Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1995 Apr 18;14(8):1798–1811. doi: 10.1002/j.1460-2075.1995.tb07168.x

ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents.

H van Dam 1, D Wilhelm 1, I Herr 1, A Steffen 1, P Herrlich 1, P Angel 1
PMCID: PMC398273  PMID: 7737130

Abstract

The major regulators of the c-jun promoter are ATF-2 and c-Jun. They act as pre-bound heterodimers on two 'AP-1-like' sites, and are preferentially addressed by different types of extracellular signals. The transactivating potential of ATF-2 is stimulated to a higher extent than that of c-Jun by a broad group of agents causing DNA damage and other types of cellular stress, such as short-wavelength UV, or the alkylating compounds N-methyl-N'-nitro-N-nitroso-guanidine (MNNG) or methylmethanesulphonate (MMS). In contrast, treatment with the phorbol ester TPA preferentially enhances c-Jun-dependent transactivation but does not affect ATF-2. Accordingly, UV and MMS but not TPA induce c-jun transcription in F9 cells, which express ATF-2, but not c-Jun. Stimulation of ATF-2-dependent transactivation by genotoxic agents requires the presence of threonines 69 and 71 located in the N-terminal transactivation domain. These sites are the target of p54 and p46 stress-activated protein kinases (SAPKs) which bind to, and phosphorylate ATF-2 in vitro. However, p46 and p54 kinase activity is not increased by phorbol ester, which strongly suggests that the protein kinase phosphorylating c-Jun in response to TPA is distinct from SAPKs and does not act on ATF-2. Our data demonstrate that distinct signal transduction pathways converge at c-Jun/ATF-2, whereby each subunit is individually addressed by a specific class of protein kinases. This allows fine tuned modulation of c-jun expression by a large spectrum of extracellular signals.

Full text

PDF
1798

Images in this article

Selected References

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

  1. Abdel-Hafiz H. A., Chen C. Y., Marcell T., Kroll D. J., Hoeffler J. P. Structural determinants outside of the leucine zipper influence the interactions of CREB and ATF-2: interaction of CREB with ATF-2 blocks E1a-ATF-2 complex formation. Oncogene. 1993 May;8(5):1161–1174. [PubMed] [Google Scholar]
  2. Abdel-Hafiz H. A., Heasley L. E., Kyriakis J. M., Avruch J., Kroll D. J., Johnson G. L., Hoeffler J. P. Activating transcription factor-2 DNA-binding activity is stimulated by phosphorylation catalyzed by p42 and p54 microtubule-associated protein kinases. Mol Endocrinol. 1992 Dec;6(12):2079–2089. doi: 10.1210/mend.6.12.1337144. [DOI] [PubMed] [Google Scholar]
  3. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988 Dec 2;55(5):875–885. doi: 10.1016/0092-8674(88)90143-2. [DOI] [PubMed] [Google Scholar]
  4. Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
  5. Angel P., Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta. 1991 Dec 10;1072(2-3):129–157. doi: 10.1016/0304-419x(91)90011-9. [DOI] [PubMed] [Google Scholar]
  6. Angel P., Smeal T., Meek J., Karin M. Jun and v-jun contain multiple regions that participate in transcriptional activation in an interdependent manner. New Biol. 1989 Oct;1(1):35–43. [PubMed] [Google Scholar]
  7. Auer H. P., König H., Litfin M., Stein B., Rahmsdorf H. J. Ultraviolet irradiation, although it activates the transcription factor AP-1 in F9 teratocarcinoma stem cells, does not induce the full complement of differentiation-associated genes. Exp Cell Res. 1994 Sep;214(1):131–138. doi: 10.1006/excr.1994.1241. [DOI] [PubMed] [Google Scholar]
  8. Benbrook D. M., Jones N. C. Heterodimer formation between CREB and JUN proteins. Oncogene. 1990 Mar;5(3):295–302. [PubMed] [Google Scholar]
  9. Bengal E., Ransone L., Scharfmann R., Dwarki V. J., Tapscott S. J., Weintraub H., Verma I. M. Functional antagonism between c-Jun and MyoD proteins: a direct physical association. Cell. 1992 Feb 7;68(3):507–519. doi: 10.1016/0092-8674(92)90187-h. [DOI] [PubMed] [Google Scholar]
  10. Bergelson S., Pinkus R., Daniel V. Induction of AP-1 (Fos/Jun) by chemical agents mediates activation of glutathione S-transferase and quinone reductase gene expression. Oncogene. 1994 Feb;9(2):565–571. [PubMed] [Google Scholar]
  11. Boulton T. G., Nye S. H., Robbins D. J., Ip N. Y., Radziejewska E., Morgenbesser S. D., DePinho R. A., Panayotatos N., Cobb M. H., Yancopoulos G. D. 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):663–675. doi: 10.1016/0092-8674(91)90098-j. [DOI] [PubMed] [Google Scholar]
  12. Boulton T. G., Yancopoulos G. D., Gregory J. S., Slaughter C., Moomaw C., Hsu J., Cobb M. H. An insulin-stimulated protein kinase similar to yeast kinases involved in cell cycle control. Science. 1990 Jul 6;249(4964):64–67. doi: 10.1126/science.2164259. [DOI] [PubMed] [Google Scholar]
  13. Brach M. A., Herrmann F., Yamada H., Bäuerle P. A., Kufe D. W. Identification of NF-jun, a novel inducible transcription factor that regulates c-jun gene transcription. EMBO J. 1992 Apr;11(4):1479–1486. doi: 10.1002/j.1460-2075.1992.tb05192.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Buratowski S., Hahn S., Guarente L., Sharp P. A. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell. 1989 Feb 24;56(4):549–561. doi: 10.1016/0092-8674(89)90578-3. [DOI] [PubMed] [Google Scholar]
  15. Chatton B., Bocco J. L., Gaire M., Hauss C., Reimund B., Goetz J., Kedinger C. Transcriptional activation by the adenovirus larger E1a product is mediated by members of the cellular transcription factor ATF family which can directly associate with E1a. Mol Cell Biol. 1993 Jan;13(1):561–570. doi: 10.1128/mcb.13.1.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chatton B., Bocco J. L., Goetz J., Gaire M., Lutz Y., Kedinger C. Jun and Fos heterodimerize with ATFa, a member of the ATF/CREB family and modulate its transcriptional activity. Oncogene. 1994 Feb;9(2):375–385. [PubMed] [Google Scholar]
  17. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Deng T., Karin M. c-Fos transcriptional activity stimulated by H-Ras-activated protein kinase distinct from JNK and ERK. Nature. 1994 Sep 8;371(6493):171–175. doi: 10.1038/371171a0. [DOI] [PubMed] [Google Scholar]
  19. Devary Y., Gottlieb R. A., Lau L. F., Karin M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol. 1991 May;11(5):2804–2811. doi: 10.1128/mcb.11.5.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Devary Y., Gottlieb R. A., Smeal T., Karin M. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell. 1992 Dec 24;71(7):1081–1091. doi: 10.1016/s0092-8674(05)80058-3. [DOI] [PubMed] [Google Scholar]
  21. Dérijard B., Hibi M., Wu I. H., Barrett T., Su B., Deng T., Karin M., Davis R. J. 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):1025–1037. doi: 10.1016/0092-8674(94)90380-8. [DOI] [PubMed] [Google Scholar]
  22. Flint K. J., Jones N. C. Differential regulation of three members of the ATF/CREB family of DNA-binding proteins. Oncogene. 1991 Nov;6(11):2019–2026. [PubMed] [Google Scholar]
  23. Franklin C. C., Sanchez V., Wagner F., Woodgett J. R., Kraft A. S. Phorbol ester-induced amino-terminal phosphorylation of human JUN but not JUNB regulates transcriptional activation. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):7247–7251. doi: 10.1073/pnas.89.15.7247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gaire M., Chatton B., Kedinger C. Isolation and characterization of two novel, closely related ATF cDNA clones from HeLa cells. Nucleic Acids Res. 1990 Jun 25;18(12):3467–3473. doi: 10.1093/nar/18.12.3467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Georgopoulos K., Morgan B. A., Moore D. D. Functionally distinct isoforms of the CRE-BP DNA-binding protein mediate activity of a T-cell-specific enhancer. Mol Cell Biol. 1992 Feb;12(2):747–757. doi: 10.1128/mcb.12.2.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Hagmeyer B. M., König H., Herr I., Offringa R., Zantema A., van der Eb A., Herrlich P., Angel P. Adenovirus E1A negatively and positively modulates transcription of AP-1 dependent genes by dimer-specific regulation of the DNA binding and transactivation activities of Jun. EMBO J. 1993 Sep;12(9):3559–3572. doi: 10.1002/j.1460-2075.1993.tb06030.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hai T. W., Liu F., Coukos W. J., Green M. R. Transcription factor ATF cDNA clones: an extensive family of leucine zipper proteins able to selectively form DNA-binding heterodimers. Genes Dev. 1989 Dec;3(12B):2083–2090. doi: 10.1101/gad.3.12b.2083. [DOI] [PubMed] [Google Scholar]
  29. Hai T., Curran T. Cross-family dimerization of transcription factors Fos/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3720–3724. doi: 10.1073/pnas.88.9.3720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Han T. H., Lamph W. W., Prywes R. Mapping of epidermal growth factor-, serum-, and phorbol ester-responsive sequence elements in the c-jun promoter. Mol Cell Biol. 1992 Oct;12(10):4472–4477. doi: 10.1128/mcb.12.10.4472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Herr I., van Dam H., Angel P. 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):1105–1113. doi: 10.1093/carcin/15.6.1105. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Hibi M., Lin A., Smeal T., Minden A., Karin M. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 1993 Nov;7(11):2135–2148. doi: 10.1101/gad.7.11.2135. [DOI] [PubMed] [Google Scholar]
  34. Hilberg F., Aguzzi A., Howells N., Wagner E. F. c-jun is essential for normal mouse development and hepatogenesis. Nature. 1993 Sep 9;365(6442):179–181. doi: 10.1038/365179a0. [DOI] [PubMed] [Google Scholar]
  35. Ivashkiv L. B., Fleming M. D., Glimcher L. H. Dominant negative mutants of transcription factor mXBP (CRE-BP1, ATF-2). New Biol. 1992 Apr;4(4):360–368. [PubMed] [Google Scholar]
  36. Ivashkiv L. B., Liou H. C., Kara C. J., Lamph W. W., Verma I. M., Glimcher L. H. mXBP/CRE-BP2 and c-Jun form a complex which binds to the cyclic AMP, but not to the 12-O-tetradecanoylphorbol-13-acetate, response element. Mol Cell Biol. 1990 Apr;10(4):1609–1621. doi: 10.1128/mcb.10.4.1609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Johnson R. S., van Lingen B., Papaioannou V. E., Spiegelman B. M. A null mutation at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev. 1993 Jul;7(7B):1309–1317. doi: 10.1101/gad.7.7b.1309. [DOI] [PubMed] [Google Scholar]
  38. Jonat C., Rahmsdorf H. J., Park K. K., Cato A. C., Gebel S., Ponta H., Herrlich P. Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell. 1990 Sep 21;62(6):1189–1204. doi: 10.1016/0092-8674(90)90395-u. [DOI] [PubMed] [Google Scholar]
  39. Kaina B., Fritz G., Mitra S., Coquerelle T. Transfection and expression of human O6-methylguanine-DNA methyltransferase (MGMT) cDNA in Chinese hamster cells: the role of MGMT in protection against the genotoxic effects of alkylating agents. Carcinogenesis. 1991 Oct;12(10):1857–1867. doi: 10.1093/carcin/12.10.1857. [DOI] [PubMed] [Google Scholar]
  40. Karin M., Smeal T. Control of transcription factors by signal transduction pathways: the beginning of the end. Trends Biochem Sci. 1992 Oct;17(10):418–422. doi: 10.1016/0968-0004(92)90012-x. [DOI] [PubMed] [Google Scholar]
  41. Kaszubska W., Hooft van Huijsduijnen R., Ghersa P., DeRaemy-Schenk A. M., Chen B. P., Hai T., DeLamarter J. F., Whelan J. Cyclic AMP-independent ATF family members interact with NF-kappa B and function in the activation of the E-selectin promoter in response to cytokines. Mol Cell Biol. 1993 Nov;13(11):7180–7190. doi: 10.1128/mcb.13.11.7180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kedar P. S., Widen S. G., Englander E. W., Fornace A. J., Jr, Wilson S. H. The ATF/CREB transcription factor-binding site in the polymerase beta promoter mediates the positive effect of N-methyl-N'-nitro-N-nitrosoguanidine on transcription. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3729–3733. doi: 10.1073/pnas.88.9.3729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Kyriakis J. M., Banerjee P., Nikolakaki E., Dai T., Rubie E. A., Ahmad M. F., Avruch J., Woodgett J. R. The stress-activated protein kinase subfamily of c-Jun kinases. Nature. 1994 May 12;369(6476):156–160. doi: 10.1038/369156a0. [DOI] [PubMed] [Google Scholar]
  44. Li L., Chambard J. C., Karin M., Olson E. N. Fos and Jun repress transcriptional activation by myogenin and MyoD: the amino terminus of Jun can mediate repression. Genes Dev. 1992 Apr;6(4):676–689. doi: 10.1101/gad.6.4.676. [DOI] [PubMed] [Google Scholar]
  45. Liu F., Green M. R. A specific member of the ATF transcription factor family can mediate transcription activation by the adenovirus E1a protein. Cell. 1990 Jun 29;61(7):1217–1224. doi: 10.1016/0092-8674(90)90686-9. [DOI] [PubMed] [Google Scholar]
  46. Livingstone C., Patel G., Jones N. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 1995 Apr 18;14(8):1785–1797. doi: 10.1002/j.1460-2075.1995.tb07167.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  49. Minden A., Lin A., Smeal T., Dérijard B., Cobb M., Davis R., Karin M. 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):6683–6688. doi: 10.1128/mcb.14.10.6683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Muegge K., Vila M., Gusella G. L., Musso T., Herrlich P., Stein B., Durum S. K. Interleukin 1 induction of the c-jun promoter. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7054–7058. doi: 10.1073/pnas.90.15.7054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Mueller P. R., Wold B. In vivo footprinting of a muscle specific enhancer by ligation mediated PCR. Science. 1989 Nov 10;246(4931):780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
  52. Nomura N., Zu Y. L., Maekawa T., Tabata S., Akiyama T., Ishii S. Isolation and characterization of a novel member of the gene family encoding the cAMP response element-binding protein CRE-BP1. J Biol Chem. 1993 Feb 25;268(6):4259–4266. [PubMed] [Google Scholar]
  53. Patel G., Nasmyth K., Jones N. A new method for the isolation of recombinant baculovirus. Nucleic Acids Res. 1992 Jan 11;20(1):97–104. doi: 10.1093/nar/20.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Pulverer B. J., Hughes K., Franklin C. C., Kraft A. S., Leevers S. J., Woodgett J. R. Co-purification of mitogen-activated protein kinases with phorbol ester-induced c-Jun kinase activity in U937 leukaemic cells. Oncogene. 1993 Feb;8(2):407–415. [PubMed] [Google Scholar]
  55. Pulverer B. J., Kyriakis J. M., Avruch J., Nikolakaki E., Woodgett J. R. Phosphorylation of c-jun mediated by MAP kinases. Nature. 1991 Oct 17;353(6345):670–674. doi: 10.1038/353670a0. [DOI] [PubMed] [Google Scholar]
  56. Radler-Pohl A., Sachsenmaier C., Gebel S., Auer H. P., Bruder J. T., Rapp U., Angel P., Rahmsdorf H. J., Herrlich P. UV-induced activation of AP-1 involves obligatory extranuclear steps including Raf-1 kinase. EMBO J. 1993 Mar;12(3):1005–1012. doi: 10.1002/j.1460-2075.1993.tb05741.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Rozek D., Pfeifer G. P. In vivo protein-DNA interactions at the c-jun promoter: preformed complexes mediate the UV response. Mol Cell Biol. 1993 Sep;13(9):5490–5499. doi: 10.1128/mcb.13.9.5490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sachsenmaier C., Radler-Pohl A., Zinck R., Nordheim A., Herrlich P., Rahmsdorf H. J. Involvement of growth factor receptors in the mammalian UVC response. Cell. 1994 Sep 23;78(6):963–972. doi: 10.1016/0092-8674(94)90272-0. [DOI] [PubMed] [Google Scholar]
  59. Sadowski I., Ma J., Triezenberg S., Ptashne M. GAL4-VP16 is an unusually potent transcriptional activator. Nature. 1988 Oct 6;335(6190):563–564. doi: 10.1038/335563a0. [DOI] [PubMed] [Google Scholar]
  60. Schmitz M. L., Baeuerle P. A. The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B. EMBO J. 1991 Dec;10(12):3805–3817. doi: 10.1002/j.1460-2075.1991.tb04950.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Schüle R., Rangarajan P., Kliewer S., Ransone L. J., Bolado J., Yang N., Verma I. M., Evans R. M. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor. Cell. 1990 Sep 21;62(6):1217–1226. doi: 10.1016/0092-8674(90)90397-w. [DOI] [PubMed] [Google Scholar]
  62. Sherman M. L., Datta R., Hallahan D. E., Weichselbaum R. R., Kufe D. W. Ionizing radiation regulates expression of the c-jun protooncogene. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5663–5666. doi: 10.1073/pnas.87.15.5663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  64. Stein B., Angel P., van Dam H., Ponta H., Herrlich P., van der Eb A., Rahmsdorf H. J. Ultraviolet-radiation induced c-jun gene transcription: two AP-1 like binding sites mediate the response. Photochem Photobiol. 1992 Mar;55(3):409–415. doi: 10.1111/j.1751-1097.1992.tb04255.x. [DOI] [PubMed] [Google Scholar]
  65. Stein B., Baldwin A. S., Jr, Ballard D. W., Greene W. C., Angel P., Herrlich P. Cross-coupling of the NF-kappa B p65 and Fos/Jun transcription factors produces potentiated biological function. EMBO J. 1993 Oct;12(10):3879–3891. doi: 10.1002/j.1460-2075.1993.tb06066.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Vogt P. K., Bos T. J. jun: oncogene and transcription factor. Adv Cancer Res. 1990;55:1–35. doi: 10.1016/s0065-230x(08)60466-2. [DOI] [PubMed] [Google Scholar]
  67. Webster N., Jin J. R., Green S., Hollis M., Chambon P. The yeast UASG is a transcriptional enhancer in human HeLa cells in the presence of the GAL4 trans-activator. Cell. 1988 Jan 29;52(2):169–178. doi: 10.1016/0092-8674(88)90505-3. [DOI] [PubMed] [Google Scholar]
  68. White E., Cipriani R., Sabbatini P., Denton A. Adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of E1A proteins. J Virol. 1991 Jun;65(6):2968–2978. doi: 10.1128/jvi.65.6.2968-2978.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Yamaguchi M., Hayashi Y., Hirose F., Shiroki K., Matsukage A. Activation of the mouse DNA polymerase beta gene promoter by adenovirus type 12 E1A proteins. Nucleic Acids Res. 1992 May 11;20(9):2321–2325. doi: 10.1093/nar/20.9.2321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Yang-Yen H. F., Chambard J. C., Sun Y. L., Smeal T., Schmidt T. J., Drouin J., Karin M. Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell. 1990 Sep 21;62(6):1205–1215. doi: 10.1016/0092-8674(90)90396-v. [DOI] [PubMed] [Google Scholar]
  71. Yang-Yen H. F., Chiu R., Karin M. Elevation of AP1 activity during F9 cell differentiation is due to increased c-jun transcription. New Biol. 1990 Apr;2(4):351–361. [PubMed] [Google Scholar]
  72. van Dam H., Duyndam M., Rottier R., Bosch A., de Vries-Smits L., Herrlich P., Zantema A., Angel P., van der Eb A. J. 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):479–487. doi: 10.1002/j.1460-2075.1993.tb05680.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. van Dam H., Offringa R., Meijer I., Stein B., Smits A. M., Herrlich P., Bos J. L., van der Eb A. J. Differential effects of the adenovirus E1A oncogene on members of the AP-1 transcription factor family. Mol Cell Biol. 1990 Nov;10(11):5857–5864. doi: 10.1128/mcb.10.11.5857. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES