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. 1994 Jun;14(6):4258–4268. doi: 10.1128/mcb.14.6.4258

TATA-dependent enhancer stimulation of promoter activity in mice is developmentally acquired.

S Majumder 1, M L DePamphilis 1
PMCID: PMC358792  PMID: 8196662

Abstract

Herpes simplex virus (HSV) thymidine kinase (tk) promoter activity depends on four transcription factor binding sites, one of which is a TATA box sequence, and the presence of either a cis-acting enhancer sequence or a transactivator protein. Studies presented here show that this TATA box was required for promoter activity only after cells began to differentiate and then only when promoter activity was stimulated by either an enhancer or a transactivator. When the HSV tk promoter was utilized by mouse embryos from the one-cell to eight-cell stage of development or by undifferentiated mouse embryonic stem cells, disruption of the HSV tk TATA box by site-specific mutations did not reduce promoter activity. This was true even when HSV tk promoter activity was stimulated strongly by either the embryo-responsive polyomavirus F101 enhancer or its natural transactivator, the HSV ICP4 gene product. However, stimulated expression was dependent on a distal Sp1 DNA binding site. Similarly, disruption of the TATA box did not reduce tk promoter activity in primary mouse embryonic fibroblasts or in immortalized 3T3 mouse fibroblasts; in fact, promoter activity was increased up to 2.6-fold. However, in these differentiated cells, stimulation of the HSV tk promoter by either the F101 enhancer or ICP4 protein required the TATA box. HSV tk promoter activity also was dependent on its TATA box in the mouse oocyte, a terminally differentiated cell with an endogenous transactivating activity. These results reveal that the need for a TATA box is developmentally acquired and depends on at least two parameters: the differentiated state of the cell and stimulation of the promoter by either an enhancer or a transactivator.

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Selected References

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

  1. Abbondanzo S. J., Gadi I., Stewart C. L. Derivation of embryonic stem cell lines. Methods Enzymol. 1993;225:803–823. doi: 10.1016/0076-6879(93)25052-4. [DOI] [PubMed] [Google Scholar]
  2. Banerji J., Rusconi S., Schaffner W. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell. 1981 Dec;27(2 Pt 1):299–308. doi: 10.1016/0092-8674(81)90413-x. [DOI] [PubMed] [Google Scholar]
  3. Bird A. P. CpG-rich islands and the function of DNA methylation. Nature. 1986 May 15;321(6067):209–213. doi: 10.1038/321209a0. [DOI] [PubMed] [Google Scholar]
  4. Blake M. C., Jambou R. C., Swick A. G., Kahn J. W., Azizkhan J. C. Transcriptional initiation is controlled by upstream GC-box interactions in a TATAA-less promoter. Mol Cell Biol. 1990 Dec;10(12):6632–6641. doi: 10.1128/mcb.10.12.6632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blatt C., DePamphilis M. L. Striking homology between mouse and human transcription enhancer factor-1 (TEF-1). Nucleic Acids Res. 1993 Feb 11;21(3):747–748. doi: 10.1093/nar/21.3.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boyer T. G., Berk A. J. Functional interaction of adenovirus E1A with holo-TFIID. Genes Dev. 1993 Sep;7(9):1810–1823. doi: 10.1101/gad.7.9.1810. [DOI] [PubMed] [Google Scholar]
  7. Böni J., Coen D. M. Examination of the roles of transcription factor Sp1-binding sites and an octamer motif in trans induction of the herpes simplex virus thymidine kinase gene. J Virol. 1989 Sep;63(9):4088–4092. doi: 10.1128/jvi.63.9.4088-4092.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carcamo J., Lobos S., Merino A., Buckbinder L., Weinmann R., Natarajan V., Reinberg D. Factors involved in specific transcription by mammalian RNA polymerase II. Role of factors IID and MLTF in transcription from the adenovirus major late and IVa2 promoters. J Biol Chem. 1989 May 5;264(13):7704–7714. [PubMed] [Google Scholar]
  9. Chalifour L. E., Wirak D. O., Hansen U., Wassarman P. M., DePamphilis M. L. cis- and trans-acting sequences required for expression of simian virus 40 genes in mouse oocytes. Genes Dev. 1987 Dec;1(10):1096–1106. doi: 10.1101/gad.1.10.1096. [DOI] [PubMed] [Google Scholar]
  10. Chalifour L. E., Wirak D. O., Wassarman P. M., DePamphilis M. L. Expression of simian virus 40 early and late genes in mouse oocytes and embryos. J Virol. 1986 Sep;59(3):619–627. doi: 10.1128/jvi.59.3.619-627.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chung Y. T., Keller E. B. The TATA-dependent and TATA-independent promoters of the Drosophila melanogaster actin 5C-encoding gene. Gene. 1991 Oct 15;106(2):237–241. doi: 10.1016/0378-1119(91)90204-o. [DOI] [PubMed] [Google Scholar]
  12. Coen D. M., Weinheimer S. P., McKnight S. L. A genetic approach to promoter recognition during trans induction of viral gene expression. Science. 1986 Oct 3;234(4772):53–59. doi: 10.1126/science.3018926. [DOI] [PubMed] [Google Scholar]
  13. Dooley T. P., Miranda M., Jones N. C., DePamphilis M. L. Transactivation of the adenovirus EIIa promoter in the absence of adenovirus E1A protein is restricted to mouse oocytes and preimplantation embryos. Development. 1989 Dec;107(4):945–956. doi: 10.1242/dev.107.4.945. [DOI] [PubMed] [Google Scholar]
  14. Drapkin R., Merino A., Reinberg D. Regulation of RNA polymerase II transcription. Curr Opin Cell Biol. 1993 Jun;5(3):469–476. doi: 10.1016/0955-0674(93)90013-g. [DOI] [PubMed] [Google Scholar]
  15. Eisenberg S. P., Coen D. M., McKnight S. L. Promoter domains required for expression of plasmid-borne copies of the herpes simplex virus thymidine kinase gene in virus-infected mouse fibroblasts and microinjected frog oocytes. Mol Cell Biol. 1985 Aug;5(8):1940–1947. doi: 10.1128/mcb.5.8.1940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. ElKareh A., Murphy A. J., Fichter T., Efstratiadis A., Silverstein S. "Transactivation" control signals in the promoter of the herpesvirus thymidine kinase gene. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1002–1006. doi: 10.1073/pnas.82.4.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Everett R. D. Trans activation of transcription by herpes virus products: requirement for two HSV-1 immediate-early polypeptides for maximum activity. EMBO J. 1984 Dec 20;3(13):3135–3141. doi: 10.1002/j.1460-2075.1984.tb02270.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Garrity P. A., Wold B. J. Tissue-specific expression from a compound TATA-dependent and TATA-independent promoter. Mol Cell Biol. 1990 Nov;10(11):5646–5654. doi: 10.1128/mcb.10.11.5646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gelman I. H., Silverstein S. Identification of immediate early genes from herpes simplex virus that transactivate the virus thymidine kinase gene. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5265–5269. doi: 10.1073/pnas.82.16.5265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Greene J. M., Kingston R. E. TATA-dependent and TATA-independent function of the basal and heat shock elements of a human hsp70 promoter. Mol Cell Biol. 1990 Apr;10(4):1319–1328. doi: 10.1128/mcb.10.4.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hahn S., Buratowski S., Sharp P. A., Guarente L. Yeast TATA-binding protein TFIID binds to TATA elements with both consensus and nonconsensus DNA sequences. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5718–5722. doi: 10.1073/pnas.86.15.5718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Homa F. L., Glorioso J. C., Levine M. A specific 15-bp TATA box promoter element is required for expression of a herpes simplex virus type 1 late gene. Genes Dev. 1988 Jan;2(1):40–53. doi: 10.1101/gad.2.1.40. [DOI] [PubMed] [Google Scholar]
  23. Imbalzano A. N., Coen D. M., DeLuca N. A. Herpes simplex virus transactivator ICP4 operationally substitutes for the cellular transcription factor Sp1 for efficient expression of the viral thymidine kinase gene. J Virol. 1991 Feb;65(2):565–574. doi: 10.1128/jvi.65.2.565-574.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jones K. A., Yamamoto K. R., Tjian R. Two distinct transcription factors bind to the HSV thymidine kinase promoter in vitro. Cell. 1985 Sep;42(2):559–572. doi: 10.1016/0092-8674(85)90113-8. [DOI] [PubMed] [Google Scholar]
  25. Majumder S., DePamphilis M. L. Requirements for DNA transcription and replication at the beginning of mouse development. J Cell Biochem. 1994 May;55(1):59–68. doi: 10.1002/jcb.240550107. [DOI] [PubMed] [Google Scholar]
  26. Majumder S., Miranda M., DePamphilis M. L. Analysis of gene expression in mouse preimplantation embryos demonstrates that the primary role of enhancers is to relieve repression of promoters. EMBO J. 1993 Mar;12(3):1131–1140. doi: 10.1002/j.1460-2075.1993.tb05754.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Martínez-Salas E., Cupo D. Y., DePamphilis M. L. The need for enhancers is acquired upon formation of a diploid nucleus during early mouse development. Genes Dev. 1988 Sep;2(9):1115–1126. doi: 10.1101/gad.2.9.1115. [DOI] [PubMed] [Google Scholar]
  28. Martínez-Salas E., Linney E., Hassell J., DePamphilis M. L. The need for enhancers in gene expression first appears during mouse development with formation of the zygotic nucleus. Genes Dev. 1989 Oct;3(10):1493–1506. doi: 10.1101/gad.3.10.1493. [DOI] [PubMed] [Google Scholar]
  29. McKnight S. L., Gavis E. R., Kingsbury R., Axel R. Analysis of transcriptional regulatory signals of the HSV thymidine kinase gene: identification of an upstream control region. Cell. 1981 Aug;25(2):385–398. doi: 10.1016/0092-8674(81)90057-x. [DOI] [PubMed] [Google Scholar]
  30. McKnight S. L., Kingsbury R. C., Spence A., Smith M. The distal transcription signals of the herpesvirus tk gene share a common hexanucleotide control sequence. Cell. 1984 May;37(1):253–262. doi: 10.1016/0092-8674(84)90321-0. [DOI] [PubMed] [Google Scholar]
  31. McKnight S. L., Kingsbury R. Transcriptional control signals of a eukaryotic protein-coding gene. Science. 1982 Jul 23;217(4557):316–324. doi: 10.1126/science.6283634. [DOI] [PubMed] [Google Scholar]
  32. Miranda M., Majumder S., Wiekowski M., DePamphilis M. L. Application of firefly luciferase to preimplantation development. Methods Enzymol. 1993;225:412–433. doi: 10.1016/0076-6879(93)25029-2. [DOI] [PubMed] [Google Scholar]
  33. Mitchell P. J., Tjian R. Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins. Science. 1989 Jul 28;245(4916):371–378. doi: 10.1126/science.2667136. [DOI] [PubMed] [Google Scholar]
  34. Myers R. M., Tilly K., Maniatis T. Fine structure genetic analysis of a beta-globin promoter. Science. 1986 May 2;232(4750):613–618. doi: 10.1126/science.3457470. [DOI] [PubMed] [Google Scholar]
  35. Mélin F., Miranda M., Montreau N., DePamphilis M. L., Blangy D. Transcription enhancer factor-1 (TEF-1) DNA binding sites can specifically enhance gene expression at the beginning of mouse development. EMBO J. 1993 Dec;12(12):4657–4666. doi: 10.1002/j.1460-2075.1993.tb06154.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Olsen H. S., Rosen C. A. Contribution of the TATA motif to Tat-mediated transcriptional activation of human immunodeficiency virus gene expression. J Virol. 1992 Sep;66(9):5594–5597. doi: 10.1128/jvi.66.9.5594-5597.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pellman D., McLaughlin M. E., Fink G. R. TATA-dependent and TATA-independent transcription at the HIS4 gene of yeast. Nature. 1990 Nov 1;348(6296):82–85. doi: 10.1038/348082a0. [DOI] [PubMed] [Google Scholar]
  38. Resnick J., Boyd B. A., Haffey M. L. DNA binding by the herpes simplex virus type 1 ICP4 protein is necessary for efficient down regulation of the ICP0 promoter. J Virol. 1989 Jun;63(6):2497–2503. doi: 10.1128/jvi.63.6.2497-2503.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rigby P. W. Three in one and one in three: it all depends on TBP. Cell. 1993 Jan 15;72(1):7–10. doi: 10.1016/0092-8674(93)90042-o. [DOI] [PubMed] [Google Scholar]
  40. Sacks W. R., Schaffer P. A. Deletion mutants in the gene encoding the herpes simplex virus type 1 immediate-early protein ICP0 exhibit impaired growth in cell culture. J Virol. 1987 Mar;61(3):829–839. doi: 10.1128/jvi.61.3.829-839.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Simon M. C., Fisch T. M., Benecke B. J., Nevins J. R., Heintz N. Definition of multiple, functionally distinct TATA elements, one of which is a target in the hsp70 promoter for E1A regulation. Cell. 1988 Mar 11;52(5):723–729. doi: 10.1016/0092-8674(88)90410-2. [DOI] [PubMed] [Google Scholar]
  42. Simon M. C., Rooney R. J., Fisch T. M., Heintz N., Nevins J. R. E1A-dependent trans-activation of the c-fos promoter requires the TATAA sequence. Proc Natl Acad Sci U S A. 1990 Jan;87(2):513–517. doi: 10.1073/pnas.87.2.513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stow N. D., Stow E. C. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J Gen Virol. 1986 Dec;67(Pt 12):2571–2585. doi: 10.1099/0022-1317-67-12-2571. [DOI] [PubMed] [Google Scholar]
  44. Ustav M., Ustav E., Szymanski P., Stenlund A. Identification of the origin of replication of bovine papillomavirus and characterization of the viral origin recognition factor E1. EMBO J. 1991 Dec;10(13):4321–4329. doi: 10.1002/j.1460-2075.1991.tb05010.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang W. D., Gralla J. D. Differential ability of proximal and remote element pairs to cooperate in activating RNA polymerase II transcription. Mol Cell Biol. 1991 Sep;11(9):4561–4571. doi: 10.1128/mcb.11.9.4561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wasylyk B. Enhancers and transcription factors in the control of gene expression. Biochim Biophys Acta. 1988 Nov 10;951(1):17–35. doi: 10.1016/0167-4781(88)90021-8. [DOI] [PubMed] [Google Scholar]
  47. Wefald F. C., Devlin B. H., Williams R. S. Functional heterogeneity of mammalian TATA-box sequences revealed by interaction with a cell-specific enhancer. Nature. 1990 Mar 15;344(6263):260–262. doi: 10.1038/344260a0. [DOI] [PubMed] [Google Scholar]
  48. Wiekowski M., Miranda M., DePamphilis M. L. Regulation of gene expression in preimplantation mouse embryos: effects of the zygotic clock and the first mitosis on promoter and enhancer activities. Dev Biol. 1991 Oct;147(2):403–414. doi: 10.1016/0012-1606(91)90298-h. [DOI] [PubMed] [Google Scholar]
  49. Wiekowski M., Miranda M., DePamphilis M. L. Requirements for promoter activity in mouse oocytes and embryos distinguish paternal pronuclei from maternal and zygotic nuclei. Dev Biol. 1993 Sep;159(1):366–378. doi: 10.1006/dbio.1993.1248. [DOI] [PubMed] [Google Scholar]
  50. Xu L. C., Thali M., Schaffner W. Upstream box/TATA box order is the major determinant of the direction of transcription. Nucleic Acids Res. 1991 Dec 25;19(24):6699–6704. doi: 10.1093/nar/19.24.6699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yang L., Mohr I., Li R., Nottoli T., Sun S., Botchan M. Transcription factor E2 regulates BPV-1 DNA replication in vitro by direct protein-protein interaction. Cold Spring Harb Symp Quant Biol. 1991;56:335–346. doi: 10.1101/sqb.1991.056.01.040. [DOI] [PubMed] [Google Scholar]

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