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PMID: 11546803 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway.

The Journal of biological chemistry ·Vol. 276 ·No. 45 ·2001-11-09 ·Pages 42580-7

Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ

Abstract

Treatment of macrophages with pyridinyl imidazole inhibitors of p38 protein kinases can inhibit lipopolysaccharide-stimulated tumor necrosis factor alpha secretion. However, bone marrow-derived macrophages from tristetraprolin (TTP)-deficient mice were less sensitive than normal macrophages to this effect of p38 inhibitors, despite evidence for normal p38 activation in response to lipopolysaccharide. TTP is known to cause decreased stability of tumor necrosis factor alpha and granulocyte-macrophage colony-stimulating factor mRNAs after binding to an AU-rich element in their 3'-untranslated regions. A recombinant TTP fusion protein could be phosphorylated by a recombinant p38 kinase in cell-free assays and was phosphorylated to the same extent by immunoprecipitated p38 derived from normal and TTP-deficient cells stimulated with lipopolysaccharide; in both cases, the enzyme activity was inhibited by the p38 inhibitors. TTP phosphorylation also was increased in intact macrophages after lipopolysaccharide stimulation, an effect that was blocked by the p38 inhibitors. Finally, TTP in mammalian cell extracts bound less well to an AU-rich element RNA probe than did the same amount of TTP following dephosphorylation. These results suggest that TTP may be a component of the signaling cascade, initiated by inflammatory stimuli and mediated in part by activation of p38, that ultimately leads to enhanced secretion of tumor necrosis factor alpha.

MeSH Terms
3' Untranslated Regions/metabolism Animals DNA-Binding Proteins Enzyme Inhibitors/pharmacology Immediate-Early Proteins/physiology Interleukin-3/genetics Macrophages/metabolism Mice Mice, Knockout Mitogen-Activated Protein Kinases/antagonists & inhibitors,physiology Phosphorylation RNA, Messenger/analysis Recombinant Fusion Proteins/metabolism Tristetraprolin Tumor Necrosis Factor-alpha/biosynthesis,genetics p38 Mitogen-Activated Protein Kinases
Chemicals
3' Untranslated Regions DNA-Binding Proteins Enzyme Inhibitors Immediate-Early Proteins Interleukin-3 RNA, Messenger Recombinant Fusion Proteins Tristetraprolin Tumor Necrosis Factor-alpha Zfp36 protein, mouse Mitogen-Activated Protein Kinases p38 Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Carballo E
Office of Clinical Research and Laboratory of Signal Transduction, NIEHS, Research Triangle Park, North Carolina 27709, USA.
Cao H
Lai W S
Kennington E A
Campbell D
Blackshear P J
References (43)
43 references, click to expand
  1. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor.
    EMBO J. 1996 Apr 15;15(8):1914-23 PMID: 8617238
  2. Pharmacological profile of SB 203580, a selective inhibitor of cytokine suppressive binding protein/p38 kinase, in animal models of arthritis, bone resorption, endotoxin shock and immune function.
    J Pharmacol Exp Ther. 1996 Dec;279(3):1453-61 PMID: 8968371
  3. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors.
    Mol Cell Biol. 1997 May;17(5):2360-71 PMID: 9111305
  4. Novel homologues of CSBP/p38 MAP kinase: activation, substrate specificity and sensitivity to inhibition by pyridinyl imidazoles.
    Biochem Biophys Res Commun. 1997 Jun 27;235(3):533-8 PMID: 9207191
  5. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay.
    Mol Cell Biol. 1997 Aug;17(8):4611-21 PMID: 9234718
  6. Bone marrow transplantation reproduces the tristetraprolin-deficiency syndrome in recombination activating gene-2 (-/-) mice. Evidence that monocyte/macrophage progenitors may be responsible for TNFalpha overproduction.
    J Clin Invest. 1997 Sep 1;100(5):986-95 PMID: 9276715
  7. Characteristics of the intron involvement in the mitogen-induced expression of Zfp-36.
    J Biol Chem. 1998 Jan 2;273(1):506-17 PMID: 9417109
  8. Pharmacological effects of SB 220025, a selective inhibitor of P38 mitogen-activated protein kinase, in angiogenesis and chronic inflammatory disease models.
    J Pharmacol Exp Ther. 1998 Feb;284(2):687-92 PMID: 9454815
  9. The p38-MAPK inhibitor, SB203580, inhibits cardiac stress-activated protein kinases/c-Jun N-terminal kinases (SAPKs/JNKs).
    FEBS Lett. 1998 Apr 10;426(1):93-6 PMID: 9598985
  10. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin.
    Science. 1998 Aug 14;281(5379):1001-5 PMID: 9703499
  11. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2.
    Curr Biol. 1998 Sep 24;8(19):1049-57 PMID: 9768359
  12. Enhancement of the surface expression of tumor necrosis factor alpha (TNFalpha) but not the p55 TNFalpha receptor in the THP-1 monocytic cell line by matrix metalloprotease inhibitors.
    Biochem Pharmacol. 1999 Feb 1;57(3):291-302 PMID: 9890556
  13. Differential expression and activation of p38 mitogen-activated protein kinase alpha, beta, gamma, and delta in inflammatory cell lineages.
    J Immunol. 1999 Apr 1;162(7):4246-52 PMID: 10201954
  14. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies.
    Immunity. 1999 Mar;10(3):387-98 PMID: 10204494
  15. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA.
    Mol Cell Biol. 1999 Jun;19(6):4311-23 PMID: 10330172
  16. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism.
    EMBO J. 1999 Sep 15;18(18):4969-80 PMID: 10487749
  17. Induction of interleukin-8 synthesis integrates effects on transcription and mRNA degradation from at least three different cytokine- or stress-activated signal transduction pathways.
    Mol Cell Biol. 1999 Oct;19(10):6742-53 PMID: 10490613
  18. p38 MAPK signalling cascades in inflammatory disease.
    Mol Med Today. 1999 Oct;5(10):439-47 PMID: 10498912
  19. RWJ 67657, a potent, orally active inhibitor of p38 mitogen-activated protein kinase.
    J Pharmacol Exp Ther. 1999 Nov;291(2):680-7 PMID: 10525088
  20. Cytokine mRNA decay is accelerated by an inhibitor of p38-mitogen-activated protein kinase.
    Inflamm Res. 1999 Oct;48(10):533-8 PMID: 10563470
  21. MAPKAP kinase 2 is essential for LPS-induced TNF-alpha biosynthesis.
    Nat Cell Biol. 1999 Jun;1(2):94-7 PMID: 10559880
  22. New alpha-substituted succinate-based hydroxamic acids as TNFalpha convertase inhibitors.
    J Med Chem. 1999 Nov 18;42(23):4890-908 PMID: 10579851
  23. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability.
    Blood. 2000 Mar 15;95(6):1891-9 PMID: 10706852
  24. Arachidonic acid activates mitogen-activated protein (MAP) kinase-activated protein kinase 2 and mediates adhesion of a human breast carcinoma cell line to collagen type IV through a p38 MAP kinase-dependent pathway.
    J Biol Chem. 2000 Apr 14;275(15):11284-90 PMID: 10753939
  25. MAP kinase pathways activated by stress: the p38 MAPK pathway.
    Crit Care Med. 2000 Apr;28(4 Suppl):N67-77 PMID: 10807318
  26. Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway.
    Mol Cell Biol. 2000 Jun;20(11):3753-63 PMID: 10805719
  27. Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA.
    J Biol Chem. 2000 Jun 9;275(23):17827-37 PMID: 10751406
  28. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha.
    EMBO J. 2000 Aug 1;19(15):4154-63 PMID: 10921895
  29. Regulation of tumour necrosis factor alpha mRNA stability by the mitogen-activated protein kinase p38 signalling cascade.
    FEBS Lett. 2000 Oct 13;483(1):57-61 PMID: 11033356
  30. p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages in vitro and during infection in vivo.
    J Immunol. 2001 Jan 1;166(1):582-7 PMID: 11123340
  31. The 3' untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR.
    Mol Cell Biol. 2001 Feb;21(3):721-30 PMID: 11154260
  32. Gene suppression by tristetraprolin and release by the p38 pathway.
    Am J Physiol Lung Cell Mol Physiol. 2001 Aug;281(2):L499-508 PMID: 11435226
  33. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology.
    EMBO J. 2001 Jul 16;20(14):3760-70 PMID: 11447117
  34. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase.
    Mol Cell Biol. 2001 Sep;21(17):5778-89 PMID: 11486017
  35. An Escherichia coli vector to express and purify foreign proteins by fusion to and separation from maltose-binding protein.
    Gene. 1988 Dec 30;74(2):365-73 PMID: 3073105
  36. Dissociation of IL-1 beta synthesis and secretion in human blood monocytes stimulated with bacterial cell wall products.
    J Immunol. 1993 Nov 15;151(10):5574-85 PMID: 8228247
  37. Pyridinyl imidazoles inhibit IL-1 and TNF production at the protein level.
    Agents Actions. 1993;39 Spec No:C67-9 PMID: 8273589
  38. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis.
    Nature. 1994 Dec 22-29;372(6508):739-46 PMID: 7997261
  39. Phosphorylation of tristetraprolin, a potential zinc finger transcription factor, by mitogen stimulation in intact cells and by mitogen-activated protein kinase in vitro.
    J Biol Chem. 1995 Jun 2;270(22):13341-7 PMID: 7768935
  40. Mechanism of action of bicyclic imidazoles defines a translational regulatory pathway for tumor necrosis factor alpha.
    J Inflamm. 1995;45(2):97-105 PMID: 7583362
  41. Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast.
    Curr Opin Cell Biol. 1995 Dec;7(6):798-805 PMID: 8608010
  42. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency.
    Immunity. 1996 May;4(5):445-54 PMID: 8630730
  43. Mitogens stimulate the rapid nuclear to cytosolic translocation of tristetraprolin, a potential zinc-finger transcription factor.
    Mol Endocrinol. 1996 Feb;10(2):140-6 PMID: 8825554
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
2001-11-09
Epub
2001-00-06
Pages
42580-7
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC1351389
Subset
IM
Grants
NIEHS NIH HHS · Z01 ES090080-08 · United States
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