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The Journal of Immunology, Vol 158, Issue 7 3165-3173, Copyright © 1997 by American Association of Immunologists

ARTICLES

Actions of IL-1 are selectively controlled by p38 mitogen-activated protein kinase: regulation of prostaglandin H synthase-2, metalloproteinases, and IL-6 at different levels

SH Ridley, SJ Sarsfield, JC Lee, HF Bigg, TE Cawston, DJ Taylor, DL DeWitt and J Saklatvala
Department of Signalling, the Babraham Institute, Cambridge, United Kingdom.

The role of p38 mitogen-activated protein kinase (MAPK) in responses of human fibroblasts and vascular endothelial cells to IL-1 was investigated by use of a pyridinyl imidazole compound (SB 203580), which specifically inhibits the enzyme. SB 203580 inhibited (50% inhibitory concentration approximately 0.5 microM) IL-1-induced phosphorylation of heat shock protein 27 (an indicator of p38 MAPK activity) in fibroblasts without affecting the other known IL-1- activated protein kinase pathways (p42/p44 MAPK, p54 MAPK/c-Jun N- terminal kinase and beta-casein kinase). SB 203580 significantly inhibited IL-1-stimulated IL-6, (30 to 50% at 1 microM) but not IL-8 production from human fibroblasts (gingival and dermal) and umbilical vein endothelial cells. IL-1 induction of steady state level of IL-6 mRNA was not significantly inhibited, which is consistent with p38 MAPK regulating IL-6 production at the translational level. SB 203580 strongly inhibited IL-1-stimulated PG production by fibroblasts and human umbilical vein endothelial cells. This was associated with the inhibition of the induction of PGH synthase-2 protein and mRNA. SB 203580 also inhibited the stimulation of collagenase-1 and stromelysin- 1 production by IL-1 without affecting synthesis of the tissue inhibitor of metalloproteinases (TIMP)-1. SB 203580 prevented the increase in collagenase-1 and stromelysin-1 mRNA stimulated by IL-1. In a model of cartilage breakdown, short-term IL-1-stimulated proteoglycan resorption and inhibition of proteoglycan synthesis were unaffected by SB 203580, while longer term collagen breakdown was prevented. It is concluded that 1) p38 MAPK plays an important role in the regulation of some, but not all, responses to IL-1, and 2) it is involved in the regulation of mRNA levels of some IL-1-responsive genes.


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H. J. Cao, H.-S. Wang, Y. Zhang, H.-Y. Lin, R. P. Phipps, and T. J. Smith
Activation of Human Orbital Fibroblasts through CD40 Engagement Results in a Dramatic Induction of Hyaluronan Synthesis and Prostaglandin Endoperoxide H Synthase-2 Expression. INSIGHTS INTO POTENTIAL PATHOGENIC MECHANISMS OF THYROID-ASSOCIATED OPHTHALMOPATHY
J. Biol. Chem., November 6, 1998; 273(45): 29615 - 29625.
[Abstract] [Full Text] [PDF]

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K. Miyazawa, A. Mori, H. Miyata, M. Akahane, Y. Ajisawa, and H. Okudaira
Regulation of Interleukin-1beta -induced Interleukin-6 Gene Expression in Human Fibroblast-like Synoviocytes by p38 Mitogen-activated Protein Kinase
J. Biol. Chem., September 18, 1998; 273(38): 24832 - 24838.
[Abstract] [Full Text] [PDF]

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A. Krause, H. Holtmann, S. Eickemeier, R. Winzen, M. Szamel, K. Resch, J. Saklatvala, and M. Kracht
Stress-activated Protein Kinase/Jun N-terminal Kinase Is Required for Interleukin (IL)-1-induced IL-6 and IL-8 Gene Expression in the Human Epidermal Carcinoma Cell Line KB
J. Biol. Chem., September 11, 1998; 273(37): 23681 - 23689.
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M. Pouliot, C. Gilbert, P. Borgeat, P. E. Poubelle, S. Bourgoin, C. Créminon, J. Maclouf, S. R. Mccoll, and P. H. Naccache
Expression and activity of prostaglandin endoperoxide synthase-2 in agonist-activated human neutrophils
FASEB J, September 1, 1998; 12(12): 1109 - 1123.
[Abstract] [Full Text]

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A. Kumar, A. Middleton, T. C. Chambers, and K. D. Mehta
Differential Roles of Extracellular Signal-regulated Kinase-1/2 and p38MAPK in Interleukin-1beta - and Tumor Necrosis Factor-alpha -induced Low Density Lipoprotein Receptor Expression in HepG2 Cells
J. Biol. Chem., June 19, 1998; 273(25): 15742 - 15748.
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P. Kanakaraj, P. H. Schafer, D. E. Cavender, Y. Wu, K. Ngo, P. F. Grealish, S. A. Wadsworth, P. A. Peterson, J. J. Siekierka, C. A. Harris, et al.
Interleukin (IL)-1 Receptor-associated Kinase (IRAK) Requirement for Optimal Induction of Multiple IL-1 Signaling Pathways and IL-6 Production
J. Exp. Med., June 15, 1998; 187(12): 2073 - 2079.
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K. Miyazawa, A. Mori, K. Yamamoto, and H. Okudaira
Transcriptional Roles of CCAAT/Enhancer Binding Protein-beta , Nuclear Factor-kappa B, and C-promoter Binding Factor 1 in Interleukin (IL)-1beta -induced IL-6 Synthesis by Human Rheumatoid Fibroblast-like Synoviocytes
J. Biol. Chem., March 27, 1998; 273(13): 7620 - 7627.
[Abstract] [Full Text] [PDF]

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A. B. Meriin, V. L. Gabai, J. Yaglom, V. I. Shifrin, and M. Y. Sherman
Proteasome Inhibitors Activate Stress Kinases and Induce Hsp72. DIVERSE EFFECTS ON APOPTOSIS
J. Biol. Chem., March 13, 1998; 273(11): 6373 - 6379.
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F. Guesdon, C. G. Knight, L. M. Rawlinson, and J. Saklatvala
Dual Specificity of the Interleukin 1- and Tumor Necrosis Factor-activated beta  Casein Kinase
J. Biol. Chem., November 28, 1997; 272(48): 30017 - 30024.
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J. Da Silva, B. Pierrat, J.-L. Mary, and W. Lesslauer
Blockade of p38 Mitogen-activated Protein Kinase Pathway Inhibits Inducible Nitric-oxide Synthase Expression in Mouse Astrocytes
J. Biol. Chem., November 7, 1997; 272(45): 28373 - 28380.
[Abstract] [Full Text] [PDF]

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T. L. Born, D. E. Smith, K. E. Garka, B. R. Renshaw, J. S. Bertles, and J. E. Sims
Identification and Characterization of Two Members of a Novel Class of the Interleukin-1 Receptor (IL-1R) Family. DELINEATION OF A NEW CLASS OF IL-1R-RELATED PROTEINS BASED ON SIGNALING
J. Biol. Chem., September 22, 2000; 275(39): 29946 - 29954.
[Abstract] [Full Text] [PDF]

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G. E. Caughey, L. G. Cleland, J. R. Gamble, and M. J. James
Up-regulation of Endothelial Cyclooxygenase-2 and Prostanoid Synthesis by Platelets. ROLE OF THROMBOXANE A2
J. Biol. Chem., October 5, 2001; 276(41): 37839 - 37845.
[Abstract] [Full Text] [PDF]

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Y.-Z. Wang, P. Zhang, A. B. Rice, and J. C. Bonner
Regulation of Interleukin-1beta -induced Platelet-derived Growth Factor Receptor-alpha Expression in Rat Pulmonary Myofibroblasts by p38 Mitogen-activated Protein Kinase
J. Biol. Chem., July 14, 2000; 275(29): 22550 - 22557.
[Abstract] [Full Text] [PDF]


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