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PMID: 10022864 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Activation of c-Jun N-terminal kinase 1 by UV irradiation is inhibited by wortmannin without affecting c-iun expression.

Molecular and cellular biology ·Vol. 19 ·No. 3 ·1999-03-00 ·Pages 1768-74

Fritz G, Kaina B

Abstract

Activation of c-Jun N-terminal kinases (JNKs)/stress-activated protein kinases is an early response of cells upon exposure to DNA-damaging agents. JNK-mediated phosphorylation of c-Jun is currently understood to stimulate the transactivating potency of AP-1 (e.g., c-Jun/c-Fos; c-Jun/ATF-2), thereby increasing the expression of AP-1 target genes. Here we show that stimulation of JNK1 activity is not a general early response of cells exposed to genotoxic agents. Treatment of NIH 3T3 cells with UV light (UV-C) as well as with methyl methanesulfonate (MMS) caused activation of JNK1 and an increase in c-Jun protein and AP-1 binding activity, whereas antineoplastic drugs such as mafosfamide, mitomycin C, N-hydroxyethyl-N-chloroethylnitrosourea, and treosulfan did not elicit this response. The phosphatidylinositol 3-kinase inhibitor wortmannin specifically blocked the UV-stimulated activation of JNK1 but did not affect UV-driven activation of extracellular regulated kinase 2 (ERK2). To investigate the significance of JNK1 for transactivation of c-jun, we analyzed the effect of UV irradiation on c-jun expression under conditions of wortmannin-mediated inhibition of UV-induced stimulation of JNK1. Neither the UV-induced increase in c-jun mRNA, c-Jun protein, and AP-1 binding nor the activation of the collagenase and c-jun promoters was affected by wortmannin. In contrast, the mitogen-activated protein kinase/ERK kinase inhibitor PD98056, which blocked ERK2 but not JNK1 activation by UV irradiation, impaired UV-driven c-Jun protein induction and AP-1 binding. Based on the data, we suggest that JNK1 stimulation is not essential for transactivation of c-jun after UV exposure, whereas activation of ERK2 is required for UV-induced signaling leading to elevated c-jun expression.

MeSH Terms
3T3 Cells Alkylating Agents/pharmacology Androstadienes/pharmacology Animals Calcium-Calmodulin-Dependent Protein Kinases/metabolism Collagenases/genetics Enzyme Activation Gene Expression Regulation, Neoplastic/drug effects JNK Mitogen-Activated Protein Kinases Methyl Methanesulfonate/pharmacology Mice Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinases Proto-Oncogene Proteins c-jun/genetics Transcription Factor AP-1/metabolism Ultraviolet Rays Wortmannin
Chemicals
Alkylating Agents Androstadienes Proto-Oncogene Proteins c-jun Transcription Factor AP-1 Methyl Methanesulfonate Calcium-Calmodulin-Dependent Protein Kinases JNK Mitogen-Activated Protein Kinases Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinases Collagenases Wortmannin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Fritz G
Institute of Toxicology, Division of Applied Toxicology, University of Mainz, D-55131 Mainz, Germany. Fritz@mail.uni-mainz.de
Kaina B
References (48)
48 references, click to expand
  1. ATF-2 contains a phosphorylation-dependent transcriptional activation domain.
    EMBO J. 1995 Apr 18;14(8):1785-97 PMID: 7737129
  2. Human mitogen-activated protein kinase kinase 7 (MKK7) is a highly conserved c-Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) activated by environmental stresses and physiological stimuli.
    J Biol Chem. 1998 Apr 10;273(15):9344-51 PMID: 9535930
  3. c-Fos is involved in the cellular defence against the genotoxic effect of UV radiation.
    Carcinogenesis. 1995 May;16(5):985-91 PMID: 7767997
  4. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway.
    Cell. 1995 Jun 30;81(7):1137-46 PMID: 7600581
  5. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs.
    Cell. 1995 Jun 30;81(7):1147-57 PMID: 7600582
  6. PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase.
    Curr Biol. 1995 Apr 1;5(4):393-403 PMID: 7627555
  7. The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments.
    J Biol Chem. 1995 Oct 20;270(42):25172-7 PMID: 7559652
  8. Intracellular signalling. PI 3-kinase puts GTP on the Rac.
    Curr Biol. 1995 Jun 1;5(6):577-9 PMID: 7552159
  9. Fos is an essential component of the mammalian UV response.
    EMBO J. 1995 Nov 1;14(21):5338-49 PMID: 7489723
  10. Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase.
    Science. 1996 May 31;272(5266):1347-9 PMID: 8650547
  11. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents.
    EMBO J. 1996 Oct 1;15(19):5314-25 PMID: 8895576
  12. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors.
    Science. 1996 Nov 15;274(5290):1194-7 PMID: 8895468
  13. Signal transduction. Three paths to stress relief.
    Nature. 1996 Nov 21;384(6606):213-4 PMID: 8918868
  14. Three distinct signalling responses by murine fibroblasts to genotoxic stress.
    Nature. 1996 Nov 21;384(6606):273-6 PMID: 8918879
  15. Role of the stress-activated/c-Jun NH2-terminal protein kinase pathway in the cellular response to adriamycin and other chemotherapeutic drugs.
    J Biol Chem. 1996 Nov 29;271(48):30950-5 PMID: 8940082
  16. Ultraviolet B-induced activated protein-1 activation does not require epidermal growth factor receptor but is blocked by a dominant negative PKClambda/iota.
    J Biol Chem. 1996 Dec 6;271(49):31262-8 PMID: 8940130
  17. The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light.
    EMBO J. 1996 Dec 2;15(23):6552-63 PMID: 8978682
  18. Stress-signalling kinase Sek1 protects thymocytes from apoptosis mediated by CD95 and CD3.
    Nature. 1997 Jan 23;385(6614):350-3 PMID: 9002521
  19. High-dose selection with mafosfamide results in sensitivity to DNA cross-linking agents: characterization of hypersensitive cell lines.
    Cancer Res. 1997 Feb 1;57(3):454-60 PMID: 9012473
  20. Targeted disruption of the MKK4 gene causes embryonic death, inhibition of c-Jun NH2-terminal kinase activation, and defects in AP-1 transcriptional activity.
    Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):3004-9 PMID: 9096336
  21. Activation of NF-kappaB by antineoplastic agents. Role of protein kinase C.
    J Biol Chem. 1997 Jun 6;272(23):14914-20 PMID: 9169462
  22. A general role for c-Fos in cellular protection against DNA-damaging carcinogens and cytostatic drugs.
    Cancer Res. 1997 Jul 1;57(13):2721-31 PMID: 9205083
  23. The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents.
    Mol Cell Biol. 1997 Aug;17(8):4792-800 PMID: 9234735
  24. The Ras farnesylation inhibitor BZA-5B increases the resistance to cisplatin in a human melanoma cell line.
    Anticancer Res. 1997 Jul-Aug;17(4A):2347-52 PMID: 9252645
  25. Effect of wortmannin and 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002) on N-formyl-methionyl-leucyl-phenylalanine-induced phospholipase D activation in differentiated HL60 cells: possible involvement of phosphatidylinositol 3-kinase in phospholipase D activation.
    Biochem Pharmacol. 1997 Jun 15;53(12):1929-36 PMID: 9256168
  26. Proteinase inhibitors I and II from potatoes specifically block UV-induced activator protein-1 activation through a pathway that is independent of extracellular signal-regulated kinases, c-Jun N-terminal kinases, and P38 kinase.
    Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):11957-62 PMID: 9342344
  27. Activation of CD95 (APO-1/Fas) signaling by ceramide mediates cancer therapy-induced apoptosis.
    EMBO J. 1997 Oct 15;16(20):6200-8 PMID: 9321399
  28. A novel SAPK/JNK kinase, MKK7, stimulated by TNFalpha and cellular stresses.
    EMBO J. 1997 Dec 1;16(23):7045-53 PMID: 9384583
  29. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  30. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  31. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1.
    Cell. 1988 Dec 2;55(5):875-85 PMID: 3142689
  32. Ionizing radiation regulates expression of the c-jun protooncogene.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5663-6 PMID: 2116003
  33. Protein kinase C mediates x-ray inducibility of nuclear signal transducers EGR1 and JUN.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2156-60 PMID: 1900938
  34. Phosphorylation of c-jun mediated by MAP kinases.
    Nature. 1991 Oct 17;353(6345):670-4 PMID: 1922387
  35. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73.
    Nature. 1991 Dec 12;354(6353):494-6 PMID: 1749429
  36. Oncoprotein-mediated signalling cascade stimulates c-Jun activity by phosphorylation of serines 63 and 73.
    Mol Cell Biol. 1992 Aug;12(8):3507-13 PMID: 1630458
  37. Embryonic stem (ES) cells lacking functional c-jun: consequences for growth and differentiation, AP-1 activity and tumorigenicity.
    Oncogene. 1992 Dec;7(12):2371-80 PMID: 1281302
  38. Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 amino acid adenovirus E1A protein.
    EMBO J. 1993 Feb;12(2):479-87 PMID: 8382609
  39. UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase.
    EMBO J. 1993 Mar;12(3):1005-12 PMID: 8384549
  40. Contribution of O6-alkylguanine and N-alkylpurines to the formation of sister chromatid exchanges, chromosomal aberrations, and gene mutations: new insights gained from studies of genetically engineered mammalian cell lines.
    Environ Mol Mutagen. 1993;22(4):283-92 PMID: 8223512
  41. Blockage of chemotactic peptide-induced stimulation of neutrophils by wortmannin as a result of selective inhibition of phosphatidylinositol 3-kinase.
    J Biol Chem. 1994 Feb 4;269(5):3563-7 PMID: 8106399
  42. Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin.
    J Biol Chem. 1994 Feb 4;269(5):3568-73 PMID: 8106400
  43. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain.
    Cell. 1994 Mar 25;76(6):1025-37 PMID: 8137421
  44. Binding of promoter-associated AP-1 is not altered during induction and subsequent repression of the c-jun promoter by TPA and UV irradiation.
    Carcinogenesis. 1994 Jun;15(6):1105-13 PMID: 8020141
  45. Involvement of growth factor receptors in the mammalian UVC response.
    Cell. 1994 Sep 23;78(6):963-72 PMID: 7923365
  46. PI 3-kinase activation is required for insulin stimulation of glucose transport into L6 myotubes.
    Biochem Biophys Res Commun. 1994 Nov 30;205(1):570-6 PMID: 7999081
  47. Transcription factor ATF2 regulation by the JNK signal transduction pathway.
    Science. 1995 Jan 20;267(5196):389-93 PMID: 7824938
  48. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents.
    EMBO J. 1995 Apr 18;14(8):1798-811 PMID: 7737130
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1999-03-00
Pages
1768-74
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC83970
Subset
IM
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