TLR4-dependent NF-κB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages

Journal of Immunology

Volumn 177, Issue 11, 2006, Pages 7950-7958

  Pathak, Sushil Kumar ^a   Basu, Sanchita ^a   Bhattacharyya, Asima ^a   Pathak, Shresh ^a   Banerjee, Anirban ^a   Basu, Joyoti ^a   Kundu, Manikuntala ^a  

^a BOSE INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN; HISTONE H3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOTAGMIN; TOLL LIKE RECEPTOR 4;

ARTICLE; CELL INFILTRATION; CELL STRAIN HEK293; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; GASTRITIS; GENE; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HP0175 GENE; HUMAN; HUMAN CELL; LAMINA PROPRIA; MACROPHAGE; MONOCYTE; MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOMACH ULCER;

EID: 33751578866     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.11.7950     Document Type: Article

References (48)

1. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347: 1175-1186.
2. Crabtree, J. E., T. M. Shallcross, R. V. Heatly, and J. I. Wyatt. 1991. Mucosal tumor necrosis factor-α and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut 32: 1473-1477.
3. Noach, L. A., N. B. Bosma, J. Jansen, F. J. Hoek, S. J. van Deventer, and G. N. Tytgat. 1994. Mucosal tumor necrosis factor-α, interleukin-1β, and interleukin-8 production in patients with Helicobacter pylori infection. Scand. J. Gastroenterol. 29: 425-429.
4. Tilg, H., E. Trehu, M. B. Atkin, C. A. Dinarelo, and J. W. Mier. 1994. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83: 113-118.
5. Akira, S., T. Taga, and T. Kishimoto. 1993. Interleukin-6 in biology and medicine. J. Adv. Immunol. 54: 1-78.
6. Furukawa, K., T. Takahashi, F. Arai, K. Matsushima, and H. Asakura. 1989. Enhanced mucosal expression of interleukin-6 mRNA but not of interleukin-8 mRNA at the margin of gastric ulcer in Helicobacter pylori-positive gastritis. Gastroenterology 33: 625-633.
7. Yamaoka, Y., T. Kodama, M. Kita, J. Imanishi, K. Kashima, and D. Y. Graham. 2001. Relation between cytokines and Helicobacter pylori in gastric cancer. Helicobacter 6: 116-124.
8. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
9. Akira, S. 2003. Toll-like receptor signaling. J. Biol. Chem. 278: 38105-38108.
10. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1: 135-145.
11. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, S. A. Tadlen, C. Chen, S. Ghosh, and C. A. Janeway. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2: 253-258.
12. Muzio, M., J. Ni, P. Feng, and V. M. Dixit. 1997. IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278: 1612-1615.
13. Wesche, H., W. J. Henzel, W. Shillinglaw, S. Li, and Z. Cao. 1997. MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7: 837-847.
14. Cao, Z., W. J. Henzel, and X. Gao. 1996. IRAK: a kinase associated with the interleukin-1 receptor. Science 271: 1128-1131.
15. Bradley, J. R., and J. S. Pober. 2001. Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 20: 6482-6491.
16. Cao, Z., J. Xiong, M. Takeuchi, T. Kurama, and D. V. Goeddel. 1996. TRAF6 is a signal transducer for interleukin-1. Nature 383: 443-446.
17. Swantek, J. L., M. F. Tsen, M. H. Cobb, and J. A. Thomas. 2000. IL-1 receptor-associated kinase modulates host responsiveness to endotoxin. J. Immunol. 164: 4301-4306.
18. Zhang, G., and S. Ghosh. 2001. Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J. Clin. Invest. 107: 13-19.
19. Ishihara, S., M. A. Rumi, Y. Kadowaki, C. F. Ortega-Cava, T. Yuki, N. Yoshino, Y. Miyaoka, H. Kazumori, N. Ishimura, Y. Amano, and Y. Kinoshita. 2004. Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J. Immunol. 173: 1406-1416.
20. Gobert, A. P., J.-C. Bambou, C. Werts, V. Balloy, M. Chignard, A. P. Moran, and R. L. Ferrero. 2004. Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a Toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J. Biol. Chem. 279: 245-250.
21. Tanahashi, T., M. Kita, T. Kodama, Y. Yamaoka, N. Sawai, T. Ohno, S. Mitsufuji , Y. P. Wei, K. Kashima, and J. Imanishi, J. 2000. Cytokine expression and production by purified Helicobacter pylori urease in human gastric epithelial cells. Infect. Immun. 68: 664-667.
22. Kim, N., D. L. Weeks, J. M. Shin, D. R. Scott, M. K. Young, and G. Sachs. 2002. Proteins released by Helicobacter pylori in vitro. J. Bacteriol. 184: 6155-6162.
23. Atanassov, C., L. Pezennec, J. d'Alayer, G. Grollier, B. Picard, and J. L. Fauchere. 2002. Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J. Clin. Microbiol. 40: 547-552.
24. McAtee, C. P., M. Y. Lim, K. Fung, M. Velligan, K. Fry, T. P. Chow, and D. E. Berg. 1998. Characterization of a Helicobacter pylori vaccine candidate by proteome techniques. J. Chromatogr. B Biomed. Sci. Appl. 714: 325-333.
25. Basak, C., S. K. Pathak, A. Bhattacharyya, S. Pathak, J. Basu, and M. Kundu. 2005. The secreted peptidyl prolyl cis,trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J. Immunol. 174: 5672-5680.
26. Hyakushima, N., H. Mitsuzawa, C. Nishitani, H. Sano, M. Kuronuma, T. Himi, K. Miyake, and Y. Kuroki. 2004. Interaction of soluble form of recombinant extracellular TLR4 domain with MD-2 enables lipopolysaccharide binding and attenuates TLR4-mediated signaling. J. Immunol. 173: 6949-6954.
27. Bhattacharyya, A., S. Pathak, S. Datta, S. Chattopadhyay, J. Basu, and M. Kundu. 2002. Mitogen-activated protein kinases and nuclear factor-κB regulate Helicobacter pylori-mediated interleukin-8 release from macrophages. Biochem. J. 368: 121-129.
28. Heuermann, D., and R. Haas. 1998. A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol. Gen. Genet. 257: 519-528.
29. Taylor, S. J., R. J. Resnick, and D. Shalloway. 2001. Nonradioactive determination of Ras-GTP levels using activated ras interaction assay. Methods Enzymol. 333: 333-342.
30. Benard, V., B. P. Bohl, and G. M. Bokoch. 1999. Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274: 13198-13204.
31. Alessi, D. R., P. Cohen, A. Ashworth, S. Cowley, S. J. Leever, and C. J. Marshall. 1995. Assay and expression of mitogen-activated protein kinase, MAP kinase kinase, and Raf. Methods Enzymol. 255: 279-290.
32. Saccani, S., S. Pandano, and O. Natoli. 2002. p38-dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3: 69-75.
33. Harris, P. R., L. E. Smythies, P. D. Smith, and A. Dubois. 2000. Inflammatory cytokine mRNA expression during early and persistent Helicobacter pylori infection in nonhuman primates. J. Infect. Dis. 181: 783-786.
34. Deak, M., A. D. Clifton, L. M. Lucocq, and D. R. Alessi. 1998. Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J. 17: 4426-4441.
35. Vanden Berghe, W., S. Plaisance, E. Boone, K. De Bosscher, M. Lienhard Schmitz, W. Fiers, and G. Haegeman. 1998. p38 and extracellular signal-regulated kinase mitogen activated protein kinase pathways are required for nuclear factor-κB p65 transactivation mediated by tumor necrosis factor. J. Biol. Chem. 273: 3285-3290.
36. Akira, S., and T. Kishimoto. 1992. IL-6 and NF-IL6 in acute-phase response and viral infection. Immunol. Rev. 127: 25-50.
37. Shibuya, H., K. Yamaguchi, K. Shirakabe, A. Tonegawa, Y. Gotoh, N. Ueno, K. Irie, E. Nishida, and K. Matsumoto. 1996. TAB1: an activator of the TAK1 MAPKKK in TGF-β signal transduction. Science 272: 1179-1182.
38. Takaesu, G., S. Kishida, A. Hiyama, K. Yamaguchi, H. Shibuya, K. Trie, J. Ninomiya-Tsujc, and K. Matsumoto. 2000. TAB2, a novel adaptor protein, mediates activation of TAK1 MAPKKK by linking TAK1 to TRAF6 in the IL-1 signal transduction pathway. Mol. Cell 5: 649-658.
39. Janknecht, R. 2003. Regulation of the ER81 transcription factor and its coactivators by mitogen- and stress-activated protein kinase 1 (MSK1). Oncogene 22: 746-755.
40. Vermeulen, I., G. De Wilde, P. Van Damme, W. Vanden Berghe, and G. Haegeman. 2003. Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J. 22: 1313-1324.
41. Zhong, H., M. J. May, E. Jimi, and S. Ghosh. 2002. The phosphorylation status of nuclear NF-κB determines its association with CBP/p300 or HDAC-1. Mol. Cell 9: 625-636.
42. Thomson, S., A. L. Clayton, C. A. Hazzalin, S. Rose, M. J. Barratt, and L. C. Mahadevan. 1999. The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J. 18: 4779-4793.
43. Smith, M. F., 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.
44. Mandell, L., A. P. Moran, A. Cocchiarella, J.-M. Houghton, N. Taylor, J. G. Fox, T. C. Wang, and E. A. Kurt-Jones. 2004. 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.
45. Su, B., P. J. M. Seponis, S. Lebel, H. Huynh, and P. M. Sherman. 2003. Helicobacter pylori activates Toll-like receptor 4 expression in gastrointestinal epithelial cells. Infect. Immun. 71: 3496-3502.
46. Shaw, P. E. 2002. Peptidyl-prolyl isomerases: a new twist to transcription. EMBO Rep. 3: 521-526.
47. Kohler, R., J. Fanghanel, B. Konig, E. Luneberg, M. Frosch, J. U. Rahfeld, R. Hilgenfeld, G. Fischer, J. Hacker, and M. Steinert. 2003. Biochemical and functional analyses of the Mip protein: influence of the N-terminal half and of peptidylprolyl isomerase activity on the virulence of Legionella pneumophila. Infect. Immun. 71: 4389-4397.
48. Hermans, P. W., P. V. Adrian, C. Albert, S. Estevao, T. Hoogenboezem, I. H. Luijendijk, T. Kamphausen, and S. Hammerschmidt. 2006. The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J. Biol. Chem. 281: 968-976.