Prostaglandin E1 inhibits IL-6-induced MCP-1 expression by interfering specifically in IL-6-dependent ERK1/2, but not STAT3, activation

Biochemical Journal

Volumn 412, Issue 1, 2008, Pages 65-72

  Sobota, Radoslaw M ^a   Müller, Pia J ^a   Heinrich, Peter C ^a   Schaper, Fred ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Cytokine; Inflammation; Interleukin 6 (IL 6); Janus kinase (JAK); Prostaglandin (PG); Signal transducer and activator of transcription (STAT); Signal transduction

Indexed keywords

AMINO ACIDS; BLOOD; HORMONES; PROTEINS; SIGNAL TRANSDUCTION;

ANTI-INFLAMMATORY ACTIVITIES; JANUS KINASE; PROSTAGLANDIN;

GENE EXPRESSION;

CYCLIC AMP; FORSKOLIN; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; PERTUSSIS TOXIN; PROSTAGLANDIN E1; STAT3 PROTEIN;

ARTICLE; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ALPROSTADIL; ANIMALS; CELLS, CULTURED; CHEMOKINE CCL2; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOWN-REGULATION; ENZYME ACTIVATION; FORSKOLIN; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTERLEUKIN-6; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PERTUSSIS TOXIN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; SUBSTRATE SPECIFICITY;

HUMAN ECHOVIRUS 1;

EID: 43549111588     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071572     Document Type: Article

References (49)

1. Bode, J. and Heinrich, P. C. (2001) Interleukin-6 signaling during the acute-phase response of the liver. In The Liver: Biology and Pathobiology (Arias, I. M., Boyer, J. L., Chisari, F. V., Fausto, N., Schachter, D. and Shafritz, D. A., eds.), pp. 565-580, Lippincott Williams Wilkins, Philadelphia
2. Andus, T., Geiger, T., Hirano, T., Kishimoto, T., Tran-Thi, T. A., Decker, K. and Heinrich, P. C. (1988) Regulation of synthesis and secretion of major rat acute-phase proteins by recombinant human interleukin-6 (BSF-2/IL-6) in hepatocyte primary cultures. Eur. J. Biochem. 173, 287-293
3. Scheller, J., Grötzinger, J. and Rose-John, S. (2006) Updating interleukin-6 classic- and trans-signaling. Signal Transduction 6, 240-259
4. Heinrich, P. C., Behrmann, I., Müller-Newen, G., Schaper, F. and Graeve, L. (1998) Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 334, 297-314
5. Heinrich, P. C., Behrmann, I., Haan, S., Hermanns, H. M., Müller-Newen, G. and Schaper, F. (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374, 1-20
6. Schmitz, J., Dahmen, H., Grimm, C., Gendo, C., Müller-Newen, G., Heinrich, P. C. and Schaper, F. (2000) The cytoplasmic tyrosine motifs in full-length glycoprotein 130 have different roles in IL-6 signal transduction. J. Immunol. 164, 848-854
7. Lehmann, U., Sommer, U., Smyczek, T., Hörtner, M., Frisch, W., Volkmer-Engert, R., Heinrich, P. C., Schaper, F. and Haan, S. (2006) Determinants governing the potency of STAT3 activation via the individual STAT3-recruiting motifs of gp130. Cell. Signaling 18, 40-49
8. Fukada, T., Hibi, M., Yamanaka, Y., Takahashi-Tezuka, M., Fujitani, Y., Yamaguchi, T., Nakajima, K. and Hirano, T. (1996) Two signals are necessary for cell proliferation induced by a cytokine receptor gp130: involvement of STAT3 in anti-apoptosis. Immunity 5, 449-460
9. Nakajima, K., Yamanaka, Y., Nakae, K., Kojima, H., Ichiba, M., Kiuchi, N., Kitaoka, T., Fukada, T., Hibi, M. and Hirano, T. (1996) A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651-3658
10. Ihara, S., Nakajima, K., Fukada, T., Hibi, M., Nagata, S., Hirano, T. and Fukui, Y. (1997) Dual control of neurite outgrowth by STAT3 and MAP kinase in PC12 cells stimulated with interleukin-6. EMBO J. 16, 5345-5352
11. Schiemann, W. P., Bartoe, J. L. and Nathanson, N. M. (1997) Box 3-independent signaling mechanisms are involved in leukemia inhibitory factor receptor α- and gp130-mediated stimulation of mitogen-activated protein kinase. Evidence for participation of multiple signaling pathways which converge at Ras. J. Biol. Chem. 272, 16631-16636
12. Schaper, F., Gendo, C., Eck, M., Schmitz, J., Grimm, C., Anhuf, D., Kerr, I. M. and Heinrich, P. C. (1998) Activation of the protein tyrosine phophatase SHP2 via the interleukin-6 signal transducing receptor protein gp130 requires JAK1 and limits acute-phase protein expression. Biochem. J. 335, 557-565
13. Lehmann, U., Schmitz, J., Weissenbach, M., Sobota, R. M., Hörtner, M., Friederichs, K., Behrmann, I., Tsiaris, W., Sasaki, A., Schneider-Mergener, J. et al. (2003) SHP2 and SOCS3 contribute to Tyr-759-dependent attenuation of interleukin-6 signaling through gp130. J. Biol. Chem. 278, 661-671
14. Schmitz, J., Weissenbach, M., Haan, S., Heinrich, P. C. and Schaper, F. (2000) SOCS3 exerts its inhibitory function on interleukin-6 signal transduction through the SHP2 recruitment site of gp130. J. Biol. Chem. 275, 12848-12856
15. Ernst, M. and Jenkins, B. J. (2004) Acquiring signalling specificity from the cytokine receptor gp130. Trends Genet. 20, 23-32
16. Endo, T. A., Masuhara, M., Yokouchi, M., Suzuki, R., Sakamoto, H., Mitsui, K., Matsumoto, A., Tanimura, S., Ohtsubo, M., Misawa, H. et al. (1997) A new protein containing an SH2 domain that inhibits JAK kinases. Nature 387, 921-924
17. Naka, T., Narazaki, M., Hirata, M., Matsumoto, T., Minamoto, S., Aono, A., Nishimoto, N., Kajita, T., Taga, T., Yoshizaki, K. et al. (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature 387, 924-929
18. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A. and Hilton, D. J. (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921
19. Sasaki, A., Yasukawa, H., Suzuki, A., Kamizono, S., Syoda, T., Kinjyo, I., Sasaki, M., Johnston, J. A. and Yoshimura, A. (1999) Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4, 339-351
20. Nicholson, S. E., De Souza, D., Fabri, L. J., Corbin, J., Willson, T. A., Zhang, J. G., Silva, A., Asimakis, M., Farley, A., Nash, A. D. et al. (2000) Suppressor of cytokine signaling-3 preferentially binds to the SHP-2-binding site on the shared cytokine receptor subunit gp130. Proc. Natl. Acad. Sci. U.S.A. 97, 6493-6498
21. Yamamoto, T., Sekine, Y., Kashima, K., Kubota, A., Sato, N., Aoki, N. and Matsuda, T. (2002) The nuclear isoform of protein-tyrosine phosphatase TC-PTP regulates interleukin-6-mediated signaling pathway through STAT3 dephosphorylation. Biochem. Biophys. Res. Commun. 297, 811-817
22. Yang, X. P., Albrecht, U., Zakowski, V., Sobota, R. M., Haussinger, D., Heinrich, P. C., Ludwig, S., Bode, J. G. and Schaper, F. (2004) Dual function of interleukin-1β for the regulation of interleukin-6-induced suppressor of cytokine signaling 3 expression. J. Biol. Chem. 279, 45279-45289
23. Ehlting, C., Lai, W. S., Schaper, F., Brenndorfer, E. D., Matthes, R. J., Heinrich, P. C., Ludwig, S., Blackshear, P. J., Gaestel, M., Haussinger, D. and Bode, J. G. (2007) Regulation of suppressor of cytokine signaling 3 (SOCS3) mRNA stability by TNF-α involves activation of the MKK6/p38MAPK/MK2 cascade. J. Immunol. 178, 2813-2826
24. Bode, J. G., Fischer, R., Häussinger, D., Graeve, L., Heinrich, P. C. and Schaper, F. (2001) The inhibitory effect of IL-1β on IL-6-induced α2-macroglobulin expression is due to activation of NF-κB. J. Immunol. 167, 1469-1481
25. Zhang, Z. and Fuller, G. M. (2000) Interleukin 1β inhibits interleukin 6-mediated rat γ-fibrinogen gene expression. Blood 96, 3466-3472
26. Sengupta, T. K., Talbot, E. S., Scherle, P. A. and Ivashkiv, L. B. (1998) Rapid inhibition of interleukin-6 signaling and stat3 activation mediated by mitogen-activated protein kinases. Proc. Natl. Acad. Sci. U.S.A. 95, 11107-11112
27. Ahmed, S. T., Mayer, A., Ji, J. D. and Ivashkiv, L. B. (2002) Inhibition of IL-6 signaling by a p38-dependent pathway occurs in the absence of new protein synthesis. J. Leukoc. Biol. 72, 154-162
28. Gao, F. and Horie, T. (2002) A synthetic analog of prostaglandin E(1) prevents the production of reactive oxygen species in the intestinal mucosa of methotrexate-treated rats. Life Sci. 71, 1091-1099
29. Hafez, T., Moussa, M., Nesim, I., Baligh, N., Davidson, B. and Abdul-Hadi, A. (2007) The effect of intraportal prostaglandin E1 on adhesion molecule expression, inflammatory modulator function, and histology in canine hepatic ischemia/reperfusion injury. J. Surg. Res. 138, 88-99
30. de Perrot, M., Fischer, S., Liu, M., Jin, R., Bai, X. H., Waddell, T. K. and Keshavjee, S. (2001) Prostaglandin E1 protects lung transplants from ischemia-reperfusion injury: a shift from pro- to anti-inflammatory cytokines. Transplantation 72, 1505-1512
31. Matsui, K., Ikeda, U., Murakami, Y., Yoshioka, T. and Shimada, K. (2003) Intravenous prostaglandin E1 reduces monocyte chemoattractant protein-1 levels in peripheral arterial obstructive disease. Am. Heart J. 145, 330-333
32. Sporri, B., Muller, K. M., Wiesmann, U. and Bickel, M. (1999) Soluble IL-6 receptor induces calcium flux and selectively modulates chemokine expression in human dermal fibroblasts. Int. Immunol. 11, 1053-1058
33. Weiergräber, O., Hemmann, U., Küster, A., Müller-Newen, G., Schneider, J., Rose-John, S., Kurschat, P., Brakenhoff, J. P. J., Hart, M. H. L., Stabel, S. and Heinrich, P. C. (1995) Soluble human interleukin-6 receptor: expression in insect cells, purification and characterization. Eur. J. Biochem. 234, 661-669
34. Noguchi, K., Shitashige, M., Endo, H., Kondo, H. and Ishikawa, I. (2002) Binary regulation of interleukin (IL)-6 production by EP1 and EP2/EP4 subtypes of PGE2 receptors in IL-1β-stimulated human gingival fibroblasts. J. Periodontal. Res. 37, 29-36
35. Schmitt, J. M. and Stork, P. J. (2002) PKA phosphorylation of Src mediates cAMP's inhibition of cell growth via Rap1. Mol. Cell 9, 85-94
36. Chio, C. C., Chang, Y. H., Hsu, Y. W., Chi, K. H. and Lin, W. W. (2004) PKA-dependent activation of PKC, p38 MAPK and IKK in macrophage: implication in the induction of inducible nitric oxide synthase and interleukin-6 by dibutyryl cAMP. Cell. Signalling 16, 565-575
37. Takanaga, H., Yoshitake, T., Hara, S., Yamasaki, C. and Kunimoto, M. (2004) cAMP-induced astrocytic differentiation of C6 glioma cells is mediated by autocrine interleukin-6. J. Biol. Chem. 279, 15441-15447
38. Bergamaschi, A., Corsi, M. and Garnier, M. J. (2006) Synergistic effects of cAMP-dependent signalling pathways and IL-1 on IL-6 production by H19-7/IGF-IR neuronal cells. Cell. Signalling 18, 1679-1684
39. Yin, F., Wang, Y. Y., Du, J. H., Li, C., Lu, Z. Z., Han, C. and Zhang, Y. Y. (2006) Noncanonical cAMP pathway and p38 MAPK mediate β2-adrenergic receptor-induced IL-6 production in neonatal mouse cardiac fibroblasts. J. Mol. Cell. Cardiol. 40, 384-393
40. Sands, W. A., Woolson, H. D., Milne, G. R., Rutherford, C. and Palmer, T. M. (2006) Exchange protein activated by cyclic AMP (Epac)-mediated induction of suppressor of cytokine signaling 3 (SOCS-3) in vascular endothelial cells. Mol. Cell Biol. 26, 6333-6346
41. Kirtland, S. J. (1988) Prostaglandin E1: a review. Prostaglandins Leukotrienes Essent. Fatty Acids 32, 165-174
42. Chen, J. and Iyengar, R. (1994) Suppression of Ras-induced transformation of NIH 3T3 cells by activated Gαs. Science 263, 1278-1281
43. Bos, C. L., Richel, D. J., Ritsema, T., Peppelenbosch, M. P. and Versteeg, H. H. (2004) Prostanoids and prostanoid receptors in signal transduction. Int. J. Biochem. Cell Biol. 36, 1187-1205
44. Cheon, H., Rho, Y. H., Choi, S. J., Lee, Y. H., Song, G. G., Sohn, J., Won, N. H. and Ji, J. D. (2006) Prostaglandin E2 augments IL-10 signaling and function. J. Immunol. 177, 1092-1100
45. de Silva, K. I., Daud, A. N., Deng, J., Jones, S. B., Gamelli, R. L. and Shankar, R. (2003) Prostaglandin E2 mediates growth arrest in NFS-60 cells by down-regulating interleukin-6 receptor expression. Biochem. J. 370, 315-321
46. Schmitt, J. M. and Stork, P. J. (2001) Cyclic AMP-mediated inhibition of cell growth requires the small G protein Rap1. Mol. Cell Biol. 21, 3671-3683
47. Stork, P. J. (2003) Does Rap1 deserve a bad Rap? Trends Biochem. Sci. 28, 267-275
48. Stork, P. J. and Schmitt, J. M. (2002) Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol. 12, 258-266
49. Wang, Z., Dillon, T. J., Pokala, V., Mishra, S., Labudda, K., Hunter, B. and Stork, P. J. (2006) Rap1-mediated activation of extracellular signal-regulated kinases by cyclic AMP is dependent on the mode of Rap1 activation. Mol. Cell Biol. 26, 2130-2145