Helicobacter pylori phase variation, immune modulation and gastric autoimmunity

Nature Reviews Microbiology

Volumn 4, Issue 2, 2006, Pages 151-159

  Bergman, Mathijs ^a   Del Prete, Gianfranco ^b   van Kooyk, Yvette ^c   Appelmelk, Ben ^c  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF FLORENCE   (Italy)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CARBOHYDRATE; LECTIN;

ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; BACTERIAL COLONIZATION; BLOOD GROUP LEWIS SYSTEM; CELL ACTIVITY; GASTROINTESTINAL TRACT; GENETIC SUSCEPTIBILITY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; IMMUNE RESPONSE; IMMUNOMODULATION; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH2 CELL;

AMINO ACID SEQUENCE; AUTOIMMUNITY; GENETIC PREDISPOSITION TO DISEASE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MOLECULAR SEQUENCE DATA; STOMACH DISEASES;

BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI;

EID: 31544456135     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1344     Document Type: Article

References (88)

1. Ernst, P. B. & Gold, B. D. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol. 54, 615-640 (2000).
2. Blaser, M. J. Hypothesis: The changing relationships of Helicobacter pylori and humans: Implications for health and disease. J. Infect. Dis. 179, 1523-1530 (1999).
3. Monack, D. M., Mueller, A. & Falkow, S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nature Rev. Microbiol. 2, 747-765 (2004).
4. Blaser, M. J. & Atherton, J. C. Helicobacter pylori persistence: Biology and disease. J. Clin. Invest. 113, 321-333 (2004).
5. Noach, L. A. et al. Mucosal tumor necrosis factor-α, interleukin-1β, and interleukin-8 production in patients with Helicobacter pylori infection. Scand. J. Gastroenterol. 29, 425-429 (1994).
6. Lindholm, C., Quiding-Jarbrink, M., Lonroth, H., Hamlet, A. & Svennerholm, A. M. Local cytokine response in Helicobacter pylori-infected subjects. Infect. Immun. 66, 5964-5971 (1998).
7. Lindholm, C., Quiding-Jarbrink, M., Lonroth, H. & Svennerholm, A. M. Induction of chemokine and cytokine responses by Helicobacter pylori in human stomach explants. Scand. J. Gastroenterol. 36, 1022-1029 (2001).
8. Rossi, G. et al. Immunohistochemical study of lymphocyte populations infiltrating the gastric mucosa of beagle dogs experimentally infected with Helicobacter pylori. Infect. Immun. 68, 4769-4772 (2000).
9. H1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice. J. Immunol. 156, 4729-4738 (1996).
10. H2 cells reduce bacterial load. Gastroenterology 113, 1848-1857 (1997).
11. Lepper, P. M., Triantafilou, M., Schumann, C., Schneider, E. M. & Triantafilou, K. Lipopolysaccharides from Helicobacter pylori can act as antagonists for Toll-like receptor 4. Cell. Microbiol. 7, 519-528 (2005).
12. Del Giudice, G., Covacci, A., Telford, J. L., Montecucco, C. & Rappuoli, R. The design of vaccines against Helicobacter pylori and their development. Annu. Rev. Immunol. 19, 523-563 (2001).
13. Muotiala, A., Helander, I. M., Pyhala, L., Kosunen, T. U. & Moran, A. P. Low biological activity of Helicobacter pylori lipopolysaccharide. Infect. Immun. 60, 1714-1716 (1992).
14. Moron, A., Lindner, B. & Walsh, E. Structural characterization of the lipid A component of Helicobacter pylori rough- and smooth-form lipopolysaccharides. J. Bacteriol. 179, 6453-6463 (1997).
15. Andersen-Nissen, E. et al. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl Acad. Sci. USA 102, 9247-9252 (2005).
16. Gobert, A. P. et al. Helicobacter pylori arginase inhibits nitric oxide production by eukaryotic cells: A strategy for bacterial survival. Proc. Natl Acad. Sci. USA 98, 13844-13849 (2001).
17. Allen, L.-A. H., Schlesinger, L. S. & Kang, B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med. 191, 115-128 (2000).
18. Ramarao, N., Gray-Owen, S. D., Backent, S. & Meyer, T. F. Helicobacter pylori inhibits phagocytosis by professional phagocytes involving type IV secretion components. Mol. Microbiol. 37, 1389-1404 (2000).
19. Gebert, B., Fischer, W., Weiss, E., Hoffmann, R. & Haas, R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301, 1099-1102 (2003).
20. Molinari, M. et al. Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA. J. Exp. Med. 187, 135-140 (1998).
21. Blaser, M. J. & Berg, D. E. Helicobacter pylori genetic diversity and risk of human disease. J. Clin. Invest. 107, 767-773 (2001).
22. Sakagami, T. et al. Atrophic gastric changes in both Helicobocter felis and Helicobacter pylori infected mice are host dependent and separate from antral gastritis. Gut 39, 639-648 (1996).
23. Mohammadi, M., Redline, R., Nedrud, J. & Czinn, S. Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. 64, 238-245 (1996).
24. Kamradt, A. E., Greiner, M., Ghiara, P. & Kaufmann, S. H. Helicobacter pylori infection in wildtype and cytokine-deficient C57BL/6 and BALB/c mouse mutants. Microbes Infect. 2, 593-597 (2000).
25. Panthel, K., Faller, G. & Haas, R. Colonization of C57BL/6J and BALB/c wild-type and knockout mice with Helicobacter pylori: Effect of vaccination and implications for innate and acquired immunity. Infect. Immun. 71, 794-800 (2003).
26. Dubois, A. et al. Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 116, 90-96 (1999).
27. Sutton, P., Kolesnikow, T., Danon, S., Wilson, J. & Lee, A. Dominant nonresponsiveness to Helicobacter pylori infection is associated with production of interleukin 10 but not γ interferon. Infect. Immun. 68, 4802-4804 (2000).
28. H1 mediated and exacerbated in IL-4, but not IFN-γ, gene-deficient mice. J. Immunol. 165, 1022-1029 (2000).
29. H1 cells. J. Immunol. 169, 6977-6984 (2002).
30. El-Omar, E. M. et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 404, 398-402 (2000).
31. Furuta, T. et al. Interleukin 1β polymorphisms increase risk of hypochlorhydria and atrophic gastritis and reduce risk of duodenal ulcer recurrence in Japan. Gastroenterology 123, 92-105 (2002).
32. El-Omar, E. M. et al. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124, 1193-1201 (2003).
33. H1 type of immune response is induced early during acute Helicobacter pylori infection in rhesus macaques. Gastroenterology 118, 307-315 (2000).
34. 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).
35. 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).
36. D'Elios, M. M. et al. Different cytokine profile and antigen-specificity repertoire in Helicobacter pylori-specific T cell clones from the antrum of chronic gastritis patients with or without peptic ulcer. Eur. J. Immunol. 27, 1751-1755 (1997).
37. Karnes, W. E. Jr et al. Positive serum antibody and negative tissue staining for Helicobacter pylori in subjects with atrophic body gastritis. Gastroenterologg 101, 167-174 (1991).
38. Ma, J. Y., Borch, K., Sjostrand, S. E., Janzon, L. & Mardh, S. Positive correlation between H,K-adenosine triphosphatase autoantibodies and Helicobacter pylori antibodies in patients with pernicious anemia. Scand. J. Gastroenterol. 29, 961-965 (1994).
39. Bergman, M. P. et al. 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. 200, 979-990 (2004).
40. Lerouge, I. & Vanderleyden, J. O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol. Rev. 26, 17-47 (2002).
41. Vimr, E. R., Kalivoda, K. A., Deszo, E. L. & Steenbergen, S. M. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68, 132-153 (2004).
42. Guerry P. et al. Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70, 787-793 (2002).
43. Simmons-Smit, I. M. et al. Typing of Helicobacter pylori with monoclonal antibodies against Lewis antigens in lipopolysaccharide. J. Clin. Microbiol. 34, 2196-2200 (1996).
44. Wang, G., Ge, Z., Rasko, D. A. & Taylor, D. E. Lewis antigens in Helicobacter pylori: Biosynthesis and phase variation. Mol. Microbiol. 36, 1187-1196 (2000).
45. y expression by H. pylori lipopolysaccharides. J. Biol. Chem. 277, 5785-5795 (2002).
46. Wirth, H. P., Yang, M., Peek, R. M. Jr, Tham, K. T. & Blaser, M. J. Helicobacter pylori Lewis expression is related to the host Lewis phenotype. Gastroenterology 113, 1091-1098 (1997).
47. Taylor, D. E., Rasko, D. A., Sherburne, R., Ho, C. & Jewell, L. D. Lack of correlation between Lewis antigen expression by Helicobacter pylori and gastric epithelial cells in infected patients. Gastroenterology 115, 1113-1122 (1998).
48. Mahdavi, J., Boren, T., Vandenbroucke-Grauls, C. & Appelmelk, B. J. Limited role of lipopolysaccharide Lewis antigens in adherence of Helicobacter pylori to the human gastric epithelium. Infect. Immun. 71, 2876-2880 (2003).
49. Heneghan, M. A., McCarthy, C. F. & Moran, A. P. Relationship of blood group determinants on Helicobacter pylori lipopolysaccharide with host Lewis phenotype and inflammatory response. Infect. Immun. 68, 937-941 (2000).
50. Rasko, D. A., Keelan, M., Wilson, T. J. & Taylor, D. E. Lewis antigen expression by Helicobacter pylori. J. Infect. Dis. 184, 315-321 (2001).
51. Engering, A. et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J. Immunol. 168, 2118-2126 (2002).
52. Geijtenbeek, T. B. et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100, 587-597 (2000).
53. Geijtenbeek, T. B. H. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003).
54. Rescigno, M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature Immunol. 2, 361-367 (2001).
55. Banchereau, J. & Steinman, R. M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
56. Appelmelk B. J. et al. Carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells. J. Immunol. 170, 1635-1639 (2003).
57. H2 and Leishmania: Paradox rather than paradigm. Immunol. Lett. 99, 17-23 (2005).
58. H2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunol. Rev. 201, 117-126 (2004).
59. Steere, A. C. Lyme disease. N. Engl. J. Med. 345, 115-125 (2001).
60. Gross, D. M. et al. Identification of LFA-1 as a candidate autoantigen in treatment-resistant Lyme arthritis. Science 281, 703-706 (1998).
61. Meyer, A. L. et al. Direct enumeration of Borrelia-reactive CD4 T cells ex vivo by using MHC class II tetramers. Proc. Natl Acad. Sci. USA 97, 11433-11438 (2000).
62. Bergman, M. P. et al. The story so far: Helicobacter pylori and gastric autoimmunity. Int. Rev. Immunol. 24, 63-91 (2005).
63. +-ATPase is a major autoantigen in chronic Helicobacter pylori gastritis with body mucosa atrophy. Gastroenterology 115, 340-347 (1998).
64. Faller, G. et al. Antigastric autoantibodies in Helicobacter pylori infection: Implications of histological and clinical parameters of gastritis. Gut 41, 619-623 (1997).
65. Stolte, M. et al. Active autoimmune gastritis without total atrophy of the glands. Z. Gastroenterol. 30, 729-735 (1992) (in German).
66. Stolte, M., Meier, E. & Meining, A. Cure of autoimmune gastritis by Helicobacter pylori eradication in a 21-year-old male. Z. Gastroenterol. 36, 641-643 (1998) (in German).
67. Tucci, A. et al. Reversal of fundic atrophy after eradication of Helicobacter pylori. Am. J. Gastroenterol. 93, 1425-1431 (1998).
68. +-adenosine triphosphatase in human gastric autoimmunity. J. Exp. Med. 198, 1147-1156 (2003).
69. H1-type cytotoxic T cells in autoimmune gastritis. Gastroenterology 120, 377-386 (2001).
70. Ungar, B., Mathews, J. D., Tait, B. D. & Cowling, D. C. HLA-DR patterns in pernicious anaemia. Br. Med. J. (Clin. Res. Ed.) 282, 768-770 (1981).
71. Alderuccio, F., Toh, B. H., Tan, S. S., Gleeson, P. A. & van Driel, I. R. An autoimmune disease with multiple molecular targets abrogated by the transgenic expression of a single autoantigen in the thymus. J. Exp. Med. 178, 419-426 (1993).
72. Suri-Payer, E. et al. Post-thymectomy autoimmune gastritis: Fine specificity and pathogenicity of anti-H/K ATPase-reactive T cells. Eur. J. Immunol. 29, 669-677 (1999).
73. Wirth, H. P. et al. Phenotypic diversity in Lewis expression of Helicobacter pylori isolates from the same host. J. Lab. Clin. Med. 133, 488-500 (1999).
74. Biondo, M., Nasa, Z., Marshall, A., Toh, B. H. & Alderuccio, F. Local transgenic expression of granulocyte macrophage-colony stimulating factor initiates autoimmunity. J. Immunol. 166, 2090-2099 (2001).
75. Nigou, J., Zelle-Rieser, C., Gilleron, M., Thurnher, M. & Puzo, G. Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: Evidence for a negative signal delivered through the mannose receptor. J. Immunol. 166, 7477-7485 (2001).
76. Quesniaux, V. J. et al. Toll-like receptor 2 (TLR2)-dependent-positive and TLR2-independent-negative regulation of proinflammatory cytokines by mycobacterial lipomannans. J. Immunol. 172, 4425-4434 (2004).
77. Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S. & Underhill, D. M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197, 1107-1117 (2003).
78. Brown, G. D. et al. Dectin-1 mediates the biological effects of β-glucans. J. Exp. Med. 197, 1119-1124 (2003).
79. Mandell, L. et al. Intact Gram-negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus bacteria activate innate immunity via Toll-like receptor 2 but not Toll-like receptor 4. Infect. Immun. 72, 6446-6454 (2004).
80. Krutzik, S. R. et al. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nature Med. 11, 653-660 (2005).
81. Cambi, A., Koopman, M. & Figdor, C. G. How C-type lectins detect pathogens. Cell. Microbiol. 7, 481-488 (2005).
82. Christen, U. & van Herrath, M. G. Initiation of autoimmuniy. Curr. Opin. Immunol. 16. 759-767 (2004).
83. + 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).
84. Engstrand, L. et al. Association of Campylobacter pylori with induced expression of class II transplantation antigens on gastric epithelial cells. Infect. Immun. 57, 827-832 (1989).
85. + T cell activation during Helicobacter pylori infection. J. Clin. Invest. 99, 1628-1636 (1997).
86. Garhart, C. A., Heinzel, F. P., Czinn, S. J. & Nedrud, J. G. Vaccine-induced reduction of Helicobacter pylori colonization in mice is interleukin-12 dependent but γ interferon and inducible nitric oxide synthase independent. Infect. Immun. 71, 910-921 (2003).
87. H1 immunization of mice against Helicobacter pylori infection with CpG oligodeoxynucleotides as adjuvants does not protect from infection but enhances gastritis. Infect. Immun. 72, 1029-1035 (2004).
88. Scheinecker, C., McHugh, R., Shevach, E. M. & Germain, R. N. Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J. Exp. Med. 196, 1079-1090 (2002).