Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1991 Dec;19(25):7117–7123. doi: 10.1093/nar/19.25.7117

SV40 activates transcription from the transferrin receptor promoter by inducing a factor which binds to the CRE/AP-1 recognition sequence.

P Beard 1, E Offord 1, N Paduwat 1, H Bruggmann 1
PMCID: PMC332531  PMID: 1662807

Abstract

During the course of lytic infection by simian virus 40 (SV40), expression of both the viral late genes and certain host cellular genes is induced. The promoter of the cellular transferrin receptor (TR) gene contains a DNA sequence which is similar to the AP-1- and AP-4-binding region in SV40 which has been implicated in the control of the viral late promoter. Expression of TR is needed for cells to enter S-phase and is therefore expected to be important for the SV40 lytic cycle. Here we show that the level of TR mRNA in vivo was increased by SV40 infection. A factor which activates transcription from the TR promoter in vitro was specifically induced in SV40-infected cells. Gel mobility shift assays with an oligonucleotide comprising this part of the TR promoter showed three nucleoprotein complexes to be formed with proteins from CV-1 cells. Following SV40 infection, one of the complexes was increased ten-fold. Formation of this complex was specifically reduced by competition with the phorbol ester-responsive element of the collagenase gene, implying that the factor is a member of the AP-1/Jun/Fos family. Cross-linking of the complex by ultraviolet light showed major DNA-binding components to be proteins of about 55 kD and 47 kD. Removal of this factor by adding the oligonucleotide to in vitro transcription reactions with the TR promoter, abolished the activation of TR transcription. The factor which binds to the TR promoter co-sedimented with SV40 chromosomes extracted late in infection. This suggests that similar transcriptional regulatory proteins are involved in controlling transcription from both the SV40 and the TR promoters, and that the virus can use a common mechanism to induce viral and host cellular transcription.

Full text

PDF

Images in this article

7118Image
on p.7118
7119Image
on p.7119
7119Image
on p.7119
7119Image
on p.7119
7120Image
on p.7120
7120Image
on p.7120
7120Image
on p.7120
7121Image
on p.7121

Selected References

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

  1. Angel P., Baumann I., Stein B., Delius H., Rahmsdorf H. J., Herrlich P. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5'-flanking region. Mol Cell Biol. 1987 Jun;7(6):2256–2266. doi: 10.1128/mcb.7.6.2256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Beard P., Bruggmann H. A transcription factor from simian virus 40 chromosomes which activates the viral late promoter in vitro. J Virol. 1988 Nov;62(11):4296–4302. doi: 10.1128/jvi.62.11.4296-4302.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beard P., Bruggmann H. Control of transcription in vitro from simian virus 40 promoters by proteins from viral minichromosomes. Curr Top Microbiol Immunol. 1989;144:47–54. doi: 10.1007/978-3-642-74578-2_6. [DOI] [PubMed] [Google Scholar]
  5. Ben-Hattar J., Beard P., Jiricny J. Cytosine methylation in CTF and Sp1 recognition sites of an HSV tk promoter: effects on transcription in vivo and on factor binding in vitro. Nucleic Acids Res. 1989 Dec 25;17(24):10179–10190. doi: 10.1093/nar/17.24.10179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casey J. L., Di Jeso B., Rao K. K., Rouault T. A., Klausner R. D., Harford J. B. Deletional analysis of the promoter region of the human transferrin receptor gene. Nucleic Acids Res. 1988 Jan 25;16(2):629–646. doi: 10.1093/nar/16.2.629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cockell M., Stevenson B. J., Strubin M., Hagenbüchle O., Wellauer P. K. Identification of a cell-specific DNA-binding activity that interacts with a transcriptional activator of genes expressed in the acinar pancreas. Mol Cell Biol. 1989 Jun;9(6):2464–2476. doi: 10.1128/mcb.9.6.2464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Gruda M. C., Alwine J. C. Simian virus 40 (SV40) T-antigen transcriptional activation mediated through the Oct/SPH region of the SV40 late promoter. J Virol. 1991 Jul;65(7):3553–3558. doi: 10.1128/jvi.65.7.3553-3558.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hai T. W., Liu F., Allegretto E. A., Karin M., Green M. R. A family of immunologically related transcription factors that includes multiple forms of ATF and AP-1. Genes Dev. 1988 Oct;2(10):1216–1226. doi: 10.1101/gad.2.10.1216. [DOI] [PubMed] [Google Scholar]
  11. Hirai S., Yaniv M. Jun DNA-binding is modulated by mutations between the leucines or by direct interaction of fos with the TGACTCA sequence. New Biol. 1989 Nov;1(2):181–191. [PubMed] [Google Scholar]
  12. Hu Y. F., Lüscher B., Admon A., Mermod N., Tjian R. Transcription factor AP-4 contains multiple dimerization domains that regulate dimer specificity. Genes Dev. 1990 Oct;4(10):1741–1752. doi: 10.1101/gad.4.10.1741. [DOI] [PubMed] [Google Scholar]
  13. Huang H. C., Sundseth R., Hansen U. Transcription factor LSF binds two variant bipartite sites within the SV40 late promoter. Genes Dev. 1990 Feb;4(2):287–298. doi: 10.1101/gad.4.2.287. [DOI] [PubMed] [Google Scholar]
  14. Hurst H. C., Masson N., Jones N. C., Lee K. A. The cellular transcription factor CREB corresponds to activating transcription factor 47 (ATF-47) and forms complexes with a group of polypeptides related to ATF-43. Mol Cell Biol. 1990 Dec;10(12):6192–6203. doi: 10.1128/mcb.10.12.6192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lee W., Mitchell P., Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell. 1987 Jun 19;49(6):741–752. doi: 10.1016/0092-8674(87)90612-x. [DOI] [PubMed] [Google Scholar]
  16. Lesley J. F., Schulte R. J. Inhibition of cell growth by monoclonal anti-transferrin receptor antibodies. Mol Cell Biol. 1985 Aug;5(8):1814–1821. doi: 10.1128/mcb.5.8.1814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. May E., Omilli F., Ernoult-Lange M., Zenke M., Chambon P. The sequence motifs that are involved in SV40 enhancer function also control SV40 late promoter activity. Nucleic Acids Res. 1987 Mar 25;15(6):2445–2461. doi: 10.1093/nar/15.6.2445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mermod N., Williams T. J., Tjian R. Enhancer binding factors AP-4 and AP-1 act in concert to activate SV40 late transcription in vitro. Nature. 1988 Apr 7;332(6164):557–561. doi: 10.1038/332557a0. [DOI] [PubMed] [Google Scholar]
  19. Müllner E. W., Neupert B., Kühn L. C. A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell. 1989 Jul 28;58(2):373–382. doi: 10.1016/0092-8674(89)90851-9. [DOI] [PubMed] [Google Scholar]
  20. Oda K., Dulbecco R. Induction of cellular mRNA synthesis in BSC-1 cells infected by SV40. Virology. 1968 Jul;35(3):439–444. doi: 10.1016/0042-6822(68)90222-5. [DOI] [PubMed] [Google Scholar]
  21. Offord E. A., Beard P. A member of the activator protein 1 family found in keratinocytes but not in fibroblasts required for transcription from a human papillomavirus type 18 promoter. J Virol. 1990 Oct;64(10):4792–4798. doi: 10.1128/jvi.64.10.4792-4798.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Owen D., Kühn L. C. Noncoding 3' sequences of the transferrin receptor gene are required for mRNA regulation by iron. EMBO J. 1987 May;6(5):1287–1293. doi: 10.1002/j.1460-2075.1987.tb02366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Roberts M. R., Miskimins W. K., Ruddle F. H. Nuclear proteins TREF1 and TREF2 bind to the transcriptional control element of the transferrin receptor gene and appear to be associated as a heterodimer. Cell Regul. 1989 Nov;1(1):151–164. doi: 10.1091/mbc.1.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Saffer J. D., Jackson S. P., Thurston S. J. SV40 stimulates expression of the transacting factor Sp1 at the mRNA level. Genes Dev. 1990 Apr;4(4):659–666. doi: 10.1101/gad.4.4.659. [DOI] [PubMed] [Google Scholar]
  25. Schutzbank T., Robinson R., Oren M., Levine A. J. SV40 large tumor antigen can regulate some cellular transcripts in a positive fashion. Cell. 1982 Sep;30(2):481–490. doi: 10.1016/0092-8674(82)90245-8. [DOI] [PubMed] [Google Scholar]
  26. Stewart C. J., Ito M., Conrad S. E. Evidence for transcriptional and post-transcriptional control of the cellular thymidine kinase gene. Mol Cell Biol. 1987 Mar;7(3):1156–1163. doi: 10.1128/mcb.7.3.1156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tack L. C., Beard P. Both trans-acting factors and chromatin structure are involved in the regulation of transcription from the early and late promoters in simian virus 40 chromosomes. J Virol. 1985 Apr;54(1):207–218. doi: 10.1128/jvi.54.1.207-218.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Trowbridge I. S., Lopez F. Monoclonal antibody to transferrin receptor blocks transferrin binding and inhibits human tumor cell growth in vitro. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1175–1179. doi: 10.1073/pnas.79.4.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Xiao J. H., Davidson I., Matthes H., Garnier J. M., Chambon P. Cloning, expression, and transcriptional properties of the human enhancer factor TEF-1. Cell. 1991 May 17;65(4):551–568. doi: 10.1016/0092-8674(91)90088-g. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES