Helicobacter pylori-Induced IL-1β secretion in innate immune cells is regulated by the NLRP3 inflammasome and requires the cag pathogenicity Island

Journal of Immunology

Volumn 193, Issue 7, 2014, Pages 3566-3576

  Semper, Raphaela P ^a   Mejías Luque, Raquel ^a   Groß, Christina ^b   Anderl, Florian ^a   Müller, Anne ^c   Vieth, Michael ^d   Busch, Dirk H ^a,e   Da Costa, Clarissa Prazeres ^a   Ruland, Jürgen ^b,e   Groß, Olaf ^b   Gerhard, Markus ^a,e  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d INSTITUTE OF PATHOLOGY   (Germany)

^e Partner Site Munich   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CAG PATHOGENICITY ISLAND; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; POTASSIUM ION; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VACUOLATING TOXIN; BACTERIAL PROTEIN; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; IL1B PROTEIN, HUMAN; IL1B PROTEIN, MOUSE; NLRP3 PROTEIN, HUMAN; VACA PROTEIN, HELICOBACTER PYLORI;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BONE MARROW CELL; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IN VIVO STUDY; INNATE IMMUNITY; LYSOSOME; MOLECULAR STABILITY; MOUSE; NONHUMAN; POTASSIUM TRANSPORT; ANIMAL; CLINICAL TRIAL; GENETICS; GENOMIC ISLAND; HUMAN; IMMUNOLOGY; MALE; PATHOLOGY;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; FEMALE; GENOMIC ISLANDS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; MICE;

EID: 84907205655     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400362     Document Type: Article

References (43)

1. Cave, D. R. 1996. Transmission and epidemiology of Helicobacter pylori. Am. J. Med. 100: 12S-17S; discussion 17S-18S.
2. Blaser, M. J., G. I. Perez-Perez, H. Kleanthous, T. L. Cover, R. M. Peek, P. H. Chyou, G. N. Stemmermann, and A. Nomura. 1995. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res. 55: 2111-2115.
3. Shimoyama, T., S. Fukuda, M. Tanaka, T. Mikami, A. Munakata, and J. E. Crabtree. 1998. CagA seropositivity associated with development of gastric cancer in a Japanese population. J. Clin. Pathol. 51: 225-228.
4. Atherton, J. C., P. Cao, R. M. Peek, Jr., M. K. Tummuru, M. J. Blaser, and T. L. Cover. 1995. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori: association of specific vacA types wi th cytotoxin production and peptic ulceration. J. Biol. Chem. 270: 17771-17777.
5. Rudi, J., C. Kolb, M. Maiwald, I. Zuna, A. von Herbay, P. R. Galle, and W. Stremmel. 1997. Serum antibodi es against Helicobacter pylori proteins VacA and CagA are associated with increased risk for gastric adenocarcinoma. Dig. Dis. Sci. 42: 1652-1659.
6. Crabtree, J. E. 1996. Gastric mucosal inflammatory responses to Helicobacter pylori. Aliment. Pharmacol. Ther. 10(Suppl. 1): 29-37.
7. Viala, J., C. Chaput, I. G. Boneca, A. Cardona, S. E. Girardin, A. P. Moran, R. Athman, S. Mémet, M. R. Huerre, A. J. Coyle, et al. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5: 1166-1174.
8. Kim, D. J., J. H. Park, L. Franchi, S. Backert, and G. Nún? ez. 2013. The Cag pathogenicity island and interaction between TLR2/NOD2 and NLRP3 regulate IL-1b production in Helicobacter pylori infected dendritic cells. Eur. J. Immunol. 43: 2650-2658.
9. Mar tinon, F., K. Burns, and J. Tschopp. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proILb. Mol. Cell 10: 417-426.
10. Belhocine, K., and D. M. Monack. 2012. Francisella infection triggers activation of the AIM2 inflammasome in murine dendritic cells. Cell. Microbiol. 14: 71-80.
11. Prinz, C., N. Neumayer, S. Mahr, M. Classen, and W. Schepp. 1997. Functional impairment of rat enterochromaffin-like cells by interleukin 1b. Gastroenterology 112: 364-375.
12. 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, et al. 2000. Interleukin-1 polymorphisms associated wi th increased risk of gastric cancer. Nature 404: 398-402.
13. Haghshenas, M. R., S. V. Hosseini, M. Mahmoudi, M. Saberi-Firozi, S. Farjadian, and A. Ghaderi. 2009. IL-18 serum level and I L-18 promoter gene polymorphism in Iranian patients with gastrointestinal cancers. J. Gastroenterol. Hepatol. 24: 1119-1122.
14. Tu, S., G. Bhagat, G. Cui, S. Takaishi, E. A. Kurt-Jones, B. Rickman, K. S. Betz, M. Penz-Oesterreicher, O. Bjorkdahl, J. G. Fox, and T. C. Wang. 2008. Overexpression of interleukin-1b induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 14: 408-419.
15. Shigematsu, Y., T. Niwa, E. Rehnberg, T. Toyoda, S. Yoshida, A. Mori, M. Wakabayashi, Y. Iwakura, M. Ichinose, Y. J. Kim, and T. Ushijima. 2013. Interleukin-1b induced by Helicobacter pylori infection enhances mouse gastric carcinogenesis. Cancer Lett. 340: 141-147.
16. Kang, J. S., S. Y. Bae, H. R. Kim, Y. S. Kim, D. J. Kim, B. J. Cho, H. K. Yang, Y. I. Hwang, K. J. Kim, H. S. Park, et al. 2009. Interleukin-18 increases metastasis and immune escape of stomach cancer via the downregulation of CD70 and maintenance of CD44. Carcinogenesis 30: 1987-1996.
17. El-Omar E. M., 2001, The importance of interleukin 1b in Helicobacter pylori associated disease, Gut, 48, 743-747.
18. Hitzler, I., A. Sayi, E. Kohler, D. B. Engler, K. N. Koch, W. D. Hardt, and A. M€ uller. 2012. Caspase-1 has both proinflammatory and regulatory properties in Helicobacter infections, which are differentially mediated by its substrates IL-1b and IL-18. J. Immunol. 188: 3594-3602.
19. Baltrus, D. A., M. R. Amieva, A. Covacci, T. M. Lowe, D. S. Merrell, K. M. Ottemann, M. Stein, N. R. Salama, and K. Guillemin. 2009. The complete genome sequence of Helicobacter pylori strain G27. J. Bacteriol. 191: 447-448.
20. 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 infecti on: introducing the Sydney strain. Gastroenterology 112: 1386-1397.
21. Oertli, M., M. Noben, D. B. Engler, R. P. Semper, S. Reuter, J. Maxeiner, M. Gerhard, C. Taube, and A. Müller. 2013. Helicobacter pylori g-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc. Natl. Acad. Sci. USA 110: 3047-3052.
22. Arnold, I. C., J. Y. Lee, M. R. Amieva, A. Roers, R. A. Flavell, T. Sparwasser, and A. M€ uller. 2011. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 140: 199-209.
23. S chmees, C., C. Prinz, T. Treptau, R. Rad, L. Hengst, P. Voland, S. Bauer, L. Brenner, R. M. Schmid, and M. Gerhard. 2007. Inhibition of T-cell proliferation by Helicobacter pylori g-glutamyl transpeptidase. Gastroenterology 132: 1820-1833.
24. Martinon, F., V. Pé trilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
25. Mariathasan, S., K. Newton, D. M. Monack, D. Vucic, D. M. French, W. P. Lee, M. Roose-Girma, S. Erickson, and V. M. Dixit. 2004. Differential activation of the inflamm asome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213-218.
26. Kuida, K., J. A. Lippke, G. Ku, M. W. Harding, D. J. Livingston, M. S. Su, and R. A. Flavell. 1995. Altered cytokine export and apoptosis in mice deficient in interleukin-1b converting enzyme. Science 267: 2000-2003.
27. Dixon, M. F., R. M. Genta, J. H. Yardley, and P. Correa. 1996. 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.
28. Pacheco, R., T. Gallart, C. Lluis, and R. Franco. 2007. Role of glutamate on Tcell mediated immunity. J. Neuroimmunol. 185: 9-19.
29. Fallarino, F., C. Volpi, F. Fazio, S. Notartomaso, C. Vacca, C. Busceti, S. Bicciato, G. Battaglia, V. Bruno, P. Puccetti, et al. 2010. Metabotropic glutamate receptor-4 modulates adaptive immunity and restrains neuroinflammation. Nat. Med. 16: 897-902.
30. van Doorn, N. E., F. Namavar, M. Sparrius, J. Stoof, E. P. van Rees, L. J. van Doorn, and C. M. Vandenbroucke-Grauls. 1999. Helicobacter pylori-associated gastritis in mice is host and strain specific. Infect. Immun. 67: 3040-3046.
31. Day, A. S., N. L. Jones, Z. Policova, H. A. Jennings, E. K. Yau, P. Shannon, A. W. Neumann, and P. M. Sherman. 2001. Characterization of virulence factors of mouse-ad apted Helicobacter pylori strain SS1 and effects on gastric hydrophobicity. Dig. Dis. Sci. 46: 1943-1951.
32. Moll, G., E. Papini, R. Colonna, D. Burroni, J. Telford, R. Rappuoli, and C. Montecucco . 1995. Lipid interaction of the 37-kDa and 58-kDa fragments of the Helicobacter pylori cytotoxin. Eur. J. Biochem. 234: 947-952.
33. Kimura, M., S. Goto, A. Wada, K. Yahiro, T. Niidome, T. Hatakeyama, H. Aoyagi, T. Hirayama, and T. Kondo. 1999. Vacuolating cytotoxin purified from Helicobacter pylori causes mitochondrial damage in human gastric cells. Microb. Pathog. 26: 45-52.
34. Kim ura, M., S. Goto, Y. Ihara, A. Wada, K. Yahiro, T. Niidome, H. Aoyagi, T. Hirayama, and T. Kondo. 2001. Impairment of glutathione metabolism in human gastric epithelial cells treated with vacuolating cytotoxin from Helicobacter pylori. Microb. Pathog. 31: 29-36.
35. Kim, J. M., J. S. Kim, J. Y. Lee, Y. J. Kim, H. J. Youn, I. Y. Kim, Y. J. Chee, Y. K. Oh, N. Kim, H. C. Jung, and I. S. Song . 2007. Vacuolating cytotoxin in Helicobacter pylori water-soluble proteins upregulates chemokine expression in human eosinophils via Ca2+ influx, mitochondrial reactive oxygen intermediates, and NF-kB activation. Infect. Immun. 75: 3373-3 381.
36. Markiewicz, E., K. Tilgner, N. Barker, M. van de Wetering, H. Clevers, M. Dorobek, I. Hausmanowa-Petrusewicz, F. C. Ramaekers, J. L. Broers, W. M. Blankesteijn, et al. 2006. Th e inner nuclear membrane protein emerin regulates b-catenin activity by restricting its accumulation in the nucleus. EMBO J. 25: 3275-3285.
37. Shimada, K., T. R. Crother, J. Karlin, J. Dagvadorj, N. Chiba, S. Chen, V. K. Ramanujan, A. J. Wolf, L. Vergnes, D. M. Ojcius, et al. 2012. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36: 401-414.
38. Broz P.,D.M Monack, 2011. Molecular mechanisms of inflammasome activation during microbial infections. Immunol. Rev., 243, 174-190.
39. Gomes, M. T., P. C. Campos, F. S. Oliveira, P. P. Corsetti, K. R. Bortoluci, L. D. Cunha, D. S. Zamboni, and S. C. Oliveira. 2013. Critical role of ASC inflammasomes and bacterial type IV secretion system in caspase-1 activation and host innate resistance to Brucella abortus infec tion. J. Immunol. 190: 3629-3638.
40. Shimada, T., B. G. Park, A. J. Wolf, C. Brikos, H. S. Goodridge, C. A. Becker, C. N. Reyes, E. A. Miao, A. Aderem, F. Gö tz, et al. 2010. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1b secretion. Cell Host Microbe 7: 38-49.
41. Schepp, W., K. Dehne, H. Herrmuth, K. Pfeffer, and C. Prinz. 1998. Identification and functional importance of IL-1 receptors on rat parietal cells. Am. J. Physiol. 275: G1094-G1105.
42. Neu, B., A. J. Puschmann , A. Mayerhofer, P. Hutzler, J. Grossmann, F. Lippl, W. Schepp, and C. Prinz. 2003. TNF-A induces apoptosis of parietal cells. Biochem. Pharmacol. 65: 1755-1760.
43. 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, et al. 2003. Increased risk of noncardia gastric cancer associated with proinflammato ry cytokine gene polymorphisms. Gastroenterology 124: 1193-1201.