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

Infection and Immunity

Volumn 72, Issue 11, 2004, Pages 6446-6454

  Mandell, Leisa ^a   Moran, Anthony P ^c   Cocchiarella, Andrew ^a   Houghton, JeanMarie ^a   Taylor, Nancy ^b   Fox, James G ^b   Wang, Timothy C ^a   Kurt Jones, Evelyn A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CAGA PROTEIN; INTERLEUKIN 8; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; HELICOBACTER FELIS; HELICOBACTER HEPATICUS; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; KNOCKOUT MOUSE; MACROPHAGE; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL LINE; CYTOKINES; HELICOBACTER FELIS; HELICOBACTER HEPATICUS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, NATURAL; LIPOPOLYSACCHARIDES; MACROPHAGES, PERITONEAL; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 5044240576     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.11.6446-6454.2004     Document Type: Article

References (82)

1. Akira, S., K. Takeda, and T. Kaisho. 2001. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2:675-680.
2. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413:732-738.
3. Aliprantis. A. O., R. B. Yang, M. R. Mark, S. Suggett, B. Devaux, J. D. Radolf, G. R. Klimpel, P. Godowski, and A. Zychlinsky. 1999. Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor 2. Science 285:736-739.
4. Backhed, F., B. Rokbi, E. Torstensson, Y. Zhao, C. Nilsson, D. Seguin, S. Normark, A. M. Buchan, and A. Richter-Dahlfors. 2003. Gastric mucosal recognition of Helicobacter pylori is independent of Toll-like receptor 4. J. Infect. Dis. 187:829-836.
5. Bliss, C. M., Jr., D. T. Golenbock, S. Keates, J. K. Linevsky, and C. P. Kelly. 1998. Helicobacter pylori lipopolysaccharide binds to CD14 and stimulates release of interleukin-8, epithelial neutrophil-activating peptide 78, and monocyte chemotactic protein 1 by human monocytes. Infect. Immun. 66:5357-5363.
6. Bowie, A., and L. A. O'Neill. 2000. The interleukin-1 receptor/Toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J. Leukoc. Biol 67:508-514.
7. Brightbill, H. D., D. H. Library, S. R. Krutzik, R. B. Yang, J. T. Belisle, J. R. Bleharski, M. Maitland, M. V. Norgard, S. E. Plevy, S. T. Smale, P. J. Brennan, B. R. Bloom, P. J. Godowski, and R. L. Modlin. 1999. Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285:732-736.
8. Cario, E., G. Gerken, and D. K. Podolsky. 2002. "For whom the bell tolls!"-innate defense mechanisms and survival strategies of the intestinal epithelium against lumenal pathogens. Z. Gastroenterol. 40:983-990.
9. Chaudhary, P. M., C. Ferguson, V. Nguyen, O. Nguyen, H. F. Massa, M. Eby, A. Jasmin, B. J. Trask, L. Hood, and P. S. Nelson. 1998. Cloning and characterization of two Toll/interleukin-1 receptor-like genes, TIL3 and TIL4: evidence for a multi-gene receptor family in humans. Blood 91:4020-4027.
10. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor 4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689-10692.
11. Compton, T., E. A. Kurt-Jones, K. W. Boehme, J. Belko, E. Latz, D. T. Golenbock, and R. W. Finberg. 2003. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77:4588-4596.
12. Correa, P. 1992. Human gastric carcinogenesis: a multistep and multifactorial process-first American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res. 52:6735-6740.
13. Crabtree, J. E., R. L. Ferrero, and J. G. Kusters. 2002. The mouse colonizing Helicobacter pylori strain SS1 may lack a functional cag pathogenicity island. Helicobacter 7:139-140. (Author reply, 7:140-141.)
14. El-Omar, E. M., M. Carrington, W. H. Chow, K. E. McColl, J. H. Bream, H. A. Young, J. Herrera, J. Lissowska, C. C. Yuan, N. Rothman, G. Lanyon, M. Martin, J. F. Fraumeni, Jr., and C. S. Rahkin. 2000. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 404:398-402.
15. El-Omar, E. M., C. S. Rabkin, M. D. Gammon, T. L. Vaughan, H. A. Risch, J. B. Schoenberg, J. L. Stanford, S. T. Mayne, J. Goedert, W. J. Blot, J. F. Fraumeni, Jr., and W. H. Chow. 2003. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 124:1193-1201.
16. Erdman, S., J. G. Fox, C. A. Dangler, D. Feldman, and B. H. Horwitz. 2001. Typhlocolitis in NF-κB-deficient mice. J. Immunol. 166:1443-1447.
17. + regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am. J. Pathol. 162:691-702.
18. + regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res. 63:6042-6050.
19. Ernst, P. B., and B. D. Gold. 2000. The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol. 54:615-640.
20. Fischer, W., J. Puls, R. Buhrdorf, B. Gebert, S. Odenbreit, and R. Haas. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
21. Graham, D. Y., and Y. Yamaoka. 2000. Disease-specific Helicobacter pylori virulence factors: the unfulfilled promise. Helicobacter 5(Suppl. 1):S3-S9. (Discussion, 5:S27-S31.)
22. Hansson, L. E., O. Nyren, A. W. Hsing, R. Bergstrom. S. Josefsson, W. H. Chow, J. F. Fraumeni, Jr., and H. O. Adami. 1996. The risk of stomach cancer in patients with gastric or duodenal ulcer disease. N. Engl. J. Med. 335:242-249.
23. Heine, H., C. J. Kirschning, E. Lien, B. G. Monks, M. Rothe, and D. T. Golenbock. 1999. Cutting edge: cells that carry a null allele for Toll-like receptor 2 are capable of responding to endotoxin. J. Immunol. 162:6971-6975.
24. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740-745.
25. Higashi, H., R. Tsutsumi, S. Muto, T. Sugiyama, T. Azuma, M. Asaka, and M. Hatakeyama. 2002. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295:683-686.
26. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165:618-622.
27. Houghton, J., J. G. Fox, and T. C. Wang. 2002. Gastric cancer: laboratory bench to clinic. J. Gastroenterol. Hepatol. 17:495-502.
28. Houghton, J. M., L. M. Bloch, M. Goldstein, S. Von Hagen, and R. M. Korah. 2000. In vivo disruption of the fas pathway abrogates gastric growth alterations secondary to Helicobacter infection. J. Infect. Dis. 182:856-864.
29. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. 1994. Schistosomes, liver flukes and Helicobacter pylori. IARC Monogr. Eval. Carcinog. Risks Hum. 61:1-241.
30. Imler, J. L., and J. A. Hoffmann. 2001. Toll receptors in innate immunity. Trends Cell Biol. 11:304-311.
31. Janvier, B., B. Grignon, C. Audibert, L. Pezennec, and J. L. Fauchere. 1999. Phenotypic changes of Helicobacter pylori components during an experimental infection in mice. FEMS Immunol. Med. Microbiol. 24:27-33.
32. Kaisho, T., and S. Akira. 2000. Critical roles of Toll-like receptors in host defense. Crit. Rev. Immunol. 20:393-405.
33. Kaisho, T., and S. Akira. 2002. Toll-like receptors as adjuvant receptors. Biochim. Biophys. Acta 1589:1-13.
34. Kawahara, T., Y. Kuwano, S. Teshima-Kondo, T. Kawai, T. Nikawa, K. Kishi, and K. Rokutan. 2001. Toll-like receptor 4 regulates gastric pit cell responses to Helicobacter pylori infection. J. Med. Investig. 48:190-197.
35. Kawahara, T., Y. Kuwano, S. Teshima-Kondo, T. Sugiyama, T. Kawai, T. Nikawa, K. Kishi, and K. Rokutan. 2001. Helicobacter pylori lipopolysaccharide from type I, but not type II, strains stimulates apoptosis of cultured gastric mucosal cells. J. Med. Investig. 48:167-174.
36. Kawahara, T., S. Teshima, A. Oka, T. Sugiyama, K. Kishi, and K. Rokutan. 2001. Type I Helicobacter pylori lipopolysaccharide stimulates Toll-like receptor 4 and activates mitogen oxidase 1 in gastric pit cells. Infect. Immun. 69:4382-4389.
37. Kopp, E. B., and R. Medzhitov. 1999. The Toll-receptor family and control of innate immunity. Curr. Opin. Immunol. 11:13-18.
38. Kurt-Jones, E. A., L. Mandell, C. Whitney, A. Padgett, K. Gosselin, P. E. Newburger, and R. W. Finberg. 2002. Role of Toll-like receptor 2 (TLR2) in neutrophil activation: GM-CSF enhances TLR2 expression and TLR2-mediated interleukin 8 responses in neutrophils. Blood 100:1860-1868.
39. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401.
40. Lee, A., J. G. Fox, G. Otto, and J. Murphy. 1990. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology 99:1315-1323.
41. Lee, A., J. O'Rourke, M. C. De Ungria, B. Robertson, G. Daskalopoulos, and M. F. Dixon. 1997. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397.
42. Levi, S., K. Beardshall, G. Haddad, R. Playford, P. Ghosh, and J. Calam. 1989. Campylobacter pylori and duodenal ulcers: the gastrin link. Lancet i:1167-1168.
43. Lien, E., and R. R. Ingalls. 2002. Toll-like receptors. Crit. Care Med. 30:S1-S11.
44. Lien, E., T. J. Sellati, A. Yoshimura, T. H. Flo, G. Rawadi, R. W. Finberg, J. D. Carroll, T. Espevik, R. R. Ingalls, J. D. Radolf, and D. T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J. Biol. Chem. 274:33419-33425.
45. Maeda, S., M. Akanuma, Y. Mitsuno, Y. Hirata, K. Ogura, H. Yoshida, Y. Shiratori, and M. Omata. 2001. Distinct mechanism of Helicobacter pylori-mediated NF-κB activation between gastric cancer cells and monocytic cells. J. Biol. Chem. 276:44856-44864.
46. Mahler, M., C. Janke, S. Wagner, and H. J. Hedrich. 2002. Differential susceptibility of inbred mouse strains to Helicobacter pylori infection. Scand. J. Gastroenterol. 37:267-278.
47. Mai, U. E., G. I. Perez-Perez, L. M. Wahl, S. M. Wahl, M. J. Blaser, and P. D. Smith. 1991. Soluble surface proteins from Helicobacter pylori activate monocytes/macrophages by lipopolysaccharide-independent mechanism. J. Clin. Investig. 87:894-900.
48. Martin, M., J. Katz, S. N. Vogel, and S. M. Michalek. 2001. Differential induction of endotoxin tolerance by lipopolysaccharides derived from Porphyromonas gingivalis and Escherichia coli. J. Immunol. 167:5278-5285.
49. Means, T. K., E. Lien, A. Yoshimura, S. Wang, D. T. Golenbock, and M. J. Fenton. 1999. The CD14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J. Immunol. 163:6748-6755.
50. Medzhitov, R., and C. Janeway, Jr. 2000. Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173:89-97.
51. Medzhitov, R., and C. A. Janeway, Jr. 1998. An ancient system of host defense. Curr. Opin. Immunol. 10:12-15.
52. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394-397.
53. Moran, A. 1998. The products of Helicobacter pylori that induce inflammation. Eur. J. Gastroenterol. Hepatol. 10(Suppl. 1):S3-S8.
54. Moran, A. P., I. M. Helander. and T. U. Kosunen. 1992. Compositional analysis of Helicobacter pylori rough-form lipopolysaccharides. J. Bacteriol. 174:1370-1377.
55. Moran, A. P., Y. A. Knirel, S. N. Senchenkova, G. Widmalm, S. O. Hynes, and P. E. Jansson. 2002. Phenotypic variation in molecular mimicry between Helicobacter pylori lipopolysaccharides and human gastric epithelial cell surface glycoforms. Acid-induced phase variation in Lewis(x) and Lewis(y) expression by H. pylori lipopolysaccharides. J. Biol. Chem. 277:5785-5795.
56. Moran, A. P., B. Lindner, and E. J. Walsh. 1997. Structural characterization of the lipid A component of Helicobacter pylori rough- and smooth-form lipopolysaccharides. J. Bacteriol. 179:6453-6463.
57. Mulholland, G., J. E. Ardill, D. Fillmore, R. S. Chittajallu, G. M. Fullarton, and K. E. McColl. 1993. Helicobacter pylori related hypergastrinaemia is the result of a selective increase in gastrin 17. Gut 34:757-761.
58. Muotiala, A., I. M. Helander, L. Pyhala, T. U. Kosunen, and A. P. Moran. 1992. Low biological activity of Helicobacter pylori lipopolysaccharide. Infect. Immun. 60:1714-1716.
59. O'Neill, L. 2000. The Toll/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem. Soc. Trans. 28:557-563.
60. Ortega-Cava, C. F., S. Ishihara, M. A. Rumi, K. Kawashima, N. Ishimura, H. Kazumori, J. Udagawa, Y. Kadowaki, and Y. Kinoshita. 2003. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J. Immunol. 170:3977-3985.
61. Panthel, K., G. Faller, and R. Haas. 2003. 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.
62. Parsonnet, J., R. A. Harris, H. M. Hack, and D. K. Owens. 1996. Modelling cost-effectiveness of Helicobacter pylori screening to prevent gastric cancer: a mandate for clinical trials. Lancet 348:150-154.
63. Pece, S., D. Fumarola, G. Giuliani, E. Jirillo, and A. P. Moran. 1995. Activity in the Limulus amebocyte lysate assay and induction of tumour necrosis factor by diverse Helicobacter pylori lipopolysaccharide preparations. J. Endotoxin Res. 2:455-462.
64. Perez-Perez, G. I., V. L. Shepherd, J. D. Morrow, and M. J. Blaser. 1995. Activation of human THP-1 cells and rat bone marrow-derived macrophages by Helicobacter pylori lipopolysaccharide. Infect. Immun. 63:1183-1187.
65. Podolsky, D. K. 1999. Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am. J. Physiol. 277:G495-G499.
66. Raetz, C. R., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
67. Rock, F. L., G. Hardiman, J. C. Timans, R. A. Kastelein, and J. F. Bazan. 1998. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. USA 95:588-593.
68. Sakagami, T., J. Vella, M. F. Dixon, J. O'Rourke, F. Radcliff, P. Sutton, T. Shimoyama, K. Beagley, and A. Lee. 1997. The endotoxin of Helicobacter pylori is a modulator of host-dependent gastritis. Infect. Immun. 65:3310-3316.
69. Salama, N., K. Guillemin, T. K. McDaniel, G. Sherlock, L. Tompkins, and S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97:14668-14673.
70. Sandor, F., E. Latz, F. Re, L. Mandell, G. Repik, D. T. Golenbock, T. Espevik, E. A. Kurt-Jones, and R. W. Finberg. 2003. Importance of extra- and intracellular domains of TLR1 and TLR2 in NFκB signaling. J. Cell Biol. 162:1099-1110.
71. Scherer, C., K. D. Muller, P. M. Rath, and R. A. Ansorg. 2003. Influence of culture conditions on the fatty acid profiles of laboratory-adapted and freshly isolated strains of Helicobacter pylori. J. Clin. Microbiol. 41:1114-1117.
72. Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, and C. J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem. 274:17406-17409.
73. Shimoyama, T., S. M. Everett, M. F. Dixon, A. T. Axon, and J. E. Crabtree. 1998. Chemokine mRNA expression in gastric mucosa is associated with Helicobacter pylori cagA positivity and severity of gastritis. J. Clin. Pathol. 51:765-770.
74. Smith, M. F., Jr., A. Mitchell, G. Li, S. Ding, A. M. Fitzmaurice, K. Ryan, S. Crowe, and J. B. Goldberg. 2003. Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-κB activation and chemokine expression by epithelial cells. J. Biol. Chem. 278:32552-32560.
75. Sutton, P., J. Wilson, and A. Lee. 2000. Further development of the Helicobacter pylori mouse vaccination model. Vaccine 18:2677-2685.
76. Swingler, S., A. Mann, J. Jacque, B. Brichacek, V. G. Sasseville, K. Williams, A. A. Lackner, E. N. Janoff, R. Wang, D. Fisher, and M. Stevenson. 1999. HIV-1 Nef mediates lymphocyte chemotaxis and activation by infected macrophages. Nat. Med. 5:997-1003.
77. Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, H. Takada, T. Ogawa, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 11:443-451.
78. Underbill, D. M., A. Ozinsky, A. M. Hajjar, A. Stevens, C. B. Wilson, M. Bassetti, and A. Aderem. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401:811-815.
79. Wang, T. C., C. A. Dangler, D. Chen, J. R. Goldenring, T. Koh, R. Raychowdhury, R. J. Coffey, S. Ito, A. Varro, G. J. Dockray, and J. G. Fox. 2000. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology 118:36-47.
80. Wang, T. C., J. R. Goldenring, C. Dangler, S. Ito, A. Mueller, W. K. Jeon, T. J. Koh, and J. G. Fox. 1998. Mice lacking secretory phospholipase A2 show altered apoptosis and differentiation with Helicobacter felis infection. Gastroenterology 114:675-689.
81. Yamaoka, Y., T. Kodama, M. Kita, J. Imanishi, K. Kashima, and D. Y. Graham. 1999. Relation between clinical presentation, Helicobacter pylori density, interleukin 1β and 8 production, and cagA status. Gut 45:804-811.
82. Yoshimura, A., E. Lien, R. R. Ingalls, E. Tuomanen, R. Dziarski, and D. Golenbock. 1999. Cutting edge: recognition of gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163:1-5.