1887

Abstract

Previous reports have indicated that heat-shock protein 60 (-HSP60), as an immunodominant antigen, induces interleukin (IL)-8 production in human monocytes. The exact mechanism by which -HSP60 induces IL-8 production in monocytes has not been fully elucidated. In the present study, the downstream pathway by which -HSP60 induces IL-8 secretion in human monocytic cell lines was investigated. Intact , heat-killed and recombinant HSP60 (rHpHSP60) all induced the secretion of IL-8 and the activation of mitogen-activated protein kinase (MAPK), extracellular signal-regulated kinase (ERK) and p38, but not c-Jun N-terminal kinase (JNK), up to 24 h in NOMO1 cells. The specific inhibitors PD98059 and U0126 (for ERK1/2 signalling) and SB203580 (for p38 MAPK signalling) down-regulated IL-8 secretion from rHpHSP60-treated NOMO1 cells. An anti-Toll-like receptor (TLR)2 antibody or TLR2 small interfering RNA (siRNA) partially inhibited the secretion of IL-8, and anti-TLR2 antibody also suppressed activation of ERK and p38 MAPK in rHpHSP60-treated NOMO1 cells. These reactions were associated with nuclear factor-B (NF-B)-mediated transcriptional activation, since U0126, SB203580 and the anti-TLR2 antibody decreased NF-B activation. Taken together, the results suggest that ERK and p38 MAPK signalling linked to the TLR2 recognition receptor in human monocytes may be an important pathway in -HSP60-induced IL-8 secretion.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.46882-0
2007-02-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jmm/56/2/154.html?itemId=/content/journal/jmm/10.1099/jmm.0.46882-0&mimeType=html&fmt=ahah

References

  1. Aihara, M., Tsuchimoto, D., Takizawa, H., Azuma, A., Wakebe, H., Ohmoto, Y., Imagawa, K., Kikuchi, M., Mukaida, N. & Matsushima, K. ( 1997; ). Mechanisms involved in Helicobacter pylori-induced interleukin-8 production by a gastric cancer cell line, MKN45. Infect Immun 65, 3218–3224.
    [Google Scholar]
  2. Asea, A., Rehli, M., Kabingu, E., Boch, J. A., Bare, O., Auron, P. E., Stevenson, M. A. & Calderwood, S. K. ( 2002; ). Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277, 15028–15034.[CrossRef]
    [Google Scholar]
  3. Basak, C., Pathak, S. K., Bhattacharyya, A., Mandal, D., Pathak, S. & Kundu, M. ( 2005; ). NF-kappaB- and C/EBPbeta-driven interleukin-1beta gene expression and PAK1-mediated caspase-1 activation play essential roles in interleukin-1beta release from Helicobacter pylori lipopolysaccharide-stimulated macrophages. J Biol Chem 280, 4279–4288.[CrossRef]
    [Google Scholar]
  4. Bhattacharyya, A., Pathak, S., Datta, S., Chattopadhyay, S., Basu, J. & Kundu, M. ( 2002; ). Mitogen-activated protein kinases and nuclear factor-kappaB regulate Helicobacter pylori-mediated interleukin-8 release from macrophages. Biochem J 368, 121–129.[CrossRef]
    [Google Scholar]
  5. Binder, R. J., Vatner, R. & Srivastava, P. ( 2004; ). The heat-shock protein receptors: some answers and more questions. Tissue Antigens 64, 442–451.[CrossRef]
    [Google Scholar]
  6. Bliss, C. M., Jr, Golenbock, D. T., Keates, S., Linevsky, J. K. & Kelly, C. P. ( 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.
    [Google Scholar]
  7. Brisslert, M., Enarsson, K., Lundin, S., Karlsson, A., Kusters, J. G., Svennerholm, A. M., Backert, S. & Quiding-Jarbrink, M. ( 2005; ). Helicobacter pylori induce neutrophil transendothelial migration: role of the bacterial HP-NAP. FEMS Microbiol Lett 249, 95–103.[CrossRef]
    [Google Scholar]
  8. Bulut, Y., Faure, E., Thomas, L., Karahashi, H., Michelsen, K. S., Equils, O., Morrison, S. G., Morrison, R. P. & Arditi, M. ( 2002; ). Chlamydial heat shock protein 60 activates macrophages and endothelial cells through Toll-like receptor 4 and MD2 in a MyD88-dependent pathway. J Immunol 168, 1435–1440.[CrossRef]
    [Google Scholar]
  9. Cabral, E. S., Gelderblom, H., Hornung, R. L., Munson, P. J., Martin, R. & Marques, A. R. ( 2006; ). Borrelia burgdorferi lipoprotein-mediated TLR2 stimulation causes the down-regulation of TLR5 in human monocytes. J Infect Dis 193, 849–859.[CrossRef]
    [Google Scholar]
  10. Chen, K., Iribarren, P., Hu, J., Chen, J., Gong, W., Cho, E. H., Lockett, S., Dunlop, N. M. & Wang, J. M. ( 2006; ). Activation of Toll-like receptor 2 on microglia promotes cell uptake of Alzheimer disease-associated amyloid beta peptide. J Biol Chem 281, 3651–3659.[CrossRef]
    [Google Scholar]
  11. Crabtree, J. E., Covacci, A., Farmery, S. M., Xiang, Z., Tompkins, D. S., Perry, S., Lindley, I. J. & Rappuoli, R. ( 1995; ). Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol 48, 41–45.[CrossRef]
    [Google Scholar]
  12. Cunningham, M. D., Seachord, C., Ratcliffe, K., Bainbridge, B., Aruffo, A. & Darveau, R. P. ( 1996; ). Helicobacter pylori and Porphyromonas gingivalis lipopolysaccharides are poorly transferred to recombinant soluble CD14. Infect Immun 64, 3601–3608.
    [Google Scholar]
  13. Cunningham, M. D., Shapiro, R. A., Seachord, C., Ratcliffe, K., Cassiano, L. & Darveau, R. P. ( 2000; ). CD14 employs hydrophilic regions to ‘capture’ lipopolysaccharides. J Immunol 164, 3255–3263.[CrossRef]
    [Google Scholar]
  14. Ellis, R. J. ( 1990; ). The molecular chaperone concept. Semin Cell Biol 1, 1–9.
    [Google Scholar]
  15. Evans, D. J., Jr, Evans, D. G., Takemura, T., Nakano, H., Lampert, H. C., Graham, D. Y., Granger, D. N. & Kvietys, P. R. ( 1995; ). Characterization of a Helicobacter pylori neutrophil-activating protein. Infect Immun 63, 2213–2220.
    [Google Scholar]
  16. Friedland, J. S., Shattock, R., Remick, D. G. & Griffin, G. E. ( 1993; ). Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytes. Clin Exp Immunol 91, 58–62.
    [Google Scholar]
  17. Galdiero, M., de l'Ero, G. C. & Marcatili, A. ( 1997; ). Cytokine and adhesion molecule expression in human monocytes and endothelial cells stimulated with bacterial heat shock proteins. Infect Immun 65, 699–707.
    [Google Scholar]
  18. Gewirtz, A. T., Yu, Y., Krishna, U. S., Israel, D. A., Lyons, S. L. & Peek, R. M., Jr ( 2004; ). Helicobacter pylori flagellin evades Toll-like receptor 5-mediated innate immunity. J Infect Dis 189, 1914–1920.[CrossRef]
    [Google Scholar]
  19. Gobert, A. P., Bambou, J. C., Werts, C., Balloy, V., Chignard, M., Moran, A. P. & Ferrero, R. L. ( 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.[CrossRef]
    [Google Scholar]
  20. Harris, P. R., Smythies, L. E., Smith, P. D. & Dubois, A. ( 2000; ). Inflammatory cytokine mRNA expression during early and persistent Helicobacter pylori infection in nonhuman primates. J Infect Dis 181, 783–786.[CrossRef]
    [Google Scholar]
  21. Ishihara, S., Rumi, M. A., Kadowaki, Y., Ortega-Cava, C. F., Yuki, T., Yoshino, N., Miyaoka, Y., Kazumori, H., Ishimura, N. & other authors ( 2004; ). Essential role of MD-2 in TLR4-dependent signaling during Helicobacter pylori-associated gastritis. J Immunol 173, 1406–1416.[CrossRef]
    [Google Scholar]
  22. Ishii, E., Yokota, K., Sugiyama, T., Fujinaga, Y., Ayada, K., Hokari, I., Hayashi, S., Hirai, Y., Asaka, M., Oguma, K. & other authors ( 2001; ). Immunoglobulin G1 antibody response to Helicobacter pylori heat shock protein 60 is closely associated with low-grade gastric mucosa-associated lymphoid tissue lymphoma. Clin Diagn Lab Immunol 8, 1056–1059.
    [Google Scholar]
  23. Iwao, E., Hirayama, F., Takagi, S., Yokoyama, Y. & Ikeda, Y. ( 1999; ). Virulence factors of Helicobacter pylori affecting its gastric colonization in Mongolian gerbils. J Gastroenterol 34 (Suppl. 11), 47–54.
    [Google Scholar]
  24. Juttner, S., Cramer, T., Wessler, S., Walduck, A., Gao, F., Schmitz, F., Wunder, C., Weber, M., Fischer, S. M. & other authors ( 2003; ). Helicobacter pylori stimulates host cyclooxygenase-2 gene transcription: critical importance of MEK/ERK-dependent activation of USF1/-2 and CREB transcription factors. Cell Microbiol 5, 821–834.[CrossRef]
    [Google Scholar]
  25. Kawahara, T., Kuwano, Y., Teshima-Kondo, S., Kawai, T., Nikawa, T., Kishi, K. & Rokutan, K. ( 2001; ). Toll-like receptor 4 regulates gastric pit cell responses to Helicobacter pylori infection. J Med Invest 48, 190–197.
    [Google Scholar]
  26. Keates, S., Keates, A. C., Warny, M., Peek, R. M., Jr, Murray, P. G. & Kelly, C. P. ( 1999; ). Differential activation of mitogen-activated protein kinases in AGS gastric epithelial cells by cag+ and cagHelicobacter pylori. J Immunol 163, 5552–5559.
    [Google Scholar]
  27. Kol, A., Sukhova, G. K., Lichtman, A. H. & Libby, P. ( 1998; ). Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-alpha and matrix metalloproteinase expression. Circulation 98, 300–307.[CrossRef]
    [Google Scholar]
  28. Kol, A., Bourcier, T., Lichtman, A. H. & Libby, P. ( 1999; ). Chlamydial and human heat shock protein 60s activate human vascular endothelium, smooth muscle cells, and macrophages. J Clin Invest 103, 571–577.[CrossRef]
    [Google Scholar]
  29. Kyriakis, J. M. & Avruch, J. ( 2001; ). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81, 807–869.
    [Google Scholar]
  30. Lin, S. N., Ayada, K., Zhao, Y., Yokota, K., Takenaka, R., Okada, H., Kan, R., Hayashi, S., Mizuno, M. & other authors ( 2005; ). Helicobacter pylori heat-shock protein 60 induces production of the pro-inflammatory cytokine IL8 in monocytes. J Med Microbiol 54, 225–233.[CrossRef]
    [Google Scholar]
  31. Maeda, S., Akanuma, M., Mitsuno, Y., Hirata, Y., Ogura, K., Yoshida, H., Shiratori, Y. & Omata, M. ( 2001; ). Distinct mechanism of Helicobacter pylori-mediated NF-kappa B activation between gastric cancer cells and monocytes. J Biol Chem 276, 44856–44864.[CrossRef]
    [Google Scholar]
  32. Maguire, M., Poole, S., Coates, A. R., Tormay, P., Wheeler-Jones, C. & Henderson, B. ( 2005; ). Comparative cell signalling activity of ultrapure recombinant chaperonin 60 proteins from prokaryotes and eukaryotes. Immunology 115, 231–238.[CrossRef]
    [Google Scholar]
  33. Mann, N. S. & Westblom, T. U. ( 1999; ). Helicobacter pylori and the future: an afterword. Curr Top Microbiol Immunol 241, 301–308.
    [Google Scholar]
  34. O'Neill, L. ( 2000; ). The Toll/interleukin-1 receptor domain: a molecular switch for inflammation and host defence. Biochem Soc Trans 28, 557–563.
    [Google Scholar]
  35. Peetermans, W. E., Raats, C. J., Langermans, J. A. & van Furth, R. ( 1994; ). Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol 39, 613–617.[CrossRef]
    [Google Scholar]
  36. Peetermans, W. E., Raats, C. J., van Furth, R. & Langermans, J. A. ( 1995; ). Mycobacterial 65-kilodalton heat shock protein induces tumor necrosis factor alpha and interleukin 6, reactive nitrogen intermediates, and toxoplasmastatic activity in murine peritoneal macrophages. Infect Immun 63, 3454–3458.
    [Google Scholar]
  37. Retzlaff, C., Yamamoto, Y., Hoffman, P. S., Friedman, H. & Klein, T. W. ( 1994; ). Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun 62, 5689–5693.
    [Google Scholar]
  38. Sarsfield, P., Jones, D. B., Wotherspoon, A. C., Harvard, T. & Wright, D. H. ( 1996; ). A study of accessory cells in the acquired lymphoid tissue of helicobacter gastritis. J Pathol 180, 18–25.[CrossRef]
    [Google Scholar]
  39. Shibata, W., Hirata, Y., Yoshida, H., Otsuka, M., Hoshida, Y., Ogura, K., Maeda, S., Ohmae, T., Yanai, A. & other authors ( 2005; ). NF-kappaB and ERK-signaling pathways contribute to the gene expression induced by cag PAI-positive-Helicobacter pylori infection. World J Gastroenterol 11, 6134–6143.
    [Google Scholar]
  40. Smith, M. F., Jr, Mitchell, A., Li, G., Ding, S., Fitzmaurice, A. M., Ryan, K., Crowe, S. & Goldberg, J. B. ( 2003; ). Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-kappa B activation and chemokine expression by epithelial cells. J Biol Chem 278, 32552–32560.[CrossRef]
    [Google Scholar]
  41. Suzuki, T., Kato, K., Ohara, S., Noguchi, K., Sekine, H., Nagura, H. & Shimosegawa, T. ( 2002; ). Localization of antigen-presenting cells in Helicobacter pylori-infected gastric mucosa. Pathol Int 52, 265–271.[CrossRef]
    [Google Scholar]
  42. Takenaka, R., Yokota, K., Ayada, K., Mizuno, M., Zhao, Y., Fujinami, Y., Lin, S.-N., Toyokawa, T., Okada, H. & other authors ( 2004; ). Helicobacter pylori heat-shock protein 60 induces inflammatory responses through the Toll-like receptor-triggered pathway in cultured human gastric epithelial cells. Microbiology 150, 3913–3922.[CrossRef]
    [Google Scholar]
  43. Torok, A. M., Bouton, A. H. & Goldberg, J. B. ( 2005; ). Helicobacter pylori induces interleukin-8 secretion by Toll-like receptor 2- and Toll-like receptor 5-dependent and -independent pathways. Infect Immun 73, 1523–1531.[CrossRef]
    [Google Scholar]
  44. Vabulas, R. M., Ahmad-Nejad, P., Ghose, S., Kirschning, C. J., Issels, R. D. & Wagner, H. ( 2002; ). HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 277, 15107–15112.[CrossRef]
    [Google Scholar]
  45. Wang, J. P., Kurt-Jones, E. A., Shin, O. S., Manchak, M. D., Levin, M. J. & Finberg, R. W. ( 2005; ). Varicella-zoster virus activates inflammatory cytokines in human monocytes and macrophages via Toll-like receptor 2. J Virol 79, 12658–12666.[CrossRef]
    [Google Scholar]
  46. Yamaoka, Y., Kwon, D. H. & Graham, D. Y. ( 2000; ). A M r 34,000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci U S A 97, 7533–7538.[CrossRef]
    [Google Scholar]
  47. Yokota, K., Kurebayashi, Y., Takayama, Y., Hayashi, S., Isogai, H., Isogai, E., Imai, K., Yabana, T., Yachi, A. & Oguma, K. ( 1991; ). Colonization of Helicobacter pylori in the gastric mucosa of Mongolian gerbils. Microbiol Immunol 35, 475–480.[CrossRef]
    [Google Scholar]
  48. Young, D. B. ( 1990; ). Chaperonins and immune response. Semin Cell Biol 1, 27–35.
    [Google Scholar]
  49. Zhang, D., Zhang, G., Hayden, M. S., Greenblatt, M. B., Bussey, C., Flavell, R. A. & Ghosh, S. ( 2004; ). A Toll-like receptor that prevents infection by uropathogenic bacteria. Science 303, 1522–1526.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.46882-0
Loading
/content/journal/jmm/10.1099/jmm.0.46882-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error