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PMID: 10022889 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Jun kinase phosphorylates and regulates the DNA binding activity of an octamer binding protein, T-cell factor beta1.

Molecular and cellular biology ·Vol. 19 ·No. 3 ·1999-03-00 ·Pages 2021-31

Kasibhatla S, Tailor P, Bonefoy-Berard N, Mustelin T, Altman A, Fotedar A

Abstract

POU domain proteins have been implicated as key regulators during development and lymphocyte activation. The POU domain protein T-cell factor beta1 (TCFbeta1), which binds octamer and octamer-related sequences, is a potent transactivator. In this study, we showed that TCFbeta1 is phosphorylated following activation via the T-cell receptor or by stress-induced signals. Phosphorylation of TCFbeta1 occurred predominantly at serine and threonine residues. Signals which upregulate Jun kinase (JNK)/stress-activated protein kinase activity also lead to association of JNK with TCFbeta1. JNK associates with the activation domain of TCFbeta1 and phosphorylates its DNA binding domain. The phosphorylation of recombinant TCFbeta1 by recombinant JNK enhances the ability of TCFbeta1 to bind to a consensus octamer motif. Consistent with this conclusion, TCFbeta1 upregulates reporter gene transcription in an activation- and JNK-dependent manner. In addition, inhibition of JNK activity by catalytically inactive MEKK (in which methionine was substituted for the lysine at position 432) also inhibits the ability of TCFbeta1 to drive inducible transcription from the interleukin-2 promoter. These results suggest that stress-induced signals and T-cell activation induce JNK, which then acts on multiple cis sequences by modulating distinct transactivators like c-Jun and TCFbeta1. This demonstrates a coupling between the JNK activation pathway and POU domain proteins and implicates TCFbeta1 as a physiological target in the JNK signal transduction pathway leading to coordinated biological responses.

MeSH Terms
Amino Acid Sequence Binding Sites Calcium-Calmodulin-Dependent Protein Kinases/metabolism DNA/metabolism DNA-Binding Proteins/genetics,metabolism Humans Interleukin-2/genetics JNK Mitogen-Activated Protein Kinases Jurkat Cells Mitogen-Activated Protein Kinase 9 Mitogen-Activated Protein Kinases Molecular Sequence Data POU Domain Factors Phosphorylation Promoter Regions, Genetic Protein Kinases/genetics,metabolism Recombinant Fusion Proteins/genetics,metabolism Transcriptional Activation
Chemicals
DNA-Binding Proteins Interleukin-2 POU Domain Factors POU6F1 protein, human Recombinant Fusion Proteins DNA Protein Kinases Mitogen-Activated Protein Kinase 9 Calcium-Calmodulin-Dependent Protein Kinases JNK Mitogen-Activated Protein Kinases Mitogen-Activated Protein Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kasibhatla S
Divisions of Molecular Biology, La Jolla Institute for Allergy and Immunology, San Diego, California 92121, USA.
Tailor P
Bonefoy-Berard N
Mustelin T
Altman A
Fotedar A
References (47)
47 references, click to expand
  1. Characterization of antigen receptor response elements within the interleukin-2 enhancer.
    Mol Cell Biol. 1988 Apr;8(4):1715-24 PMID: 3260003
  2. Oct-2, although not required for early B-cell development, is critical for later B-cell maturation and for postnatal survival.
    Genes Dev. 1993 Apr;7(4):570-82 PMID: 8096198
  3. A human lymphoid-specific transcription factor that activates immunoglobulin genes is a homoeobox protein.
    Nature. 1988 Dec 8;336(6199):551-7 PMID: 2904654
  4. The POU domain: a large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products.
    Genes Dev. 1988 Dec;2(12A):1513-6 PMID: 3215510
  5. The solution structure of the Oct-1 POU-specific domain reveals a striking similarity to the bacteriophage lambda repressor DNA-binding domain.
    Cell. 1993 Apr 9;73(1):193-205 PMID: 8462099
  6. A novel class of murine POU gene predominantly expressed in central nervous system.
    J Biol Chem. 1993 Apr 5;268(10):7449-57 PMID: 8463278
  7. p70 lupus autoantigen binds the enhancer of the T-cell receptor beta-chain gene.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2685-9 PMID: 8464876
  8. Solution structure of the POU-specific DNA-binding domain of Oct-1.
    Nature. 1993 Apr 29;362(6423):852-5 PMID: 8479524
  9. A novel POU domain protein which binds to the T-cell receptor beta enhancer.
    Mol Cell Biol. 1993 Sep;13(9):5450-60 PMID: 8102789
  10. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain.
    Genes Dev. 1993 Nov;7(11):2135-48 PMID: 8224842
  11. Brn-5 is a divergent POU domain factor highly expressed in layer IV of the neocortex.
    J Biol Chem. 1993 Nov 5;268(31):23390-8 PMID: 7901208
  12. Differential expression of four members of the POU family of proteins in activated and phorbol 12-myristate 13-acetate-treated Jurkat T cells.
    Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):10260-4 PMID: 8234287
  13. 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
  14. A human POU domain gene, mPOU, is expressed in developing brain and specific adult tissues.
    Eur J Biochem. 1994 Mar 15;220(3):753-62 PMID: 7908264
  15. The stress-activated protein kinase subfamily of c-Jun kinases.
    Nature. 1994 May 12;369(6476):156-60 PMID: 8177321
  16. JNK is involved in signal integration during costimulation of T lymphocytes.
    Cell. 1994 Jun 3;77(5):727-36 PMID: 8205621
  17. c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases.
    Mol Cell Biol. 1994 Oct;14(10):6683-8 PMID: 7935387
  18. JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation.
    Genes Dev. 1994 Dec 15;8(24):2996-3007 PMID: 8001819
  19. Transcription factor ATF2 regulation by the JNK signal transduction pathway.
    Science. 1995 Jan 20;267(5196):389-93 PMID: 7824938
  20. Stress-activated protein kinases bind directly to the delta domain of c-Jun in resting cells: implications for repression of c-Jun function.
    Oncogene. 1995 Mar 2;10(5):849-55 PMID: 7898927
  21. ATF-2 contains a phosphorylation-dependent transcriptional activation domain.
    EMBO J. 1995 Apr 18;14(8):1785-97 PMID: 7737129
  22. 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
  23. Pip, a novel IRF family member, is a lymphoid-specific, PU.1-dependent transcriptional activator.
    Genes Dev. 1995 Jun 1;9(11):1377-87 PMID: 7797077
  24. 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
  25. Integration of MAP kinase signal transduction pathways at the serum response element.
    Science. 1995 Jul 21;269(5222):403-7 PMID: 7618106
  26. M-phase-specific phosphorylation of the POU transcription factor GHF-1 by a cell cycle-regulated protein kinase inhibits DNA binding.
    Mol Cell Biol. 1995 Dec;15(12):6694-701 PMID: 8524234
  27. p21 contains independent binding sites for cyclin and cdk2: both sites are required to inhibit cdk2 kinase activity.
    Oncogene. 1996 May 16;12(10):2155-64 PMID: 8668341
  28. Transfer of proteins to membranes facilitates both cyanogen bromide cleavage and two-dimensional proteolytic mapping.
    Oncogene. 1990 Jun;5(6):921-3 PMID: 1688326
  29. The promoter of the human interleukin-2 gene contains two octamer-binding sites and is partially activated by the expression of Oct-2.
    Mol Cell Biol. 1990 Oct;10(10):5464-72 PMID: 2204815
  30. Dwarf locus mutants lacking three pituitary cell types result from mutations in the POU-domain gene pit-1.
    Nature. 1990 Oct 11;347(6293):528-33 PMID: 1977085
  31. I-POU: a POU-domain protein that inhibits neuron-specific gene activation.
    Nature. 1991 Apr 18;350(6319):577-84 PMID: 1673230
  32. POU-domain transcription factors: pou-er-ful developmental regulators.
    Genes Dev. 1991 Jun;5(6):897-907 PMID: 2044958
  33. Variable effects of phosphorylation of Pit-1 dictated by the DNA response elements.
    Science. 1991 Aug 16;253(5021):786-9 PMID: 1652153
  34. Differential phosphorylation of the transcription factor Oct1 during the cell cycle.
    Science. 1991 Aug 30;253(5023):1022-6 PMID: 1887216
  35. Activation of early gene expression in T lymphocytes by Oct-1 and an inducible protein, OAP40.
    Science. 1991 Oct 25;254(5031):558-62 PMID: 1683003
  36. Mitotic phosphorylation of the Oct-1 homeodomain and regulation of Oct-1 DNA binding activity.
    Science. 1991 Dec 20;254(5039):1814-6 PMID: 1684878
  37. Twin of I-POU: a two amino acid difference in the I-POU homeodomain distinguishes an activator from an inhibitor of transcription.
    Cell. 1992 Feb 7;68(3):491-505 PMID: 1346754
  38. Promoter-selective activation domains in Oct-1 and Oct-2 direct differential activation of an snRNA and mRNA promoter.
    Cell. 1992 Feb 21;68(4):755-67 PMID: 1739980
  39. Induction of the POU domain transcription factor Oct-2 during T-cell activation by cognate antigen.
    Mol Cell Biol. 1992 Jul;12(7):3149-54 PMID: 1620122
  40. Transactivation by AP-1 is a molecular target of T cell clonal anergy.
    Science. 1992 Aug 21;257(5073):1134-8 PMID: 1509265
  41. Mapping of an inducible element in the T cell receptor V beta 2 promoter.
    J Immunol. 1992 Sep 15;149(6):1980-6 PMID: 1387667
  42. Cyclin E/cdk2 and cyclin A/cdk2 kinases associate with p107 and E2F in a temporally distinct manner.
    Genes Dev. 1992 Oct;6(10):1874-85 PMID: 1398067
  43. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains.
    Cell. 1992 Dec 24;71(7):1181-94 PMID: 1335366
  44. The nuclear serine/threonine protein kinase DNA-PK.
    Crit Rev Eukaryot Gene Expr. 1992;2(4):283-314 PMID: 1486241
  45. Zebrafish pou[c]: a divergent POU family gene ubiquitously expressed during embryogenesis.
    Nucleic Acids Res. 1993 Feb 11;21(3):475-83 PMID: 8441661
  46. Effect of PU.1 phosphorylation on interaction with NF-EM5 and transcriptional activation.
    Science. 1993 Mar 12;259(5101):1622-5 PMID: 8456286
  47. The C. elegans cell lineage and differentiation gene unc-86 encodes a protein with a homeodomain and extended similarity to transcription factors.
    Cell. 1988 Dec 2;55(5):757-69 PMID: 2903797
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1999-03-00
Pages
2021-31
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC83995
Subset
IM
Grants
NCI NIH HHS · R01 CA035299 · United States
NIAID NIH HHS · AI54301 · United States
NCI NIH HHS · CA35299 · United States
NCI NIH HHS · CA74435 · United States
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