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
2024-12-01
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 pylor i 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 cag Helicobacter 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]
/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