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PMID: 8007980 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Inhibition of v-raf-dependent c-fos expression and transformation by a kinase-defective mutant of the mitogen-activated protein kinase Erk2.

Molecular and cellular biology ·Vol. 14 ·No. 7 ·1994-07-00 ·Pages 4815-24

Kortenjann M, Thomae O, Shaw PE

Abstract

Receptor-bound growth factors elicit intracellular signals that lead to the phosphorylation and activation of numerous intracellular kinases and transcription factors with consequent changes in patterns of gene expression. Several oncogene products are able to mimic these signals, resulting in cell transformation and proliferation. For example, the introduction of oncogenic forms of Raf-1 kinase into fibroblasts induces transformation and leads to the constitutive expression of, among others, the c-fos proto-oncogene. Here it is shown that the elevation of c-fos promoter activity brought about by v-raf is mediated by TCF/Elk-1, which forms a ternary complex with SRF at the serum response element and is a substrate for mitogen-activating protein kinases in vitro. In NIH 3T3 fibroblasts, v-raf activates Erk2, and overexpression of an interfering mutant of Erk2 both blocks the ability of v-raf to activate the c-fos promoter and suppresses transformation. Mutation of individual mitogen-activating protein kinase phosphoacceptor sites in TCF/Elk-1 also compromises v-raf-activated expression of a Gal-Elk/Gal-chloramphenicol acetyltransferase reporter system. However, in at least one instance the introduction of glutamate, but not aspartate, at a phosphoacceptor site is compatible with activation. These results provide compelling evidence that phosphorylation of TCF/Elk-1 by Erk2 is a major link in the Raf-1 kinase-dependent signal transduction pathway that activates c-fos expression.

MeSH Terms
3T3 Cells Animals Base Sequence Calcium-Calmodulin-Dependent Protein Kinases/biosynthesis,genetics,metabolism Cell Transformation, Neoplastic Chloramphenicol O-Acetyltransferase/biosynthesis,metabolism DNA Primers DNA-Binding Proteins Genes, fos Kinetics Mice Mitogen-Activated Protein Kinase 1 Molecular Sequence Data Mutagenesis Oncogene Proteins v-raf Oncogenes Promoter Regions, Genetic Protein Serine-Threonine Kinases/biosynthesis,metabolism Protein-Tyrosine Kinases/metabolism Proto-Oncogene Proteins/biosynthesis,metabolism Proto-Oncogene Proteins c-fos/biosynthesis Proto-Oncogene Proteins c-raf Retroviridae Proteins, Oncogenic/biosynthesis,isolation & purification,metabolism Transcription Factors Transfection ets-Domain Protein Elk-1
Chemicals
DNA Primers DNA-Binding Proteins Proto-Oncogene Proteins Proto-Oncogene Proteins c-fos Retroviridae Proteins, Oncogenic Transcription Factors ets-Domain Protein Elk-1 Chloramphenicol O-Acetyltransferase Protein-Tyrosine Kinases Oncogene Proteins v-raf Protein Serine-Threonine Kinases Proto-Oncogene Proteins c-raf Calcium-Calmodulin-Dependent Protein Kinases Mitogen-Activated Protein Kinase 1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Kortenjann M
Max-Planck-Institut für Immunobiologie, Spemann Laboratories, Freiburg, Germany.
Thomae O
Shaw P E
References (80)
80 references, click to expand
  1. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme.
    J Biol Chem. 1989 May 15;264(14):8222-9 PMID: 2722778
  2. Isolation and characterization of SRF accessory proteins.
    Philos Trans R Soc Lond B Biol Sci. 1993 Jun 29;340(1293):325-32 PMID: 8103935
  3. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling.
    Cell. 1992 Aug 7;70(3):431-42 PMID: 1322798
  4. Structure and biological activity of v-raf, a unique oncogene transduced by a retrovirus.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4218-22 PMID: 6308607
  5. Functional analysis of a growth factor-responsive transcription factor complex.
    Cell. 1993 Apr 23;73(2):395-406 PMID: 8477450
  6. Phosphorylation of the C terminus of Fos protein is required for transcriptional transrepression of the c-fos promoter.
    Nature. 1990 Nov 1;348(6296):80-2 PMID: 2122257
  7. Bone and haematopoietic defects in mice lacking c-fos.
    Nature. 1992 Dec 24-31;360(6406):741-5 PMID: 1465144
  8. Activation of mitogen-activated protein kinase kinase by v-Raf in NIH 3T3 cells and in vitro.
    Science. 1992 Sep 4;257(5075):1404-7 PMID: 1326789
  9. Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling.
    Nature. 1993 May 6;363(6424):85-8 PMID: 8479541
  10. Raf-1 protein kinase is required for growth of induced NIH/3T3 cells.
    Nature. 1991 Jan 31;349(6308):426-8 PMID: 1992343
  11. Induction of c-fos gene and protein by growth factors precedes activation of c-myc.
    Nature. 1984 Dec 20-1985 Jan 2;312(5996):716-20 PMID: 6334806
  12. Activation of mitogen-activated protein (MAP) kinase by a MAP kinase-kinase.
    J Biol Chem. 1992 Jul 5;267(19):13135-7 PMID: 1320010
  13. Direct interaction of Ras and the amino-terminal region of Raf-1 in vitro.
    Nature. 1993 Jul 22;364(6435):352-5 PMID: 8332195
  14. SPXX, a frequent sequence motif in gene regulatory proteins.
    J Mol Biol. 1989 May 5;207(1):61-84 PMID: 2500531
  15. The SIF binding element confers sis/PDGF inducibility onto the c-fos promoter.
    EMBO J. 1990 Dec;9(13):4477-84 PMID: 2176154
  16. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element.
    Cell. 1992 Feb 7;68(3):597-612 PMID: 1339307
  17. Protein kinase C alpha activates RAF-1 by direct phosphorylation.
    Nature. 1993 Jul 15;364(6434):249-52 PMID: 8321321
  18. A vector for expressing GAL4(1-147) fusions in mammalian cells.
    Nucleic Acids Res. 1989 Sep 25;17(18):7539 PMID: 2798115
  19. The structure and function of the fos proto-oncogene.
    Crit Rev Oncog. 1989;1(1):65-88 PMID: 2518683
  20. Human Sos1: a guanine nucleotide exchange factor for Ras that binds to GRB2.
    Science. 1993 May 28;260(5112):1338-43 PMID: 8493579
  21. Activation of the MAP kinase pathway by the protein kinase raf.
    Cell. 1992 Oct 16;71(2):335-42 PMID: 1330321
  22. Ternary complex formation over the c-fos serum response element: p62TCF exhibits dual component specificity with contacts to DNA and an extended structure in the DNA-binding domain of p67SRF.
    EMBO J. 1992 Aug;11(8):3011-9 PMID: 1639071
  23. The SRE: a growth factor responsive transcriptional regulator.
    Semin Cancer Biol. 1990 Feb;1(1):47-58 PMID: 2133110
  24. Mutation of the c-fos gene dyad symmetry element inhibits serum inducibility of transcription in vivo and the nuclear regulatory factor binding in vitro.
    Mol Cell Biol. 1987 Mar;7(3):1217-25 PMID: 3561415
  25. Direct activation of the serine/threonine kinase activity of Raf-1 through tyrosine phosphorylation by the PDGF beta-receptor.
    Cell. 1989 Aug 25;58(4):649-57 PMID: 2475255
  26. Transcription activation by the adenovirus E1a protein.
    Nature. 1989 Mar 2;338(6210):39-44 PMID: 2521923
  27. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain.
    Cell. 1993 Apr 23;73(2):381-93 PMID: 8386592
  28. Growth factor signaling by receptor tyrosine kinases.
    Neuron. 1992 Sep;9(3):383-91 PMID: 1326293
  29. Epidermal growth factor regulates p21ras through the formation of a complex of receptor, Grb2 adapter protein, and Sos nucleotide exchange factor.
    Cell. 1993 May 7;73(3):611-20 PMID: 8490966
  30. The ability of a ternary complex to form over the serum response element correlates with serum inducibility of the human c-fos promoter.
    Cell. 1989 Feb 24;56(4):563-72 PMID: 2492906
  31. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences.
    Cell. 1985 Oct;42(3):889-902 PMID: 2414012
  32. Mitogen-activated protein kinases: versatile transducers for cell signaling.
    Trends Biochem Sci. 1992 Jun;17(6):233-8 PMID: 1323888
  33. Mitogen-activated protein kinase activation resulting from selective oncogene expression in NIH 3T3 and rat 1a cells.
    Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7355-9 PMID: 1323832
  34. Receptor tyrosine kinases.
    FASEB J. 1992 Mar;6(6):2332-7 PMID: 1312047
  35. Pleiotropic effects of a null mutation in the c-fos proto-oncogene.
    Cell. 1992 Nov 13;71(4):577-86 PMID: 1423615
  36. Role of ion flux in the control of c-fos expression.
    Nature. 1986 Aug 7-13;322(6079):552-5 PMID: 2426600
  37. Multiple sequence elements in the c-fos promoter mediate induction by cAMP.
    Genes Dev. 1989 Feb;3(2):198-211 PMID: 2541049
  38. Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus.
    J Cell Biol. 1993 Sep;122(5):1089-101 PMID: 8394846
  39. Molecular themes in oncogenesis.
    Cell. 1991 Jan 25;64(2):235-48 PMID: 1988146
  40. Transactivation of c-fos and beta-actin genes by raf as a step in early response to transmembrane signals.
    Nature. 1990 Mar 29;344(6265):463-6 PMID: 2157161
  41. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element.
    Cell. 1988 Dec 23;55(6):989-1003 PMID: 3203386
  42. Xenopus MAP kinase activator is a serine/threonine/tyrosine kinase activated by threonine phosphorylation.
    EMBO J. 1992 Aug;11(8):2903-8 PMID: 1322292
  43. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene.
    Nature. 1984 Oct 4-10;311(5985):433-8 PMID: 6090941
  44. The mitogen-activated protein kinase activator.
    Curr Opin Cell Biol. 1992 Dec;4(6):992-9 PMID: 1485970
  45. Phorbol ester stimulates a protein-tyrosine/threonine kinase that phosphorylates and activates the Erk-1 gene product.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8200-4 PMID: 1518847
  46. A sensitive method for detection of calmodulin-dependent protein kinase II activity in sodium dodecyl sulfate-polyacrylamide gel.
    Anal Biochem. 1989 Nov 15;183(1):139-43 PMID: 2559625
  47. Normal and oncogenic p21ras proteins bind to the amino-terminal regulatory domain of c-Raf-1.
    Nature. 1993 Jul 22;364(6435):308-13 PMID: 8332187
  48. The c-fos serum response element responds to protein kinase C-dependent and -independent signals but not to cyclic AMP.
    Genes Dev. 1988 Apr;2(4):394-402 PMID: 2453393
  49. Activation of the c-Raf protein kinase by protein kinase C phosphorylation.
    Oncogene. 1992 Nov;7(11):2259-62 PMID: 1437148
  50. MAP kinase activator from insulin-stimulated skeletal muscle is a protein threonine/tyrosine kinase.
    EMBO J. 1992 Jun;11(6):2123-9 PMID: 1318193
  51. Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro.
    J Biol Chem. 1993 Mar 5;268(7):5097-106 PMID: 8444886
  52. Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro.
    Cell. 1989 Jun 30;57(7):1109-22 PMID: 2472219
  53. Microtubule-associated-protein (MAP) kinase activated by nerve growth factor and epidermal growth factor in PC12 cells. Identity with the mitogen-activated MAP kinase of fibroblastic cells.
    Eur J Biochem. 1990 Nov 13;193(3):661-9 PMID: 2174361
  54. Fos and Jun: the AP-1 connection.
    Cell. 1988 Nov 4;55(3):395-7 PMID: 3141060
  55. Analysis and prediction of the different types of beta-turn in proteins.
    J Mol Biol. 1988 Sep 5;203(1):221-32 PMID: 3184187
  56. Complexes of Ras.GTP with Raf-1 and mitogen-activated protein kinase kinase.
    Science. 1993 Jun 11;260(5114):1658-61 PMID: 8503013
  57. c-fos sequence necessary for basal expression and induction by epidermal growth factor, 12-O-tetradecanoyl phorbol-13-acetate and the calcium ionophore.
    Mol Cell Biol. 1987 Oct;7(10):3490-502 PMID: 3119989
  58. Deregulated c-fos expression interferes with normal bone development in transgenic mice.
    Nature. 1987 Jan 29-Feb 4;325(6103):412-6 PMID: 3027573
  59. Raf-1 activates MAP kinase-kinase.
    Nature. 1992 Jul 30;358(6385):417-21 PMID: 1322500
  60. Xenopus MAP kinase activator: identification and function as a key intermediate in the phosphorylation cascade.
    EMBO J. 1992 Mar;11(3):973-82 PMID: 1312468
  61. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF.
    Cell. 1991 May 17;65(4):663-75 PMID: 2032290
  62. Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter.
    Nature. 1992 Jul 30;358(6385):414-7 PMID: 1322499
  63. The immunosuppressant rapamycin induces inactivation of p70s6k through dephosphorylation of a novel set of sites.
    J Biol Chem. 1993 Aug 5;268(22):16091-4 PMID: 8344891
  64. A protein domain conserved between yeast MCM1 and human SRF directs ternary complex formation.
    EMBO J. 1991 Dec;10(13):4219-29 PMID: 1756729
  65. Synergism in ternary complex formation between the dimeric glycoprotein p67SRF, polypeptide p62TCF and the c-fos serum response element.
    EMBO J. 1990 Apr;9(4):1123-30 PMID: 2108863
  66. Improved primer design for PCR-based, site-directed mutagenesis.
    Nucleic Acids Res. 1992 Mar 11;20(5):1147 PMID: 1549485
  67. Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF.
    Nature. 1991 Dec 19-26;354(6354):531-4 PMID: 1722028
  68. Proto-oncogene c-fos expression in growth regions of fetal bone and mesodermal web tissue.
    Nature. 1987 Aug 20-26;328(6132):711-4 PMID: 3614378
  69. Yeast (Saccharomyces cerevisiae) fructose-1,6-bisphosphatase. Properties of phospho and dephospho forms and of two mutants in which serine 11 has been changed by site-directed mutagenesis.
    J Biol Chem. 1988 May 5;263(13):6058-62 PMID: 2834362
  70. ras mediates nerve growth factor receptor modulation of three signal-transducing protein kinases: MAP kinase, Raf-1, and RSK.
    Cell. 1992 Mar 20;68(6):1041-50 PMID: 1312393
  71. SH2 and SH3 domains.
    Curr Biol. 1993 Jul 1;3(7):434-42 PMID: 15335710
  72. The assembly of signalling complexes by receptor tyrosine kinases.
    Bioessays. 1993 Mar;15(3):171-7 PMID: 8387783
  73. Negative charge at the casein kinase II phosphorylation site is important for transformation but not for Rb protein binding by the E7 protein of human papillomavirus type 16.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5187-91 PMID: 2052600
  74. A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf.
    Science. 1993 Apr 16;260(5106):315-9 PMID: 8385802
  75. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors.
    Cell. 1986 Aug 15;46(4):567-74 PMID: 3524858
  76. EGF induces tyrosine phosphorylation of phospholipase C-II: a potential mechanism for EGF receptor signaling.
    Cell. 1989 Jun 30;57(7):1101-7 PMID: 2472218
  77. The MAP kinase cascade is essential for diverse signal transduction pathways.
    Trends Biochem Sci. 1993 Apr;18(4):128-31 PMID: 8388132
  78. Inducible binding of a factor to the c-fos regulatory region.
    Proc Natl Acad Sci U S A. 1987 Mar;84(5):1272-6 PMID: 3029776
  79. Platelet-derived growth factor induces rapid but transient expression of the c-fos gene and protein.
    Nature. 1984 Dec 20-1985 Jan 2;312(5996):711-6 PMID: 6514007
  80. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction.
    Cell. 1992 Jul 10;70(1):93-104 PMID: 1623525
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1994-07-00
Pages
4815-24
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC358854
Subset
IM
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