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. 1989 Aug;9(8):3218–3230. doi: 10.1128/mcb.9.8.3218

Identification of two nuclear factor-binding domains on the chicken cardiac actin promoter: implications for regulation of the gene.

W W Quitschke 1, L DePonti-Zilli 1, Z Y Lin 1, B M Paterson 1
PMCID: PMC362366  PMID: 2552286

Abstract

The cis-acting regions that appear to be involved in negative regulation of the chicken alpha-cardiac actin promoter both in vivo and in vitro have been identified. A nuclear factor(s) binding to the proximal region mapped over the TATA element between nucleotides -50 and -25. In the distal region, binding spanned nucleotides -136 to -112, a region that included a second CArG box (CArG2) 5' to the more familiar CCAAT-box (CArG1) consensus sequence. Nuclear factors binding to these different domains were found in both muscle and nonmuscle preparations but were detectable at considerably lower levels in tissues expressing the alpha-cardiac actin gene. In contrast, concentrations of the beta-actin CCAAT-box binding activity were similar in all extracts tested. The role of these factor-binding domains on the activity of the cardiac actin promoter in vivo and in vitro and the prevalence of the binding factors in nonmuscle extracts are consistent with the idea that these binding domains and their associated factors are involved in the tissue-restricted expression of cardiac actin through both positive and negative regulatory mechanisms. In the absence of negative regulatory factors, these same binding domains act synergistically, via other factors, to activate the cardiac actin promoter during myogenesis.

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Selected References

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

  1. 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]
  2. 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]
  3. Billeter R., Quitschke W., Paterson B. M. Approximately 1 kilobase of sequence 5' to the two myosin light-chain 1f/3f gene cap sites is sufficient for differentiation-dependent expression. Mol Cell Biol. 1988 Mar;8(3):1361–1365. doi: 10.1128/mcb.8.3.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cao Z. D., Barron E. A., Carillo A. J., Sharp Z. D. Reconstitution of cell-type-specific transcription of the rat prolactin gene in vitro. Mol Cell Biol. 1987 Oct;7(10):3402–3408. doi: 10.1128/mcb.7.10.3402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carroll S. L., Bergsma D. J., Schwartz R. J. A 29-nucleotide DNA segment containing an evolutionarily conserved motif is required in cis for cell-type-restricted repression of the chicken alpha-smooth muscle actin gene core promoter. Mol Cell Biol. 1988 Jan;8(1):241–250. doi: 10.1128/mcb.8.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DePonti-Zilli L., Seiler-Tuyns A., Paterson B. M. A 40-base-pair sequence in the 3' end of the beta-actin gene regulates beta-actin mRNA transcription during myogenesis. Proc Natl Acad Sci U S A. 1988 Mar;85(5):1389–1393. doi: 10.1073/pnas.85.5.1389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Elder P. K., French C. L., Subramaniam M., Schmidt L. J., Getz M. J. Evidence that the functional beta-actin gene is single copy in most mice and is associated with 5' sequences capable of conferring serum- and cycloheximide-dependent regulation. Mol Cell Biol. 1988 Jan;8(1):480–485. doi: 10.1128/mcb.8.1.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eldridge J., Zehner Z., Paterson B. M. Nucleotide sequence of the chicken cardiac alpha actin gene: absence of strong homologies in the promoter and 3'-untranslated regions with the skeletal alpha actin sequence. Gene. 1985;36(1-2):55–63. doi: 10.1016/0378-1119(85)90069-1. [DOI] [PubMed] [Google Scholar]
  9. Galas D. J., Schmitz A. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res. 1978 Sep;5(9):3157–3170. doi: 10.1093/nar/5.9.3157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gustafson T. A., Miwa T., Boxer L. M., Kedes L. Interaction of nuclear proteins with muscle-specific regulatory sequences of the human cardiac alpha-actin promoter. Mol Cell Biol. 1988 Oct;8(10):4110–4119. doi: 10.1128/mcb.8.10.4110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Heberlein U., Tjian R. Temporal pattern of alcohol dehydrogenase gene transcription reproduced by Drosophila stage-specific embryonic extracts. Nature. 1988 Feb 4;331(6155):410–415. doi: 10.1038/331410a0. [DOI] [PubMed] [Google Scholar]
  13. Jaynes J. B., Johnson J. E., Buskin J. N., Gartside C. L., Hauschka S. D. The muscle creatine kinase gene is regulated by multiple upstream elements, including a muscle-specific enhancer. Mol Cell Biol. 1988 Jan;8(1):62–70. doi: 10.1128/mcb.8.1.62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kost T. A., Theodorakis N., Hughes S. H. The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Dec 10;11(23):8287–8301. doi: 10.1093/nar/11.23.8287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lassar A. B., Paterson B. M., Weintraub H. Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell. 1986 Dec 5;47(5):649–656. doi: 10.1016/0092-8674(86)90507-6. [DOI] [PubMed] [Google Scholar]
  16. Mar J. H., Ordahl C. P. A conserved CATTCCT motif is required for skeletal muscle-specific activity of the cardiac troponin T gene promoter. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6404–6408. doi: 10.1073/pnas.85.17.6404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Mohun T. J., Garrett N., Gurdon J. B. Upstream sequences required for tissue-specific activation of the cardiac actin gene in Xenopus laevis embryos. EMBO J. 1986 Dec 1;5(12):3185–3193. doi: 10.1002/j.1460-2075.1986.tb04628.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Muscat G. E., Kedes L. Multiple 5'-flanking regions of the human alpha-skeletal actin gene synergistically modulate muscle-specific expression. Mol Cell Biol. 1987 Nov;7(11):4089–4099. doi: 10.1128/mcb.7.11.4089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ordahl C. P., Cooper T. A. Strong homology in promoter and 3'-untranslated regions of chick and rat alpha-actin genes. Nature. 1983 May 26;303(5915):348–349. doi: 10.1038/303348a0. [DOI] [PubMed] [Google Scholar]
  23. Paterson B. M., Eldridge J. D. alpha-Cardiac actin is the major sarcomeric isoform expressed in embryonic avian skeletal muscle. Science. 1984 Jun 29;224(4656):1436–1438. doi: 10.1126/science.6729461. [DOI] [PubMed] [Google Scholar]
  24. Paterson B., Strohman R. C. Myosin synthesis in cultures of differentiating chicken embryo skeletal muscle. Dev Biol. 1972 Oct;29(2):113–138. doi: 10.1016/0012-1606(72)90050-4. [DOI] [PubMed] [Google Scholar]
  25. Phan-Dinh-Tuy F., Tuil D., Schweighoffer F., Pinset C., Kahn A., Minty A. The 'CC.Ar.GG' box. A protein-binding site common to transcription-regulatory regions of the cardiac actin, c-fos and interleukin-2 receptor genes. Eur J Biochem. 1988 May 2;173(3):507–515. doi: 10.1111/j.1432-1033.1988.tb14027.x. [DOI] [PubMed] [Google Scholar]
  26. Seiler-Tuyns A., Eldridge J. D., Paterson B. M. Expression and regulation of chicken actin genes introduced into mouse myogenic and nonmyogenic cells. Proc Natl Acad Sci U S A. 1984 May;81(10):2980–2984. doi: 10.1073/pnas.81.10.2980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Treisman R. Identification and purification of a polypeptide that binds to the c-fos serum response element. EMBO J. 1987 Sep;6(9):2711–2717. doi: 10.1002/j.1460-2075.1987.tb02564.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vandekerckhove J., Weber K. At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J Mol Biol. 1978 Dec 25;126(4):783–802. doi: 10.1016/0022-2836(78)90020-7. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Walsh K., Schimmel P. DNA-binding site for two skeletal actin promoter factors is important for expression in muscle cells. Mol Cell Biol. 1988 Apr;8(4):1800–1802. doi: 10.1128/mcb.8.4.1800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Wu C., Wilson S., Walker B., Dawid I., Paisley T., Zimarino V., Ueda H. Purification and properties of Drosophila heat shock activator protein. Science. 1987 Nov 27;238(4831):1247–1253. doi: 10.1126/science.3685975. [DOI] [PubMed] [Google Scholar]
  33. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]

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