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. 1988 Dec 23;16(24):11441–11459. doi: 10.1093/nar/16.24.11441

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.

T Tamura 1, M Miura 1, K Ikenaka 1, K Mikoshiba 1
PMCID: PMC339057  PMID: 2463515

Abstract

Promoter elements of the mouse myelin basic protein (MBP) gene were analyzed by in vitro transcription using HeLa cell extracts. We demonstrated the MBTE (MBP transcription element), GC-box core and TATA-box elements, at -130, -93 and -34, respectively. The TATA-box was indispensable for the promoter function. The GC-box was suggested to function co-operatively with far upstream sequences including the MBTE. The MBTE was crucial to direct maximal transcription, and also functioned with a heterologous promoter irrespective of its orientation. We identified a ubiquitous binding factor which interacted specifically with the MBTE and activated transcription. Intensive foot-printing studies demonstrated that the MBTE had a NFI-binding sequence. The MBTE was considered to be one of the strongest NFI-binding motif among known cellular genes. Interestingly, similar strong NFI-binding motifs were suggested to be present in the enhancer of JC virus whose gene is expressed like the MBP gene, in the nervous system.

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Selected References

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  1. Borgmeyer U., Nowock J., Sippel A. E. The TGGCA-binding protein: a eukaryotic nuclear protein recognizing a symmetrical sequence on double-stranded linear DNA. Nucleic Acids Res. 1984 May 25;12(10):4295–4311. doi: 10.1093/nar/12.10.4295. [DOI] [PMC free article] [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. Cereghini S., Raymondjean M., Carranca A. G., Herbomel P., Yaniv M. Factors involved in control of tissue-specific expression of albumin gene. Cell. 1987 Aug 14;50(4):627–638. doi: 10.1016/0092-8674(87)90036-5. [DOI] [PubMed] [Google Scholar]
  4. Cohen P. The coordinated control of metabolic pathways by broad-specificity protein kinases and phosphatases. Curr Top Cell Regul. 1985;27:23–37. doi: 10.1016/b978-0-12-152827-0.50010-4. [DOI] [PubMed] [Google Scholar]
  5. Dorn A., Bollekens J., Staub A., Benoist C., Mathis D. A multiplicity of CCAAT box-binding proteins. Cell. 1987 Sep 11;50(6):863–872. doi: 10.1016/0092-8674(87)90513-7. [DOI] [PubMed] [Google Scholar]
  6. Graves B. J., Johnson P. F., McKnight S. L. Homologous recognition of a promoter domain common to the MSV LTR and the HSV tk gene. Cell. 1986 Feb 28;44(4):565–576. doi: 10.1016/0092-8674(86)90266-7. [DOI] [PubMed] [Google Scholar]
  7. Graves B. J., Johnson P. F., McKnight S. L. Homologous recognition of a promoter domain common to the MSV LTR and the HSV tk gene. Cell. 1986 Feb 28;44(4):565–576. doi: 10.1016/0092-8674(86)90266-7. [DOI] [PubMed] [Google Scholar]
  8. Gronostajski R. M., Knox J., Berry D., Miyamoto N. G. Stimulation of transcription in vitro by binding sites for nuclear factor I. Nucleic Acids Res. 1988 Mar 25;16(5):2087–2098. doi: 10.1093/nar/16.5.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gronostajski R. M. Site-specific DNA binding of nuclear factor I: effect of the spacer region. Nucleic Acids Res. 1987 Jul 24;15(14):5545–5559. doi: 10.1093/nar/15.14.5545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hennighausen L., Siebenlist U., Danner D., Leder P., Rawlins D., Rosenfeld P., Kelly T., Jr High-affinity binding site for a specific nuclear protein in the human IgM gene. Nature. 1985 Mar 21;314(6008):289–292. doi: 10.1038/314289a0. [DOI] [PubMed] [Google Scholar]
  11. Jeang K. T., Rawlins D. R., Rosenfeld P. J., Shero J. H., Kelly T. J., Hayward G. S. Multiple tandemly repeated binding sites for cellular nuclear factor 1 that surround the major immediate-early promoters of simian and human cytomegalovirus. J Virol. 1987 May;61(5):1559–1570. doi: 10.1128/jvi.61.5.1559-1570.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jones K. A., Kadonaga J. T., Rosenfeld P. J., Kelly T. J., Tjian R. A cellular DNA-binding protein that activates eukaryotic transcription and DNA replication. Cell. 1987 Jan 16;48(1):79–89. doi: 10.1016/0092-8674(87)90358-8. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Kenney S., Natarajan V., Strike D., Khoury G., Salzman N. P. JC virus enhancer-promoter active in human brain cells. Science. 1984 Dec 14;226(4680):1337–1339. doi: 10.1126/science.6095453. [DOI] [PubMed] [Google Scholar]
  16. Khalili K., Rappaport J., Khoury G. Nuclear factors in human brain cells bind specifically to the JCV regulatory region. EMBO J. 1988 Apr;7(4):1205–1210. doi: 10.1002/j.1460-2075.1988.tb02932.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Leegwater P. A., van der Vliet P. C., Rupp R. A., Nowock J., Sippel A. E. Functional homology between the sequence-specific DNA-binding proteins nuclear factor I from HeLa cells and the TGGCA protein from chicken liver. EMBO J. 1986 Feb;5(2):381–386. doi: 10.1002/j.1460-2075.1986.tb04223.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lemke G., Chao M. Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development. 1988 Mar;102(3):499–504. doi: 10.1242/dev.102.3.499. [DOI] [PubMed] [Google Scholar]
  19. Lichtsteiner S., Wuarin J., Schibler U. The interplay of DNA-binding proteins on the promoter of the mouse albumin gene. Cell. 1987 Dec 24;51(6):963–973. doi: 10.1016/0092-8674(87)90583-6. [DOI] [PubMed] [Google Scholar]
  20. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mathis D. J., Elkaim R., Kédinger C., Sassone-Corsi P., Chambon P. Specific in vitro initiation of transcription on the adenovirus type 2 early and late EII transcription units. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7383–7387. doi: 10.1073/pnas.78.12.7383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Matthieu J. M., Omlin F. X. Murine leukodystrophies as tools to study myelinogenesis in normal and pathological conditions. Neuropediatrics. 1984 Sep;15 (Suppl):37–52. doi: 10.1055/s-2008-1052381. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. McKnight S., Tjian R. Transcriptional selectivity of viral genes in mammalian cells. Cell. 1986 Sep 12;46(6):795–805. doi: 10.1016/0092-8674(86)90061-9. [DOI] [PubMed] [Google Scholar]
  25. Miksicek R., Borgmeyer U., Nowock J. Interaction of the TGGCA-binding protein with upstream sequences is required for efficient transcription of mouse mammary tumor virus. EMBO J. 1987 May;6(5):1355–1360. doi: 10.1002/j.1460-2075.1987.tb02375.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miyamoto N. G., Moncollin V., Wintzerith M., Hen R., Egly J. M., Chambon P. Stimulation of in vitro transcription by the upstream element of the adenovirus-2 major late promoter involves a specific factor. Nucleic Acids Res. 1984 Dec 11;12(23):8779–8799. doi: 10.1093/nar/12.23.8779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Nagata K., Guggenheimer R. A., Hurwitz J. Specific binding of a cellular DNA replication protein to the origin of replication of adenovirus DNA. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6177–6181. doi: 10.1073/pnas.80.20.6177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Narayan O., Penney J. B., Jr, Johnson R. T., Herndon R. M., Weiner L. P. Etiology of progressive multifocal leukoencephalopathy. Identification of papovavirus. N Engl J Med. 1973 Dec 13;289(24):1278–1282. doi: 10.1056/NEJM197312132892405. [DOI] [PubMed] [Google Scholar]
  29. Nowock J., Borgmeyer U., Püschel A. W., Rupp R. A., Sippel A. E. The TGGCA protein binds to the MMTV-LTR, the adenovirus origin of replication, and the BK virus enhancer. Nucleic Acids Res. 1985 Mar 25;13(6):2045–2061. doi: 10.1093/nar/13.6.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nowock J., Sippel A. E. Specific protein-DNA interaction at four sites flanking the chicken lysozyme gene. Cell. 1982 Sep;30(2):607–615. doi: 10.1016/0092-8674(82)90257-4. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Padgett B. L., Walker D. L., ZuRhein G. M., Hodach A. E., Chou S. M. JC Papovavirus in progressive multifocal leukoencephalopathy. J Infect Dis. 1976 Jun;133(6):686–690. doi: 10.1093/infdis/133.6.686. [DOI] [PubMed] [Google Scholar]
  33. Peterson A., Marler J. P1 deficiency in shiverer myelin is expressed by Schwann cells in shiverer dystrophic normal mouse chimaera nerves. Neurosci Lett. 1983 Jul 29;38(2):163–168. doi: 10.1016/0304-3940(83)90034-4. [DOI] [PubMed] [Google Scholar]
  34. Raymondjean M., Cereghini S., Yaniv M. Several distinct "CCAAT" box binding proteins coexist in eukaryotic cells. Proc Natl Acad Sci U S A. 1988 Feb;85(3):757–761. doi: 10.1073/pnas.85.3.757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Readhead C., Popko B., Takahashi N., Shine H. D., Saavedra R. A., Sidman R. L., Hood L. Expression of a myelin basic protein gene in transgenic shiverer mice: correction of the dysmyelinating phenotype. Cell. 1987 Feb 27;48(4):703–712. doi: 10.1016/0092-8674(87)90248-0. [DOI] [PubMed] [Google Scholar]
  36. Rupp R. A., Sippel A. E. Chicken liver TGGCA protein purified by preparative mobility shift electrophoresis (PMSE) shows a 36.8 to 29.8 kd microheterogeneity. Nucleic Acids Res. 1987 Dec 10;15(23):9707–9726. doi: 10.1093/nar/15.23.9707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Santoro C., Mermod N., Andrews P. C., Tjian R. A family of human CCAAT-box-binding proteins active in transcription and DNA replication: cloning and expression of multiple cDNAs. Nature. 1988 Jul 21;334(6179):218–224. doi: 10.1038/334218a0. [DOI] [PubMed] [Google Scholar]
  38. Siebenlist U., Hennighausen L., Battey J., Leder P. Chromatin structure and protein binding in the putative regulatory region of the c-myc gene in Burkitt lymphoma. Cell. 1984 Jun;37(2):381–391. doi: 10.1016/0092-8674(84)90368-4. [DOI] [PubMed] [Google Scholar]
  39. Sive H. L., Heintz N., Roeder R. G. Multiple sequence elements are required for maximal in vitro transcription of a human histone H2B gene. Mol Cell Biol. 1986 Oct;6(10):3329–3340. doi: 10.1128/mcb.6.10.3329. [DOI] [PMC free article] [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]

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