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. 1990 Oct;9(10):3101–3108. doi: 10.1002/j.1460-2075.1990.tb07507.x

Core promoter of the mouse myelin basic protein gene governs brain-specific transcription in vitro.

T Tamura 1, K Sumita 1, S Hirose 1, K Mikoshiba 1
PMCID: PMC552037  PMID: 1698607

Abstract

The core promoter of the mouse myelin basic protein (MBP) gene from -36 to +12 was preferentially transcribed in brain nuclear extracts. Both the TATA at -34 and downstream elements to +12 were required for efficient, accurate and brain-specific transcription. From brain and liver nuclear extracts, we have partially purified the general transcription factor TFIID. The partially purified fractions contained TATA element binding factors of the MBP promoter as well as adenovirus major late promoter (MLP). The tissue-derived TFIID was functionally exchangeable for the HeLa TFIID, and directed transcription from the MLP. Surprisingly, the brain TFIID activated transcription from the MBP core promoter while the liver TFIID did to a much lesser extent. Exchange of the TATA-containing short DNA stretch to the MBP core promoter for a corresponding region of the mouse albumin promoter or MLP abolished the brain specificity. We found that several tissue-specific promoters other than MBP, such as mouse neurofilament and human alpha-1-antitrypsin promoters were also transcribed much more efficiently by the brain and liver TFIID, respectively. We suggest that different tissues contain functionally non-equivalent TFIID or TFIID-like activities.

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  1. Aoyama A., Tamura T. A., Mikoshiba K. Regulation of brain-specific transcription of the mouse myelin basic protein gene: function of the NFI-binding site in the distal promoter. Biochem Biophys Res Commun. 1990 Mar 16;167(2):648–653. doi: 10.1016/0006-291x(90)92074-a. [DOI] [PubMed] [Google Scholar]
  2. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Buratowski S., Hahn S., Sharp P. A., Guarente L. Function of a yeast TATA element-binding protein in a mammalian transcription system. Nature. 1988 Jul 7;334(6177):37–42. doi: 10.1038/334037a0. [DOI] [PubMed] [Google Scholar]
  5. Cavallini B., Faus I., Matthes H., Chipoulet J. M., Winsor B., Egly J. M., Chambon P. Cloning of the gene encoding the yeast protein BTF1Y, which can substitute for the human TATA box-binding factor. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9803–9807. doi: 10.1073/pnas.86.24.9803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cavallini B., Huet J., Plassat J. L., Sentenac A., Egly J. M., Chambon P. A yeast activity can substitute for the HeLa cell TATA box factor. Nature. 1988 Jul 7;334(6177):77–80. doi: 10.1038/334077a0. [DOI] [PubMed] [Google Scholar]
  7. Chater K. F., Bruton C. J., Plaskitt K. A., Buttner M. J., Méndez C., Helmann J. D. The developmental fate of S. coelicolor hyphae depends upon a gene product homologous with the motility sigma factor of B. subtilis. Cell. 1989 Oct 6;59(1):133–143. doi: 10.1016/0092-8674(89)90876-3. [DOI] [PubMed] [Google Scholar]
  8. Chen W., Struhl K. Saturation mutagenesis of a yeast his3 "TATA element": genetic evidence for a specific TATA-binding protein. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2691–2695. doi: 10.1073/pnas.85.8.2691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Concino M. F., Lee R. F., Merryweather J. P., Weinmann R. The adenovirus major late promoter TATA box and initiation site are both necessary for transcription in vitro. Nucleic Acids Res. 1984 Oct 11;12(19):7423–7433. doi: 10.1093/nar/12.19.7423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Corden J., Wasylyk B., Buchwalder A., Sassone-Corsi P., Kedinger C., Chambon P. Promoter sequences of eukaryotic protein-coding genes. Science. 1980 Sep 19;209(4463):1406–1414. doi: 10.1126/science.6251548. [DOI] [PubMed] [Google Scholar]
  11. Davison B. L., Egly J. M., Mulvihill E. R., Chambon P. Formation of stable preinitiation complexes between eukaryotic class B transcription factors and promoter sequences. Nature. 1983 Feb 24;301(5902):680–686. doi: 10.1038/301680a0. [DOI] [PubMed] [Google Scholar]
  12. Dierich A., Gaub M. P., LePennec J. P., Astinotti D., Chambon P. Cell-specificity of the chicken ovalbumin and conalbumin promoters. EMBO J. 1987 Aug;6(8):2305–2312. doi: 10.1002/j.1460-2075.1987.tb02505.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dierks P., van Ooyen A., Cochran M. D., Dobkin C., Reiser J., Weissmann C. Three regions upstream from the cap site are required for efficient and accurate transcription of the rabbit beta-globin gene in mouse 3T6 cells. Cell. 1983 Mar;32(3):695–706. doi: 10.1016/0092-8674(83)90055-7. [DOI] [PubMed] [Google Scholar]
  14. Dignam J. D., Martin P. L., Shastry B. S., Roeder R. G. Eukaryotic gene transcription with purified components. Methods Enzymol. 1983;101:582–598. doi: 10.1016/0076-6879(83)01039-3. [DOI] [PubMed] [Google Scholar]
  15. Dynan W. S., Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. 1985 Aug 29-Sep 4Nature. 316(6031):774–778. doi: 10.1038/316774a0. [DOI] [PubMed] [Google Scholar]
  16. Fire A., Samuels M., Sharp P. A. Interactions between RNA polymerase II, factors, and template leading to accurate transcription. J Biol Chem. 1984 Feb 25;259(4):2509–2516. [PubMed] [Google Scholar]
  17. Giangrande A., Mettling C., Martin M., Ruiz C., Richards G. Drosophila Sgs3 TATA: effects of point mutations on expression in vivo and protein binding in vitro with staged nuclear extracts. EMBO J. 1989 Nov;8(11):3459–3466. doi: 10.1002/j.1460-2075.1989.tb08510.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gorski K., Carneiro M., Schibler U. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell. 1986 Dec 5;47(5):767–776. doi: 10.1016/0092-8674(86)90519-2. [DOI] [PubMed] [Google Scholar]
  19. Hahn S., Buratowski S., Sharp P. A., Guarente L. Isolation of the gene encoding the yeast TATA binding protein TFIID: a gene identical to the SPT15 suppressor of Ty element insertions. Cell. 1989 Sep 22;58(6):1173–1181. doi: 10.1016/0092-8674(89)90515-1. [DOI] [PubMed] [Google Scholar]
  20. Hahn S., Hoar E. T., Guarente L. Each of three "TATA elements" specifies a subset of the transcription initiation sites at the CYC-1 promoter of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8562–8566. doi: 10.1073/pnas.82.24.8562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hawley D. K., Roeder R. G. Separation and partial characterization of three functional steps in transcription initiation by human RNA polymerase II. J Biol Chem. 1985 Jul 5;260(13):8163–8172. [PubMed] [Google Scholar]
  22. Helmann J. D., Chamberlin M. J. Structure and function of bacterial sigma factors. Annu Rev Biochem. 1988;57:839–872. doi: 10.1146/annurev.bi.57.070188.004203. [DOI] [PubMed] [Google Scholar]
  23. Hen R., Sassone-Corsi P., Corden J., Gaub M. P., Chambon P. Sequences upstream from the T-A-T-A box are required in vivo and in vitro for efficient transcription from the adenovirus serotype 2 major late promoter. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7132–7136. doi: 10.1073/pnas.79.23.7132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Horikoshi M., Wang C. K., Fujii H., Cromlish J. A., Weil P. A., Roeder R. G. Cloning and structure of a yeast gene encoding a general transcription initiation factor TFIID that binds to the TATA box. Nature. 1989 Sep 28;341(6240):299–303. doi: 10.1038/341299a0. [DOI] [PubMed] [Google Scholar]
  25. Horikoshi M., Wang C. K., Fujii H., Cromlish J. A., Weil P. A., Roeder R. G. Purification of a yeast TATA box-binding protein that exhibits human transcription factor IID activity. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4843–4847. doi: 10.1073/pnas.86.13.4843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
  27. Katsuki M., Sato M., Kimura M., Yokoyama M., Kobayashi K., Nomura T. Conversion of normal behavior to shiverer by myelin basic protein antisense cDNA in transgenic mice. Science. 1988 Jul 29;241(4865):593–595. doi: 10.1126/science.2456614. [DOI] [PubMed] [Google Scholar]
  28. Khoury G., Gruss P. Enhancer elements. Cell. 1983 Jun;33(2):313–314. doi: 10.1016/0092-8674(83)90410-5. [DOI] [PubMed] [Google Scholar]
  29. Matsui T., Segall J., Weil P. A., Roeder R. G. Multiple factors required for accurate initiation of transcription by purified RNA polymerase II. J Biol Chem. 1980 Dec 25;255(24):11992–11996. [PubMed] [Google Scholar]
  30. Miura M., Tamura T., Aoyama A., Mikoshiba K. The promoter elements of the mouse myelin basic protein gene function efficiently in NG108-15 neuronal/glial cells. Gene. 1989 Jan 30;75(1):31–38. doi: 10.1016/0378-1119(89)90380-6. [DOI] [PubMed] [Google Scholar]
  31. Monaci P., Nicosia A., Cortese R. Two different liver-specific factors stimulate in vitro transcription from the human alpha 1-antitrypsin promoter. EMBO J. 1988 Jul;7(7):2075–2087. doi: 10.1002/j.1460-2075.1988.tb03047.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Moncollin V., Miyamoto N. G., Zheng X. M., Egly J. M. Purification of a factor specific for the upstream element of the adenovirus-2 major late promoter. EMBO J. 1986 Oct;5(10):2577–2584. doi: 10.1002/j.1460-2075.1986.tb04537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Nakajima N., Horikoshi M., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II: purification, genetic specificity, and TATA box-promoter interactions of TFIID. Mol Cell Biol. 1988 Oct;8(10):4028–4040. doi: 10.1128/mcb.8.10.4028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Okano H., Miura M., Moriguchi A., Ikenaka K., Tsukada Y., Mikoshiba K. Inefficient transcription of the myelin basic protein gene possibly causes hypomyelination in myelin-deficient mutant mice. J Neurochem. 1987 Feb;48(2):470–476. doi: 10.1111/j.1471-4159.1987.tb04116.x. [DOI] [PubMed] [Google Scholar]
  35. Reinberg D., Roeder R. G. Factors involved in specific transcription by mammalian RNA polymerase II. Purification and functional analysis of initiation factors IIB and IIE. J Biol Chem. 1987 Mar 5;262(7):3310–3321. [PubMed] [Google Scholar]
  36. Sawadogo M., Roeder R. G. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell. 1985 Nov;43(1):165–175. doi: 10.1016/0092-8674(85)90021-2. [DOI] [PubMed] [Google Scholar]
  37. 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]
  38. 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]
  39. Smale S. T., Baltimore D. The "initiator" as a transcription control element. Cell. 1989 Apr 7;57(1):103–113. doi: 10.1016/0092-8674(89)90176-1. [DOI] [PubMed] [Google Scholar]
  40. Takahashi N., Roach A., Teplow D. B., Prusiner S. B., Hood L. Cloning and characterization of the myelin basic protein gene from mouse: one gene can encode both 14 kd and 18.5 kd MBPs by alternate use of exons. Cell. 1985 Aug;42(1):139–148. doi: 10.1016/s0092-8674(85)80109-4. [DOI] [PubMed] [Google Scholar]
  41. Takiya S., Hui C. C., Suzuki Y. A contribution of the core-promoter and its surrounding regions to the preferential transcription of the fibroin gene in posterior silk gland extracts. EMBO J. 1990 Feb;9(2):489–496. doi: 10.1002/j.1460-2075.1990.tb08135.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tamura T., Aoyama A., Inoue T., Miura M., Okano H., Mikoshiba K. Tissue-specific in vitro transcription from the mouse myelin basic protein promoter. Mol Cell Biol. 1989 Jul;9(7):3122–3126. doi: 10.1128/mcb.9.7.3122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tamura T., Miura M., Ikenaka K., Mikoshiba K. Analysis of transcription control elements of the mouse myelin basic protein gene in HeLa cell extracts: demonstration of a strong NFI-binding motif in the upstream region. Nucleic Acids Res. 1988 Dec 23;16(24):11441–11459. doi: 10.1093/nar/16.24.11441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tokunaga K., Hirose S., Suzuki Y. In monkey COS cells only the TATA box and the cap site region are required for faithful and efficient initiation of the fibroin gene transcription. Nucleic Acids Res. 1984 Feb 10;12(3):1543–1558. doi: 10.1093/nar/12.3.1543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Watanabe H., Imai T., Sharp P. A., Handa H. Identification of two transcription factors that bind to specific elements in the promoter of the adenovirus early-region 4. Mol Cell Biol. 1988 Mar;8(3):1290–1300. doi: 10.1128/mcb.8.3.1290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. 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]
  47. Wu L., Rosser D. S., Schmidt M. C., Berk A. A TATA box implicated in E1A transcriptional activation of a simple adenovirus 2 promoter. Nature. 1987 Apr 2;326(6112):512–515. doi: 10.1038/326512a0. [DOI] [PubMed] [Google Scholar]
  48. Yaniv M. Regulation of eukaryotic gene expression by transactivating proteins and cis acting DNA elements. Biol Cell. 1984;50(3):203–216. doi: 10.1111/j.1768-322x.1984.tb00268.x. [DOI] [PubMed] [Google Scholar]

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