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. 1993 Oct;13(10):6260–6273. doi: 10.1128/mcb.13.10.6260

A growth factor-induced kinase phosphorylates the serum response factor at a site that regulates its DNA-binding activity.

V M Rivera 1, C K Miranti 1, R P Misra 1, D D Ginty 1, R H Chen 1, J Blenis 1, M E Greenberg 1
PMCID: PMC364685  PMID: 8413226

Abstract

A signaling pathway by which growth factors may induce transcription of the c-fos proto-oncogene has been characterized. Growth factor stimulation of quiescent fibroblasts activates a protein kinase cascade that leads to the rapid and transient phosphorylation of the serum response factor (SRF), a regulator of c-fos transcription. The in vivo kinetics of SRF phosphorylation and dephosphorylation parallel the activation and subsequent repression of c-fos transcription, suggesting that this phosphorylation event plays a critical role in the control of c-fos expression. The ribosomal S6 kinase pp90rsk, a growth factor-inducible kinase, phosphorylates SRF in vitro at serine 103, the site that becomes newly phosphorylated upon growth factor stimulation in vivo. Phosphorylation of serine 103 significantly enhances the affinity and rate with which SRF associates with its binding site, the serum response element, within the c-fos promoter. These results suggest a model in which the growth factor-induced phosphorylation of SRF at serine 103 contributes to the activation of c-fos transcription by facilitating the formation of an active transcription complex at the serum response element.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahn N. G., Seger R., Krebs E. G. The mitogen-activated protein kinase activator. Curr Opin Cell Biol. 1992 Dec;4(6):992–999. doi: 10.1016/0955-0674(92)90131-u. [DOI] [PubMed] [Google Scholar]
  2. Almendral J. M., Sommer D., Macdonald-Bravo H., Burckhardt J., Perera J., Bravo R. Complexity of the early genetic response to growth factors in mouse fibroblasts. Mol Cell Biol. 1988 May;8(5):2140–2148. doi: 10.1128/mcb.8.5.2140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Attar R. M., Gilman M. Z. Expression cloning of a novel zinc finger protein that binds to the c-fos serum response element. Mol Cell Biol. 1992 May;12(5):2432–2443. doi: 10.1128/mcb.12.5.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blenis J., Chung J., Erikson E., Alcorta D. A., Erikson R. L. Distinct mechanisms for the activation of the RSK kinases/MAP2 kinase/pp90rsk and pp70-S6 kinase signaling systems are indicated by inhibition of protein synthesis. Cell Growth Differ. 1991 Jun;2(6):279–285. [PubMed] [Google Scholar]
  5. Blenis J., Kuo C. J., Erikson R. L. Identification of a ribosomal protein S6 kinase regulated by transformation and growth-promoting stimuli. J Biol Chem. 1987 Oct 25;262(30):14373–14376. [PubMed] [Google Scholar]
  6. Boulden A. M., Sealy L. J. Maximal serum stimulation of the c-fos serum response element requires both the serum response factor and a novel binding factor, SRE-binding protein. Mol Cell Biol. 1992 Oct;12(10):4769–4783. doi: 10.1128/mcb.12.10.4769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boyle W. J., van der Geer P., Hunter T. Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin-layer cellulose plates. Methods Enzymol. 1991;201:110–149. doi: 10.1016/0076-6879(91)01013-r. [DOI] [PubMed] [Google Scholar]
  8. Chen R. H., Blenis J. Identification of Xenopus S6 protein kinase homologs (pp90rsk) in somatic cells: phosphorylation and activation during initiation of cell proliferation. Mol Cell Biol. 1990 Jun;10(6):3204–3215. doi: 10.1128/mcb.10.6.3204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen R. H., Chung J., Blenis J. Regulation of pp90rsk phosphorylation and S6 phosphotransferase activity in Swiss 3T3 cells by growth factor-, phorbol ester-, and cyclic AMP-mediated signal transduction. Mol Cell Biol. 1991 Apr;11(4):1861–1867. doi: 10.1128/mcb.11.4.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chen R. H., Sarnecki C., Blenis J. Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol Cell Biol. 1992 Mar;12(3):915–927. doi: 10.1128/mcb.12.3.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Christy B., Nathans D. Functional serum response elements upstream of the growth factor-inducible gene zif268. Mol Cell Biol. 1989 Nov;9(11):4889–4895. doi: 10.1128/mcb.9.11.4889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chung J., Chen R. H., Blenis J. Coordinate regulation of pp90rsk and a distinct protein-serine/threonine kinase activity that phosphorylates recombinant pp90rsk in vitro. Mol Cell Biol. 1991 Apr;11(4):1868–1874. doi: 10.1128/mcb.11.4.1868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cobb M. H., Boulton T. G., Robbins D. J. Extracellular signal-regulated kinases: ERKs in progress. Cell Regul. 1991 Dec;2(12):965–978. doi: 10.1091/mbc.2.12.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Cochran B. H., Zullo J., Verma I. M., Stiles C. D. Expression of the c-fos gene and of an fos-related gene is stimulated by platelet-derived growth factor. Science. 1984 Nov 30;226(4678):1080–1082. doi: 10.1126/science.6093261. [DOI] [PubMed] [Google Scholar]
  15. Curran T., Franza B. R., Jr Fos and Jun: the AP-1 connection. Cell. 1988 Nov 4;55(3):395–397. doi: 10.1016/0092-8674(88)90024-4. [DOI] [PubMed] [Google Scholar]
  16. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Erikson E., Maller J. L. Substrate specificity of ribosomal protein S6 kinase II from Xenopus eggs. Second Messengers Phosphoproteins. 1988;12(2-3):135–143. [PubMed] [Google Scholar]
  18. Erikson R. L. Structure, expression, and regulation of protein kinases involved in the phosphorylation of ribosomal protein S6. J Biol Chem. 1991 Apr 5;266(10):6007–6010. [PubMed] [Google Scholar]
  19. Fisch T. M., Prywes R., Roeder R. G. 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):3490–3502. doi: 10.1128/mcb.7.10.3490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Framson P., Bornstein P. A serum response element and a binding site for NF-Y mediate the serum response of the human thrombospondin 1 gene. J Biol Chem. 1993 Mar 5;268(7):4989–4996. [PubMed] [Google Scholar]
  21. Frederickson R. M., Micheau M. R., Iwamoto A., Miyamoto N. G. 5' flanking and first intron sequences of the human beta-actin gene required for efficient promoter activity. Nucleic Acids Res. 1989 Jan 11;17(1):253–270. doi: 10.1093/nar/17.1.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gauthier-Rouvière C., Cavadore J. C., Blanchard J. M., Lamb N. J., Fernandez A. p67SRF is a constitutive nuclear protein implicated in the modulation of genes required throughout the G1 period. Cell Regul. 1991 Jul;2(7):575–588. doi: 10.1091/mbc.2.7.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gille H., Sharrocks A. D., Shaw P. E. Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 1992 Jul 30;358(6385):414–417. doi: 10.1038/358414a0. [DOI] [PubMed] [Google Scholar]
  24. Gilman M. Z. 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. doi: 10.1101/gad.2.4.394. [DOI] [PubMed] [Google Scholar]
  25. Gilman M. Z., Wilson R. N., Weinberg R. A. Multiple protein-binding sites in the 5'-flanking region regulate c-fos expression. Mol Cell Biol. 1986 Dec;6(12):4305–4316. doi: 10.1128/mcb.6.12.4305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gonzalez G. A., Montminy M. R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell. 1989 Nov 17;59(4):675–680. doi: 10.1016/0092-8674(89)90013-5. [DOI] [PubMed] [Google Scholar]
  27. Graham R., Gilman M. Distinct protein targets for signals acting at the c-fos serum response element. Science. 1991 Jan 11;251(4990):189–192. doi: 10.1126/science.1898992. [DOI] [PubMed] [Google Scholar]
  28. Greenberg M. E., Hermanowski A. L., Ziff E. B. Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol Cell Biol. 1986 Apr;6(4):1050–1057. doi: 10.1128/mcb.6.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Greenberg M. E., Siegfried Z., Ziff E. B. 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):1217–1225. doi: 10.1128/mcb.7.3.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  31. Gualberto A., LePage D., Pons G., Mader S. L., Park K., Atchison M. L., Walsh K. Functional antagonism between YY1 and the serum response factor. Mol Cell Biol. 1992 Sep;12(9):4209–4214. doi: 10.1128/mcb.12.9.4209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hanson P. I., Kapiloff M. S., Lou L. L., Rosenfeld M. G., Schulman H. Expression of a multifunctional Ca2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation. Neuron. 1989 Jul;3(1):59–70. doi: 10.1016/0896-6273(89)90115-3. [DOI] [PubMed] [Google Scholar]
  33. Herrera R. E., Shaw P. E., Nordheim A. Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature. 1989 Jul 6;340(6228):68–70. doi: 10.1038/340068a0. [DOI] [PubMed] [Google Scholar]
  34. Herschman H. R. Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem. 1991;60:281–319. doi: 10.1146/annurev.bi.60.070191.001433. [DOI] [PubMed] [Google Scholar]
  35. Hill C. S., Marais R., John S., Wynne J., Dalton S., Treisman R. Functional analysis of a growth factor-responsive transcription factor complex. Cell. 1993 Apr 23;73(2):395–406. doi: 10.1016/0092-8674(93)90238-l. [DOI] [PubMed] [Google Scholar]
  36. Hipskind R. A., Rao V. N., Mueller C. G., Reddy E. S., Nordheim A. Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF. Nature. 1991 Dec 19;354(6354):531–534. doi: 10.1038/354531a0. [DOI] [PubMed] [Google Scholar]
  37. Janknecht R., Hipskind R. A., Houthaeve T., Nordheim A., Stunnenberg H. G. Identification of multiple SRF N-terminal phosphorylation sites affecting DNA binding properties. EMBO J. 1992 Mar;11(3):1045–1054. doi: 10.1002/j.1460-2075.1992.tb05143.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Karim F. D., Urness L. D., Thummel C. S., Klemsz M. J., McKercher S. R., Celada A., Van Beveren C., Maki R. A., Gunther C. V., Nye J. A. The ETS-domain: a new DNA-binding motif that recognizes a purine-rich core DNA sequence. Genes Dev. 1990 Sep;4(9):1451–1453. doi: 10.1101/gad.4.9.1451. [DOI] [PubMed] [Google Scholar]
  39. König H. Cell-type specific multiprotein complex formation over the c-fos serum response element in vivo: ternary complex formation is not required for the induction of c-fos. Nucleic Acids Res. 1991 Jul 11;19(13):3607–3611. doi: 10.1093/nar/19.13.3607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Latinkic B. V., O'Brien T. P., Lau L. F. Promoter function and structure of the growth factor-inducible immediate early gene cyr61. Nucleic Acids Res. 1991 Jun 25;19(12):3261–3267. doi: 10.1093/nar/19.12.3261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Lau L. F., Nathans D. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1182–1186. doi: 10.1073/pnas.84.5.1182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Luckow V. A., Summers M. D. High level expression of nonfused foreign genes with Autographa californica nuclear polyhedrosis virus expression vectors. Virology. 1989 May;170(1):31–39. doi: 10.1016/0042-6822(89)90348-6. [DOI] [PubMed] [Google Scholar]
  43. Luo K., Hurley T. R., Sefton B. M. Transfer of proteins to membranes facilitates both cyanogen bromide cleavage and two-dimensional proteolytic mapping. Oncogene. 1990 Jun;5(6):921–923. [PubMed] [Google Scholar]
  44. Manak J. R., Prywes R. Mutation of serum response factor phosphorylation sites and the mechanism by which its DNA-binding activity is increased by casein kinase II. Mol Cell Biol. 1991 Jul;11(7):3652–3659. doi: 10.1128/mcb.11.7.3652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Manak J. R., Prywes R. Phosphorylation of serum response factor by casein kinase II: evidence against a role in growth factor regulation of fos expression. Oncogene. 1993 Mar;8(3):703–711. [PubMed] [Google Scholar]
  46. Manak J. R., de Bisschop N., Kris R. M., Prywes R. Casein kinase II enhances the DNA binding activity of serum response factor. Genes Dev. 1990 Jun;4(6):955–967. doi: 10.1101/gad.4.6.955. [DOI] [PubMed] [Google Scholar]
  47. Marais R. M., Hsuan J. J., McGuigan C., Wynne J., Treisman R. Casein kinase II phosphorylation increases the rate of serum response factor-binding site exchange. EMBO J. 1992 Jan;11(1):97–105. doi: 10.1002/j.1460-2075.1992.tb05032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Marais R., Wynne J., Treisman R. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell. 1993 Apr 23;73(2):381–393. doi: 10.1016/0092-8674(93)90237-k. [DOI] [PubMed] [Google Scholar]
  49. McGuinness T. L., Lai Y., Greengard P. Ca2+/calmodulin-dependent protein kinase II. Isozymic forms from rat forebrain and cerebellum. J Biol Chem. 1985 Feb 10;260(3):1696–1704. [PubMed] [Google Scholar]
  50. Metz R., Ziff E. The helix-loop-helix protein rE12 and the C/EBP-related factor rNFIL-6 bind to neighboring sites within the c-fos serum response element. Oncogene. 1991 Dec;6(12):2165–2178. [PubMed] [Google Scholar]
  51. Misra R. P., Rivera V. M., Wang J. M., Fan P. D., Greenberg M. E. The serum response factor is extensively modified by phosphorylation following its synthesis in serum-stimulated fibroblasts. Mol Cell Biol. 1991 Sep;11(9):4545–4554. doi: 10.1128/mcb.11.9.4545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Mohun T. J., Chambers A. E., Towers N., Taylor M. V. Expression of genes encoding the transcription factor SRF during early development of Xenopus laevis: identification of a CArG box-binding activity as SRF. EMBO J. 1991 Apr;10(4):933–940. doi: 10.1002/j.1460-2075.1991.tb08027.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Nichols M., Weih F., Schmid W., DeVack C., Kowenz-Leutz E., Luckow B., Boshart M., Schütz G. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J. 1992 Sep;11(9):3337–3346. doi: 10.1002/j.1460-2075.1992.tb05412.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Norman C., Runswick M., Pollock R., Treisman R. 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. doi: 10.1016/0092-8674(88)90244-9. [DOI] [PubMed] [Google Scholar]
  55. Pearson R. B., Woodgett J. R., Cohen P., Kemp B. E. Substrate specificity of a multifunctional calmodulin-dependent protein kinase. J Biol Chem. 1985 Nov 25;260(27):14471–14476. [PubMed] [Google Scholar]
  56. Prywes R., Dutta A., Cromlish J. A., Roeder R. G. Phosphorylation of serum response factor, a factor that binds to the serum response element of the c-FOS enhancer. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7206–7210. doi: 10.1073/pnas.85.19.7206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Prywes R., Roeder R. G. Inducible binding of a factor to the c-fos enhancer. Cell. 1986 Dec 5;47(5):777–784. doi: 10.1016/0092-8674(86)90520-9. [DOI] [PubMed] [Google Scholar]
  58. Rangnekar V. M., Aplin A. C., Sukhatme V. P. The serum and TPA responsive promoter and intron-exon structure of EGR2, a human early growth response gene encoding a zinc finger protein. Nucleic Acids Res. 1990 May 11;18(9):2749–2757. doi: 10.1093/nar/18.9.2749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rao V. N., Huebner K., Isobe M., ar-Rushdi A., Croce C. M., Reddy E. S. elk, tissue-specific ets-related genes on chromosomes X and 14 near translocation breakpoints. Science. 1989 Apr 7;244(4900):66–70. doi: 10.1126/science.2539641. [DOI] [PubMed] [Google Scholar]
  60. Rivera V. M., Greenberg M. E. Growth factor-induced gene expression: the ups and downs of c-fos regulation. New Biol. 1990 Sep;2(9):751–758. [PubMed] [Google Scholar]
  61. Rivera V. M., Sheng M., Greenberg M. E. The inner core of the serum response element mediates both the rapid induction and subsequent repression of c-fos transcription following serum stimulation. Genes Dev. 1990 Feb;4(2):255–268. doi: 10.1101/gad.4.2.255. [DOI] [PubMed] [Google Scholar]
  62. Ryan W. A., Jr, Franza B. R., Jr, Gilman M. Z. Two distinct cellular phosphoproteins bind to the c-fos serum response element. EMBO J. 1989 Jun;8(6):1785–1792. doi: 10.1002/j.1460-2075.1989.tb03572.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Sadowski I., Ptashne M. A vector for expressing GAL4(1-147) fusions in mammalian cells. Nucleic Acids Res. 1989 Sep 25;17(18):7539–7539. doi: 10.1093/nar/17.18.7539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Schröter H., Mueller C. G., Meese K., Nordheim A. 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):1123–1130. doi: 10.1002/j.1460-2075.1990.tb08218.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Shaw P. E., Frasch S., Nordheim A. Repression of c-fos transcription is mediated through p67SRF bound to the SRE. EMBO J. 1989 Sep;8(9):2567–2574. doi: 10.1002/j.1460-2075.1989.tb08395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Sheng M., Thompson M. A., Greenberg M. E. CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science. 1991 Jun 7;252(5011):1427–1430. doi: 10.1126/science.1646483. [DOI] [PubMed] [Google Scholar]
  67. Sturgill T. W., Ray L. B., Erikson E., Maller J. L. Insulin-stimulated MAP-2 kinase phosphorylates and activates ribosomal protein S6 kinase II. Nature. 1988 Aug 25;334(6184):715–718. doi: 10.1038/334715a0. [DOI] [PubMed] [Google Scholar]
  68. Sweet L. J., Alcorta D. A., Jones S. W., Erikson E., Erikson R. L. Identification of mitogen-responsive ribosomal protein S6 kinase pp90rsk, a homolog of Xenopus S6 kinase II, in chicken embryo fibroblasts. Mol Cell Biol. 1990 May;10(5):2413–2417. doi: 10.1128/mcb.10.5.2413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Thomas S. M., DeMarco M., D'Arcangelo G., Halegoua S., Brugge J. S. Ras is essential for nerve growth factor- and phorbol ester-induced tyrosine phosphorylation of MAP kinases. Cell. 1992 Mar 20;68(6):1031–1040. doi: 10.1016/0092-8674(92)90075-n. [DOI] [PubMed] [Google Scholar]
  70. Treisman R. Identification and purification of a polypeptide that binds to the c-fos serum response element. EMBO J. 1987 Sep;6(9):2711–2717. doi: 10.1002/j.1460-2075.1987.tb02564.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Treisman R. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors. Cell. 1986 Aug 15;46(4):567–574. doi: 10.1016/0092-8674(86)90882-2. [DOI] [PubMed] [Google Scholar]
  72. Treisman R. The SRE: a growth factor responsive transcriptional regulator. Semin Cancer Biol. 1990 Feb;1(1):47–58. [PubMed] [Google Scholar]
  73. Treisman R. 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. doi: 10.1016/0092-8674(85)90285-5. [DOI] [PubMed] [Google Scholar]
  74. Troppmair J., Bruder J. T., App H., Cai H., Liptak L., Szeberényi J., Cooper G. M., Rapp U. R. Ras controls coupling of growth factor receptors and protein kinase C in the membrane to Raf-1 and B-Raf protein serine kinases in the cytosol. Oncogene. 1992 Sep;7(9):1867–1873. [PubMed] [Google Scholar]
  75. Vik T. A., Sweet L. J., Erikson R. L. Coinfection of insect cells with recombinant baculovirus expressing pp60v-src results in the activation of a serine-specific protein kinase pp90rsk. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2685–2689. doi: 10.1073/pnas.87.7.2685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Vosatka R. J., Hermanowski-Vosatka A., Metz R., Ziff E. B. Dynamic interactions of c-fos protein in serum-stimulated 3T3 cells. J Cell Physiol. 1989 Mar;138(3):493–502. doi: 10.1002/jcp.1041380308. [DOI] [PubMed] [Google Scholar]
  77. Wood K. W., Sarnecki C., Roberts T. M., Blenis J. 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):1041–1050. doi: 10.1016/0092-8674(92)90076-o. [DOI] [PubMed] [Google Scholar]
  78. de Vries-Smits A. M., Burgering B. M., Leevers S. J., Marshall C. J., Bos J. L. Involvement of p21ras in activation of extracellular signal-regulated kinase 2. Nature. 1992 Jun 18;357(6379):602–604. doi: 10.1038/357602a0. [DOI] [PubMed] [Google Scholar]

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