Abstract
The transcriptional regulation of the chicken myosin alkali light-chain (MLC) L23 gene was analyzed. Two different types of cis-regulatory regions were identified: one was a silencerlike region located between 3.7 and 2.7 kilobases upstream of the mRNA initiation site, and the other was essential for the expression of L23 in skeletal muscle cells and was located between 106 and 91 base pairs upstream of the cap site. This 16-base-pair cis-acting element was designated as the MLC box since it is well conserved in various muscle-specific MLC promoter regions. The activity of the MLC box showed tissue specificity. To analyze the relationship between the nucleotide sequence and the activity of the MLC box precisely, mutation analysis was performed. The 16-base-pair sequence was indispensable for the active transcription of L23 gene, and the MLC box could function in either orientation. The inverted sequence of the MLC box was similar to the sequence of the alpha-actin CArG box. By using a gel mobility retardation assay, the nuclear protein(s) that binds to both MLC box and CArG box was detected with nuclear extract prepared from chicken embryonic breast muscle. These observations imply that a common factor regulates the coordinate expression of these contractile proteins in muscle differentiation.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Akerblom I. E., Slater E. P., Beato M., Baxter J. D., Mellon P. L. Negative regulation by glucocorticoids through interference with a cAMP responsive enhancer. Science. 1988 Jul 15;241(4863):350–353. doi: 10.1126/science.2838908. [DOI] [PubMed] [Google Scholar]
- Bouvagnet P. F., Strehler E. E., White G. E., Strehler-Page M. A., Nadal-Ginard B., Mahdavi V. Multiple positive and negative 5' regulatory elements control the cell-type-specific expression of the embryonic skeletal myosin heavy-chain gene. Mol Cell Biol. 1987 Dec;7(12):4377–4389. doi: 10.1128/mcb.7.12.4377. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boxer L. M., Prywes R., Roeder R. G., Kedes L. The sarcomeric actin CArG-binding factor is indistinguishable from the c-fos serum response factor. Mol Cell Biol. 1989 Feb;9(2):515–522. doi: 10.1128/mcb.9.2.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1006/abio.1976.9999. [DOI] [PubMed] [Google Scholar]
- Daubas P., Robert B., Garner I., Buckingham M. A comparison between mammalian and avian fast skeletal muscle alkali myosin light chain genes: regulatory implications. Nucleic Acids Res. 1985 Jul 11;13(13):4623–4643. doi: 10.1093/nar/13.13.4623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis R. L., Weintraub H., Lassar A. B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987 Dec 24;51(6):987–1000. doi: 10.1016/0092-8674(87)90585-x. [DOI] [PubMed] [Google Scholar]
- Devlin R. B., Emerson C. P., Jr Coordinate accumulation of contractile protein mRNAs during myoblast differentiation. Dev Biol. 1979 Mar;69(1):202–216. doi: 10.1016/0012-1606(79)90286-0. [DOI] [PubMed] [Google Scholar]
- Fujisawa-Sehara A., Sogawa K., Nishi C., Fujii-Kuriyama Y. Regulatory DNA elements localized remotely upstream from the drug-metabolizing cytochrome P-450c gene. Nucleic Acids Res. 1986 Feb 11;14(3):1465–1477. doi: 10.1093/nar/14.3.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gauthier G. F., Lowey S., Benfield P. A., Hobbs A. W. Distribution and properties of myosin isozymes in developing avian and mammalian skeletal muscle fibers. J Cell Biol. 1982 Feb;92(2):471–484. doi: 10.1083/jcb.92.2.471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodbourn S., Maniatis T. Overlapping positive and negative regulatory domains of the human beta-interferon gene. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1447–1451. doi: 10.1073/pnas.85.5.1447. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Kawashima M., Nabeshima Y., Obinata T., Fujii-Kuriyama Y. A common myosin light chain is expressed in chicken embryonic skeletal, cardiac, and smooth muscles and in brain continuously from embryo to adult. J Biol Chem. 1987 Oct 25;262(30):14408–14414. [PubMed] [Google Scholar]
- Kronstad J. W., Holly J. A., MacKay V. L. A yeast operator overlaps an upstream activation site. Cell. 1987 Jul 31;50(3):369–377. doi: 10.1016/0092-8674(87)90491-0. [DOI] [PubMed] [Google Scholar]
- Lassar A. B., Buskin J. N., Lockshon D., Davis R. L., Apone S., Hauschka S. D., Weintraub H. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell. 1989 Sep 8;58(5):823–831. doi: 10.1016/0092-8674(89)90935-5. [DOI] [PubMed] [Google Scholar]
- Lopata M. A., Cleveland D. W., Sollner-Webb B. High level transient expression of a chloramphenicol acetyl transferase gene by DEAE-dextran mediated DNA transfection coupled with a dimethyl sulfoxide or glycerol shock treatment. Nucleic Acids Res. 1984 Jul 25;12(14):5707–5717. doi: 10.1093/nar/12.14.5707. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minty A., Kedes L. Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: presence of an evolutionarily conserved repeated motif. Mol Cell Biol. 1986 Jun;6(6):2125–2136. doi: 10.1128/mcb.6.6.2125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miwa T., Boxer L. M., Kedes L. CArG boxes in the human cardiac alpha-actin gene are core binding sites for positive trans-acting regulatory factors. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6702–6706. doi: 10.1073/pnas.84.19.6702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miwa T., Kedes L. Duplicated CArG box domains have positive and mutually dependent regulatory roles in expression of the human alpha-cardiac actin gene. Mol Cell Biol. 1987 Aug;7(8):2803–2813. doi: 10.1128/mcb.7.8.2803. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mohun T. J., Taylor M. V., Garrett N., Gurdon J. B. The CArG promoter sequence is necessary for muscle-specific transcription of the cardiac actin gene in Xenopus embryos. EMBO J. 1989 Apr;8(4):1153–1161. doi: 10.1002/j.1460-2075.1989.tb03486.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mohun T., Garrett N., Treisman R. Xenopus cytoskeletal actin and human c-fos gene promoters share a conserved protein-binding site. EMBO J. 1987 Mar;6(3):667–673. doi: 10.1002/j.1460-2075.1987.tb04806.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muscat G. E., Gustafson T. A., Kedes L. A common factor regulates skeletal and cardiac alpha-actin gene transcription in muscle. Mol Cell Biol. 1988 Oct;8(10):4120–4133. doi: 10.1128/mcb.8.10.4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nabeshima Y., Fujii-Kuriyama Y., Muramatsu M., Ogata K. Alternative transcription and two modes of splicing results in two myosin light chains from one gene. Nature. 1984 Mar 22;308(5957):333–338. doi: 10.1038/308333a0. [DOI] [PubMed] [Google Scholar]
- Nabeshima Y., Fujii-Kuriyama Y., Muramatsu M., Ogata K. Molecular cloning and nucleotide sequences of the complementary DNAs to chicken skeletal muscle myosin two alkali light chain mRNAs. Nucleic Acids Res. 1982 Oct 11;10(19):6099–6110. doi: 10.1093/nar/10.19.6099. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nabeshima Y., Nabeshima Y., Kawashima M., Nakamura S., Nonomura Y., Fujii-Kuriyama Y. Isolation of the chick myosin alkali light chain gene expressed in embryonic gizzard muscle and transitional expression of the light chain gene family in vivo. J Mol Biol. 1988 Dec 5;204(3):497–505. doi: 10.1016/0022-2836(88)90350-6. [DOI] [PubMed] [Google Scholar]
- Nabeshima Y., Nabeshima Y., Nonomura Y., Fujii-Kuriyama Y. Nonmuscle and smooth muscle myosin light chain mRNAs are generated from a single gene by the tissue-specific alternative RNA splicing. J Biol Chem. 1987 Aug 5;262(22):10608–10612. [PubMed] [Google Scholar]
- Nakamura S., Nabeshima Y., Kobayashi H., Nabeshima Y., Nonomura Y., Fujii-Kuriyama Y. Single chicken cardiac myosin alkali light-chain gene generates two different mRNAs by alternative splicing of a complex exon. J Mol Biol. 1988 Oct 20;203(4):895–904. doi: 10.1016/0022-2836(88)90115-5. [DOI] [PubMed] [Google Scholar]
- Norman C., Runswick M., Pollock R., Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell. 1988 Dec 23;55(6):989–1003. doi: 10.1016/0092-8674(88)90244-9. [DOI] [PubMed] [Google Scholar]
- Obinata T., Masaki T., Takano-Ohmuro H., Tanaka T., Shimizu N. Coexistence of cardiac-type and fast skeletal-type myosin light chains in embryonic chicken cardiac muscle. J Biochem. 1983 Sep;94(3):1025–1028. doi: 10.1093/oxfordjournals.jbchem.a134401. [DOI] [PubMed] [Google Scholar]
- Robert B., Daubas P., Akimenko M. A., Cohen A., Garner I., Guenet J. L., Buckingham M. A single locus in the mouse encodes both myosin light chains 1 and 3, a second locus corresponds to a related pseudogene. Cell. 1984 Nov;39(1):129–140. doi: 10.1016/0092-8674(84)90198-3. [DOI] [PubMed] [Google Scholar]
- Ryan W. A., Jr, Franza B. R., Jr, Gilman M. Z. Two distinct cellular phosphoproteins bind to the c-fos serum response element. EMBO J. 1989 Jun;8(6):1785–1792. doi: 10.1002/j.1460-2075.1989.tb03572.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shirakata M., Nabeshima Y., Konishi K., Fujii-Kuriyama Y. Upstream regulatory region for inducible expression of the chicken skeletal myosin alkali light-chain gene. Mol Cell Biol. 1988 Jun;8(6):2581–2588. doi: 10.1128/mcb.8.6.2581. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh H., Sen R., Baltimore D., Sharp P. A. A nuclear factor that binds to a conserved sequence motif in transcriptional control elements of immunoglobulin genes. Nature. 1986 Jan 9;319(6049):154–158. doi: 10.1038/319154a0. [DOI] [PubMed] [Google Scholar]
- Strehler E. E., Periasamy M., Strehler-Page M. A., Nadal-Ginard B. Myosin light-chain 1 and 3 gene has two structurally distinct and differentially regulated promoters evolving at different rates. Mol Cell Biol. 1985 Nov;5(11):3168–3182. doi: 10.1128/mcb.5.11.3168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor M., Treisman R., Garrett N., Mohun T. Muscle-specific (CArG) and serum-responsive (SRE) promoter elements are functionally interchangeable in Xenopus embryos and mouse fibroblasts. Development. 1989 May;106(1):67–78. doi: 10.1242/dev.106.1.67. [DOI] [PubMed] [Google Scholar]
- Treisman R. Transient accumulation of c-fos RNA following serum stimulation requires a conserved 5' element and c-fos 3' sequences. Cell. 1985 Oct;42(3):889–902. doi: 10.1016/0092-8674(85)90285-5. [DOI] [PubMed] [Google Scholar]
- Walsh K. Cross-binding of factors to functionally different promoter elements in c-fos and skeletal actin genes. Mol Cell Biol. 1989 May;9(5):2191–2201. doi: 10.1128/mcb.9.5.2191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wigler M., Sweet R., Sim G. K., Wold B., Pellicer A., Lacy E., Maniatis T., Silverstein S., Axel R. Transformation of mammalian cells with genes from procaryotes and eucaryotes. Cell. 1979 Apr;16(4):777–785. doi: 10.1016/0092-8674(79)90093-x. [DOI] [PubMed] [Google Scholar]