine messenger mRNA in gastric mucosa. Gastroenterology. 1996;110:1744–52.

    Article  PubMed  CAS  Google Scholar 

  31. Springer TA. Adhesion receptors of the immune system. Nature. 1990;346:425–34.

    Article  PubMed  CAS  Google Scholar 

  32. Norton J, Sloane JP, Al-Saffar N, Haskard DO. Expression of adhesion molecules in human intestinal graft-versus-host disease. Clin Exp Immunol. 1992;87:231–6.

    Article  PubMed  CAS  Google Scholar 

  33. Nakamura S, Ohtani H, Watanabe Y et al. In situ expression of the cell adhesion molecules in inflammatory bowel disease. Evidence of immunologic activation of vascular endothelial cells. Lab Invest. 1993;69:77–85.

    PubMed  CAS  Google Scholar 

  34. Kaiserlian D, Rigal D, Abello J, Revillard J-P. Expression, function and regulation of the intercellular adhesion molecule-1 (ICAM-1) on human intestinal epithelial cell lines. Eur J Immunol. 1991;21:2415–21.

    Article  PubMed  CAS  Google Scholar 

  35. Fan XG, Fan XJ, Xia HX, Keeling PWN, Kelleher D. Up-regulation of CD44 and ICAM-1 expression on gastric epithelial cells by H. pylori. APMIS. 1995;103:744–8.

    Article  PubMed  CAS  Google Scholar 

  36. Vidal K, Samarut C, Magaud J-P, Revillard J-P, Kaiserlian D. Unexpected lack of reactivity of allogeneic anti-la monoclonal antibodies with MHC class II molecules expressed by mouse intestinal epithelial cells. J Immunol. 1993;151:4642–50.

    PubMed  CAS  Google Scholar 

  37. Kelly CP, O’Keana JC, Orellana J et al. Human colon cancer cells express ICAM-1 in vivo and support LFA-1-dependent lymphocyte adhesion in vitro. Am J Physiol. 1992;263:G864–70.

    PubMed  CAS  Google Scholar 

  38. Parkos CA, Colgan SP, Madara JL. Interactions of PMN with epithelial cells: lessons from the intestine. J Am Soc Nephrol. 1994;5:138–52.

    PubMed  CAS  Google Scholar 

  39. Kvale D, Krajci P, Brandtzaeg P. Expression and regulation of adhesion molecules ICAM-1 (CD54) and LFA-3 (CD 58) in human intestinal epithelial cell lines. Scand J Immunol. 1992;35: 669–76.

    Article  PubMed  CAS  Google Scholar 

  40. Bluestone JA. New perspectives of CD28-B7-mediated T cell costimulation. Cell. 1995;81: 555–9.

    Google Scholar 

  41. Hagerty DT, Evavoid BD, Allen PM. Regulation of the costimulatory B7, not class II major histocompatibility complex, restricts the ability of murine kidney tubule cells to stimulate CD4+ T cells. J Clin Invest. 1994;93:1208–15.

    Article  PubMed  CAS  Google Scholar 

  42. Lee A, Dixon MF, Danon SJ et al. Local acid production and Helicobacter pylori: a unifying hypothesis of gastroduodenal disease. Eur J Gastroenterol Hepatol. 1995;7:461–5.

    PubMed  CAS  Google Scholar 

  43. McGowan CC, Cover TL, Blaser MJ. Helicobacter pylori and gastric acid: biological and therapeutic implications. Gastroenterology. 1996;110:926–38.

    Article  PubMed  CAS  Google Scholar 

  44. Micots I, Augeron C, Laboisse CL, Muzeau F, Megraud F. Mucin exocytosis: a major target for Helicobacter pylori. J Clin Pathol. 1993;46:241–5.

    Article  PubMed  CAS  Google Scholar 

  45. Goggin PM, Marrero JM, Spychal RT, Jackson PA, Corbishley CM, Northfield TC. Surface hydrophobicity of gastric mucosa in Helicobacter pylori infection: effect of clearance and eradication. Gastroenterology. 1992;103:1486–90.

    PubMed  CAS  Google Scholar 

  46. Go MF, Lew GM, Lichtenberger LM, Genta RM, Graham DY. Gastric mucosal hydrophobicity and Helicobacter pylori: response to antimicrobial therapy. Am J Gastroenterol. 1993;88:1362–5.

    PubMed  CAS  Google Scholar 

  47. Lichtenberger LM, Romero JJ. Effect of ammonium ion on the hydrophobic and barrier properties of the gastric mucus gel layer: implications on the role of ammonium in H. pylori-induced gastritis. J Gastroenterol Hepatol. 1994;9:S13–19.

    Article  PubMed  Google Scholar 

  48. Markesich DC, Anand BS, Lew GM, Graham DY. Helicobacter pylori infection does not reduce the viscosity of human gastric mucus gel. Gut. 1995;36:327–9.

    Article  PubMed  CAS  Google Scholar 

  49. Hatz RA, Bloch KJ, Harmatz PR et al. Divalent hapten-induced intestinal anaphylaxis in the mouse enhances macromolecular uptake from the stomach. Gastroenterology. 1990;98:894–900.

    Article  PubMed  CAS  Google Scholar 

  50. Catto-Smith AG, Patrick MK, Scott RB, Davison JS, Gall DG. Gastric response to mucosal IgE-mediated reactions. Am J Physiol. 1989;257:G704–8.

    PubMed  CAS  Google Scholar 

  51. Sutherland LR, Verhoef M, Wallace JL, Van Rosendaal G, Crutcher R, Meddings JB. A simple, non-invasive marker of gastric damage: sucrose permeability. Lancet. 1994;343:998–1000.

    Article  PubMed  CAS  Google Scholar 

  52. Graham DY, Malaty HM, Goodgame R, Ou CN. Effect of cure of H. pylori infection on the gastric mucosal permeability. Gastroenterology. 1996;110:A122(abstract).

    Google Scholar 

  53. Madara JL. Loosening tight junctions: lessons from the intestine. J Clin Invest. 1989;83:1089–94.

    Article  PubMed  CAS  Google Scholar 

  54. Madara JL. Pathobiology of the intestinal epithelial barrier. Am J Pathol. 1990;137:1273–81.

    PubMed  CAS  Google Scholar 

  55. Madara JL, Stafford J. Interferon-γ directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest. 1989;83:724–7.

    Article  PubMed  CAS  Google Scholar 

  56. Colgan SP, Resnick MB, Parkos CA et al. IL-4 directly modulates function of a model human intestinal epithelium. J Immunol. 1994;153:2122–9.

    PubMed  CAS  Google Scholar 

  57. Parkos CA, Colgan SP, Delp C, Arnaout MA, Madara JL. Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J Cell Biol. 1992;117:757–64.

    Article  PubMed  CAS  Google Scholar 

  58. Nash S, Stafford J, Madara JL. Effects of polymorphonuclear leukocyte transmigration on the barrier function of cultured intestinal epithelial monolayers. J Clin Invest. 1987;80:1104–13.

    Article  PubMed  CAS  Google Scholar 

  59. Resnick MB, Colgan SP, Patapoff TW et al. Activated eosinophils evoke chloride secretion in model intestinal epithelia primarily via regulated release of 5′-AMP. J Immunol. 1993; 151: 5716–23.

    PubMed  CAS  Google Scholar 

  60. Fujiwara Y, Sasaki E, Ikeda Y et al. Interleukin-8 stimulates polymorphonuclear leukocyte migration across a cultured monolayer of rabbit gastric epithelial cells and impairs their barrier function. Gastroenterology. 1996; 110: A110(abstract).

    Google Scholar 

  61. Cahill RJ, Xia H, Kilgallen C, Beattie S, Hamilton H, O’Morain C. Effect of eradication of Helicobacter pylori infection on gastric epithelial cell proliferation. Dig Dis Sci. 1995;40: 1627–31.

    Article  PubMed  CAS  Google Scholar 

  62. Fan XG, Kelleher D, Fan XJ, Xia HX, Keeling PWN. Helicobacter pylori increases proliferation of gastric epithelial cells. Gut. 1996;38:19–22.

    Article  PubMed  CAS  Google Scholar 

  63. Wagner S, Beil W, Nietart M et al. Antiproliferative effect of Helicobacter pylori on human gastric epithelial cells in vitro. Gastroenterology. 1996;110:A1040(abstract).

    Google Scholar 

  64. Dekigai H, Murakami M, Saita H et al. Monochloramine and ammonia produced by Helicobacter pylori infection inhibit restitution of gastric epithelial cell. Gastroenterology. 1996; 110: A92(abstract).

    Article  Google Scholar 

  65. Naito Y, Yoshikawa T, Yagi N et al. Cell growth inhibition and apoptosis induced by monochloramine in a gastric mucosal cell line. Gastroenterology. 1996; 110:A205(abstract).

    Google Scholar 

  66. Watson AJM. Necrosis and apoptosis in the gastrointestinal tract. Gut. 1995;37:165–7.

    Article  PubMed  CAS  Google Scholar 

  67. Moss SF, Calam J, Agarwal B, Wang S, Holt PG. Induction of gastric epithelial apoptosis by Helicobacter pylori. Gut. 1996;38:498–501.

    Article  PubMed  CAS  Google Scholar 

  68. Jones NL, Yeger H, Cutz E, Sherman PM. Helicobacter pylori induces apoptosis of gastric antral epithelial cells in vivo. Gastroenterology. 1996;110:A933.

    Google Scholar 

  69. Bravo LE, Mannick EE, Zhang X-J, Ruiz B, Correa P, Miller MJS. H. pylori infection is associated with inducible nitric oxide synthase expression, nitrotyrosine and DNA damage. Gastroenterology. 1995;108:A63(abstract).

    Google Scholar 

  70. Peek RM, Moss SF, Tham KT et al. Infection with H. pylori cagA+ strains dissociates gastric epithelial proliferation from apoptosis. Gastroenterology. 1996;110:A575(abstract).

    Google Scholar 

  71. Mori M, Suzuki M, Suzuki H, Akiba Y, Miura S, Ishii H. Extensive oxidative DNA damage is induced by ammonia-related oxidant, monochloramine, in cultured gastric epithelial cell. Gastroenterology. 1996;110: A201 (abstract).

    Google Scholar 

  72. Fukuda T, Arakawa T, Fujiwara Y et al. Nitric oxide induces apoptosis in gastric mucosal cells. Gastroenterology. 1996; 110: A110(abstract).

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1996 Kluwer Academic Publishers and Axcan Pharma

About this chapter

Cite this chapter

Crowe, S.E., Fan, X., Behar, S., Ye, G. (1996). Effects of infection with Helicobacter pylori on gastric epithelium. In: Hunt, R.H., Tytgat, G.N.J. (eds) Helicobacter pylori. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-1792-7_14

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-1792-7_14

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-7299-1

  • Online ISBN: 978-94-009-1792-7

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics