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. 1988 Nov;8(11):4587–4597. doi: 10.1128/mcb.8.11.4587

The chicken skeletal alpha-actin gene promoter region exhibits partial dyad symmetry and a capacity to drive bidirectional transcription.

J M Grichnik 1, B A French 1, R J Schwartz 1
PMCID: PMC365547  PMID: 3211124

Abstract

The chicken skeletal alpha-actin gene promoter region (-202 to -12) provides myogenic transcriptional specificity. This promoter contains partial dyad symmetry about an axis at nucleotide -108 and in transfection experiments is capable of directing transcription in a bidirectional manner. At least three different transcription initiation start sites, oriented toward upstream sequences, were mapped 25 to 30 base pairs from TATA-like regions. The opposing transcriptional activity was potentiated upon the deletion of sequences proximal to the alpha-actin transcription start site. Thus, sequences which serve to position RNA polymerase for alpha-actin transcription may allow, in their absence, the selection of alternative and reverse-oriented start sites. Nuclear runoff transcription assays of embryonic muscle indicated that divergent transcription may occur in vivo but with rapid turnover of nuclear transcripts. Divergent transcriptional activity enabled us to define the 3' regulatory boundary of the skeletal alpha-actin promoter which retains a high level of myogenic transcriptional activity. The 3' regulatory border was detected when serial 3' deletions bisected the element (-91 CCAAA TATGG -82) which reduced transcriptional activity by 80%. Previously we showed that disruption of its upstream counterpart (-127 CCAAAGAAGG -136) resulted in about a 90% decrease in activity. These element pairs, which we describe as CCAAT box-associated repeats, are conserved in all sequenced vertebrate sarcomeric actin genes and may act in a cooperative manner to facilitate transcription in myogenic cells.

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Selected References

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

  1. Allison L. A., Wong J. K., Fitzpatrick V. D., Moyle M., Ingles C. J. The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster, and mammals: a conserved structure with an essential function. Mol Cell Biol. 1988 Jan;8(1):321–329. doi: 10.1128/mcb.8.1.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barberis A., Superti-Furga G., Busslinger M. Mutually exclusive interaction of the CCAAT-binding factor and of a displacement protein with overlapping sequences of a histone gene promoter. Cell. 1987 Jul 31;50(3):347–359. doi: 10.1016/0092-8674(87)90489-2. [DOI] [PubMed] [Google Scholar]
  3. Bartolomei M. S., Corden J. L. Localization of an alpha-amanitin resistance mutation in the gene encoding the largest subunit of mouse RNA polymerase II. Mol Cell Biol. 1987 Feb;7(2):586–594. doi: 10.1128/mcb.7.2.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benoist C., O'Hare K., Breathnach R., Chambon P. The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res. 1980 Jan 11;8(1):127–142. doi: 10.1093/nar/8.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bergsma D. J., Grichnik J. M., Gossett L. M., Schwartz R. J. Delimitation and characterization of cis-acting DNA sequences required for the regulated expression and transcriptional control of the chicken skeletal alpha-actin gene. Mol Cell Biol. 1986 Jul;6(7):2462–2475. doi: 10.1128/mcb.6.7.2462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Carroll S. L., Bergsma D. J., Schwartz R. J. Structure and complete nucleotide sequence of the chicken alpha-smooth muscle (aortic) actin gene. An actin gene which produces multiple messenger RNAs. J Biol Chem. 1986 Jul 5;261(19):8965–8976. [PubMed] [Google Scholar]
  8. 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]
  9. Chang K. S., Rothblum K. N., Schwartz R. J. The complete sequence of the chicken alpha-cardiac actin gene: a highly conserved vertebrate gene. Nucleic Acids Res. 1985 Feb 25;13(4):1223–1237. doi: 10.1093/nar/13.4.1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chang K. S., Zimmer W. E., Jr, Bergsma D. J., Dodgson J. B., Schwartz R. J. Isolation and characterization of six different chicken actin genes. Mol Cell Biol. 1984 Nov;4(11):2498–2508. doi: 10.1128/mcb.4.11.2498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crouse G. F., Leys E. J., McEwan R. N., Frayne E. G., Kellems R. E. Analysis of the mouse dhfr promoter region: existence of a divergently transcribed gene. Mol Cell Biol. 1985 Aug;5(8):1847–1858. doi: 10.1128/mcb.5.8.1847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  14. Fisher R. P., Topper J. N., Clayton D. A. Promoter selection in human mitochondria involves binding of a transcription factor to orientation-independent upstream regulatory elements. Cell. 1987 Jul 17;50(2):247–258. doi: 10.1016/0092-8674(87)90220-0. [DOI] [PubMed] [Google Scholar]
  15. Fornwald J. A., Kuncio G., Peng I., Ordahl C. P. The complete nucleotide sequence of the chick a-actin gene and its evolutionary relationship to the actin gene family. Nucleic Acids Res. 1982 Jul 10;10(13):3861–3876. doi: 10.1093/nar/10.13.3861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fujita T., Shibuya H., Hotta H., Yamanishi K., Taniguchi T. Interferon-beta gene regulation: tandemly repeated sequences of a synthetic 6 bp oligomer function as a virus-inducible enhancer. Cell. 1987 May 8;49(3):357–367. doi: 10.1016/0092-8674(87)90288-1. [DOI] [PubMed] [Google Scholar]
  17. Fyrberg E. A., Mahaffey J. W., Bond B. J., Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell. 1983 May;33(1):115–123. doi: 10.1016/0092-8674(83)90340-9. [DOI] [PubMed] [Google Scholar]
  18. Garcia R., Paz-Aliaga B., Ernst S. G., Crain W. R., Jr Three sea urchin actin genes show different patterns of expression: muscle specific, embryo specific, and constitutive. Mol Cell Biol. 1984 May;4(5):840–845. doi: 10.1128/mcb.4.5.840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gidoni D., Kadonaga J. T., Barrera-Saldaña H., Takahashi K., Chambon P., Tjian R. Bidirectional SV40 transcription mediated by tandem Sp1 binding interactions. Science. 1985 Nov 1;230(4725):511–517. doi: 10.1126/science.2996137. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Grichnik J. M., Bergsma D. J., Schwartz R. J. Tissue restricted and stage specific transcription is maintained within 411 nucleotides flanking the 5' end of the chicken alpha-skeletal actin gene. Nucleic Acids Res. 1986 Feb 25;14(4):1683–1701. doi: 10.1093/nar/14.4.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gunning P., Hardeman E., Wade R., Ponte P., Bains W., Blau H. M., Kedes L. Differential patterns of transcript accumulation during human myogenesis. Mol Cell Biol. 1987 Nov;7(11):4100–4114. doi: 10.1128/mcb.7.11.4100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Gurdon J. B., Brennan S., Fairman S., Mohun T. J. Transcription of muscle-specific actin genes in early Xenopus development: nuclear transplantation and cell dissociation. Cell. 1984 Oct;38(3):691–700. doi: 10.1016/0092-8674(84)90264-2. [DOI] [PubMed] [Google Scholar]
  26. Hanahan D. Heritable formation of pancreatic beta-cell tumours in transgenic mice expressing recombinant insulin/simian virus 40 oncogenes. Nature. 1985 May 9;315(6015):115–122. doi: 10.1038/315115a0. [DOI] [PubMed] [Google Scholar]
  27. Hayward L. J., Schwartz R. J. Sequential expression of chicken actin genes during myogenesis. J Cell Biol. 1986 Apr;102(4):1485–1493. doi: 10.1083/jcb.102.4.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hu M. C., Sharp S. B., Davidson N. The complete sequence of the mouse skeletal alpha-actin gene reveals several conserved and inverted repeat sequences outside of the protein-coding region. Mol Cell Biol. 1986 Jan;6(1):15–25. doi: 10.1128/mcb.6.1.15. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Linial M., Gunderson N., Groudine M. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science. 1985 Dec 6;230(4730):1126–1132. doi: 10.1126/science.2999973. [DOI] [PubMed] [Google Scholar]
  31. McKeown M., Firtel R. A. Differential expression and 5' end mapping of actin genes in Dictyostelium. Cell. 1981 Jun;24(3):799–807. doi: 10.1016/0092-8674(81)90105-7. [DOI] [PubMed] [Google Scholar]
  32. Melloul D., Aloni B., Calvo J., Yaffe D., Nudel U. Developmentally regulated expression of chimeric genes containing muscle actin DNA sequences in transfected myogenic cells. EMBO J. 1984 May;3(5):983–990. doi: 10.1002/j.1460-2075.1984.tb01917.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Minty A. J., Alonso S., Caravatti M., Buckingham M. E. A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell. 1982 Aug;30(1):185–192. doi: 10.1016/0092-8674(82)90024-1. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. 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]
  36. Moye W. S., Zalkin H. Roles of the TGACT repeat sequence in the yeast TRP5 promoter. J Biol Chem. 1987 Mar 15;262(8):3609–3614. [PubMed] [Google Scholar]
  37. Natarajan V., Madden M. J., Salzman N. P. Proximal and distal domains that control in vitro transcription of the adenovirus IVa2 gene. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6290–6294. doi: 10.1073/pnas.81.20.6290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Norton P. A., Coffin J. M. Bacterial beta-galactosidase as a marker of Rous sarcoma virus gene expression and replication. Mol Cell Biol. 1985 Feb;5(2):281–290. doi: 10.1128/mcb.5.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Omilli F., Ernoult-Lange M., Borde J., May E. Sequences involved in initiation of simian virus 40 late transcription in the absence of T antigen. Mol Cell Biol. 1986 Jun;6(6):1875–1885. doi: 10.1128/mcb.6.6.1875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ptashne M., Jeffrey A., Johnson A. D., Maurer R., Meyer B. J., Pabo C. O., Roberts T. M., Sauer R. T. How the lambda repressor and cro work. Cell. 1980 Jan;19(1):1–11. doi: 10.1016/0092-8674(80)90383-9. [DOI] [PubMed] [Google Scholar]
  41. Searle P. F., Stuart G. W., Palmiter R. D. Building a metal-responsive promoter with synthetic regulatory elements. Mol Cell Biol. 1985 Jun;5(6):1480–1489. doi: 10.1128/mcb.5.6.1480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Seiler-Tuyns A., Walker P., Martinez E., Mérillat A. M., Givel F., Wahli W. Identification of estrogen-responsive DNA sequences by transient expression experiments in a human breast cancer cell line. Nucleic Acids Res. 1986 Nov 25;14(22):8755–8770. doi: 10.1093/nar/14.22.8755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Shani M. Tissue-specific and developmentally regulated expression of a chimeric actin-globin gene in transgenic mice. Mol Cell Biol. 1986 Jul;6(7):2624–2631. doi: 10.1128/mcb.6.7.2624. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stutz F., Spohr G. Isolation and characterization of sarcomeric actin genes expressed in Xenopus laevis embryos. J Mol Biol. 1986 Feb 5;187(3):349–361. doi: 10.1016/0022-2836(86)90438-9. [DOI] [PubMed] [Google Scholar]
  45. Vandekerckhove J., Weber K. Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. J Mol Biol. 1984 Nov 5;179(3):391–413. doi: 10.1016/0022-2836(84)90072-x. [DOI] [PubMed] [Google Scholar]
  46. Vandekerckhove J., Weber K. The complete amino acid sequence of actins from bovine aorta, bovine heart, bovine fast skeletal muscle, and rabbit slow skeletal muscle. A protein-chemical analysis of muscle actin differentiation. Differentiation. 1979;14(3):123–133. doi: 10.1111/j.1432-0436.1979.tb01021.x. [DOI] [PubMed] [Google Scholar]
  47. Walsh K., Schimmel P. Two nuclear factors compete for the skeletal muscle actin promoter. J Biol Chem. 1987 Jul 15;262(20):9429–9432. [PubMed] [Google Scholar]
  48. Williams T. J., Fried M. The MES-1 murine enhancer element is closely associated with the heterogeneous 5' ends of two divergent transcription units. Mol Cell Biol. 1986 Dec;6(12):4558–4569. doi: 10.1128/mcb.6.12.4558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Wilson C., Cross G. S., Woodland H. R. Tissue-specific expression of actin genes injected into Xenopus embryos. Cell. 1986 Nov 21;47(4):589–599. doi: 10.1016/0092-8674(86)90623-9. [DOI] [PubMed] [Google Scholar]
  50. Zakut R., Shani M., Givol D., Neuman S., Yaffe D., Nudel U. Nucleotide sequence of the rat skeletal muscle actin gene. Nature. 1982 Aug 26;298(5877):857–859. doi: 10.1038/298857a0. [DOI] [PubMed] [Google Scholar]

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