Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1988 Oct;8(10):4134–4142. doi: 10.1128/mcb.8.10.4134

Expression of the troponin complex genes: transcriptional coactivation during myoblast differentiation and independent control in heart and skeletal muscles.

E A Bucher 1, P C Maisonpierre 1, S F Konieczny 1, C P Emerson Jr 1
PMCID: PMC365482  PMID: 3185544

Abstract

We compared the developmental regulation of the three troponin genes that encode the proteins of the Ca2+ regulatory complex in striated muscles of the Japanese quail. Nuclear run-on transcription and RNA protection analyses showed that the fast skeletal troponin I, the fast skeletal troponin T, and the slow skeletal-cardiac troponin C genes were transcriptionally coactivated and that transcripts rapidly accumulated within 6 to 12 h after the initiation of myoblast differentiation. The fast-isoform mRNAs of troponin I and troponin T were coexpressed at similar levels in different skeletal muscles, whereas the slow-cardiac troponin C mRNA varied independently and was the only one of these genes expressed in embryonic and adult heart. We conclude that these troponin genes are transcriptionally coactivated during skeletal myoblast differentiation, indicating that their transcription is under precise temporal control. However, this troponin C gene is regulated independently is specialized striated muscles.

Full text

PDF
4134

Images in this article

4137Image
on p.4137
4138Image
on p.4138
4139Image
on p.4139
4140Image
on p.4140

Selected References

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

  1. Affara N. A., Robert B., Jacquet M., Buckingham M. E., Gros F. Changes in gene expression during myogenic differentiation. I. Regulation of messenger RNA sequences expressed during myotube formation. J Mol Biol. 1980 Jul 15;140(4):441–458. doi: 10.1016/0022-2836(80)90264-8. [DOI] [PubMed] [Google Scholar]
  2. BULLER A. J., ECCLES J. C., ECCLES R. M. Differentiation of fast and slow muscles in the cat hind limb. J Physiol. 1960 Feb;150:399–416. doi: 10.1113/jphysiol.1960.sp006394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baldwin A. S., Jr, Kittler E. L., Emerson C. P., Jr Structure, evolution, and regulation of a fast skeletal muscle troponin I gene. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8080–8084. doi: 10.1073/pnas.82.23.8080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barnard E. A., Lyles J. M., Pizzey J. A. Fibre types in chicken skeletal muscles and their changes in muscular dystrophy. J Physiol. 1982 Oct;331:333–354. doi: 10.1113/jphysiol.1982.sp014375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bender T. P., Thompson C. B., Kuehl W. M. Differential expression of c-myb mRNA in murine B lymphomas by a block to transcription elongation. Science. 1987 Sep 18;237(4821):1473–1476. doi: 10.1126/science.3498214. [DOI] [PubMed] [Google Scholar]
  6. Bowman L. H., Emerson C. P., Jr Post-transcriptional regulation of ribosome accumulation during myoblast differentiation. Cell. 1977 Apr;10(4):587–596. doi: 10.1016/0092-8674(77)90091-5. [DOI] [PubMed] [Google Scholar]
  7. Britten R. J., Davidson E. H. Gene regulation for higher cells: a theory. Science. 1969 Jul 25;165(3891):349–357. doi: 10.1126/science.165.3891.349. [DOI] [PubMed] [Google Scholar]
  8. Buonanno A., Merlie J. P. Transcriptional regulation of nicotinic acetylcholine receptor genes during muscle development. J Biol Chem. 1986 Sep 5;261(25):11452–11455. [PubMed] [Google Scholar]
  9. Carmon Y., Czosnek H., Nudel U., Shani M., Yaffe D. DNAase I sensitivity of genes expressed during myogenesis. Nucleic Acids Res. 1982 May 25;10(10):3085–3098. doi: 10.1093/nar/10.10.3085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cooper T. A., Ordahl C. P. A single troponin T gene regulated by different programs in cardiac and skeletal muscle development. Science. 1984 Nov 23;226(4677):979–982. doi: 10.1126/science.6095446. [DOI] [PubMed] [Google Scholar]
  11. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Devlin R. B., Emerson C. P., Jr Coordinate regulation of contractile protein synthesis during myoblast differentiation. Cell. 1978 Apr;13(4):599–611. doi: 10.1016/0092-8674(78)90211-8. [DOI] [PubMed] [Google Scholar]
  14. Dhoot G. K., Frearson N., Perry S. V. Polymorphic forms of troponin T and troponin C and their localization in striated muscle cell types. Exp Cell Res. 1979 Sep;122(2):339–350. doi: 10.1016/0014-4827(79)90310-0. [DOI] [PubMed] [Google Scholar]
  15. Dhoot G. K., Perry S. V. Distribution of polymorphic forms of troponin components and tropomyosin in skeletal muscle. Nature. 1979 Apr 19;278(5706):714–718. doi: 10.1038/278714a0. [DOI] [PubMed] [Google Scholar]
  16. Emerson C. P., Jr, Beckner S. K. Activation of myosin synthesis in fusing and mononucleated myoblasts. J Mol Biol. 1975 Apr 25;93(4):431–447. doi: 10.1016/0022-2836(75)90238-7. [DOI] [PubMed] [Google Scholar]
  17. Gahlmann R., Troutt A. B., Wade R. P., Gunning P., Kedes L. Alternative splicing generates variants in important functional domains of human slow skeletal troponin T. J Biol Chem. 1987 Nov 25;262(33):16122–16126. [PubMed] [Google Scholar]
  18. Garfinkel L. I., Davidson N. Developmentally regulated expression of a truncated myosin light-chain 1F/3F gene. Mol Cell Biol. 1987 Oct;7(10):3826–3829. doi: 10.1128/mcb.7.10.3826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Gustafson T. A., Markham B. E., Bahl J. J., Morkin E. Thyroid hormone regulates expression of a transfected alpha-myosin heavy-chain fusion gene in fetal heart cells. Proc Natl Acad Sci U S A. 1987 May;84(10):3122–3126. doi: 10.1073/pnas.84.10.3122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hallauer P. L., Hastings K. E., Baldwin A. S., Pearson-White S., Merrifield P. A., Emerson C. P., Jr Closely related alpha-tropomyosin mRNAs in quail fibroblasts and skeletal muscle cells. J Biol Chem. 1987 Mar 15;262(8):3590–3596. [PubMed] [Google Scholar]
  23. Hastings K. E., Bucher E. A., Emerson C. P., Jr Generation of troponin T isoforms by alternative RNA splicing in avian skeletal muscle. Conserved and divergent features in birds and mammals. J Biol Chem. 1985 Nov 5;260(25):13699–13703. [PubMed] [Google Scholar]
  24. Hastings K. E., Emerson C. P., Jr cDNA clone analysis of six co-regulated mRNAs encoding skeletal muscle contractile proteins. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1553–1557. doi: 10.1073/pnas.79.5.1553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jaynes J. B., Chamberlain J. S., Buskin J. N., Johnson J. E., Hauschka S. D. Transcriptional regulation of the muscle creatine kinase gene and regulated expression in transfected mouse myoblasts. Mol Cell Biol. 1986 Aug;6(8):2855–2864. doi: 10.1128/mcb.6.8.2855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Konieczny S. F., Emerson C. P., Jr Complex regulation of the muscle-specific contractile protein (troponin I) gene. Mol Cell Biol. 1987 Sep;7(9):3065–3075. doi: 10.1128/mcb.7.9.3065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Konieczny S. F., Emerson C. P., Jr Differentiation, not determination, regulates muscle gene activation: transfection of troponin I genes into multipotential and muscle lineages of 10T1/2 cells. Mol Cell Biol. 1985 Sep;5(9):2423–2432. doi: 10.1128/mcb.5.9.2423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Konigsberg I. R. Diffusion-mediated control of myoblast fusion. Dev Biol. 1971 Sep;26(1):133–152. doi: 10.1016/0012-1606(71)90113-8. [DOI] [PubMed] [Google Scholar]
  30. Konigsberg I. R. Skeletal myoblasts in culture. Methods Enzymol. 1979;58:511–527. doi: 10.1016/s0076-6879(79)58166-x. [DOI] [PubMed] [Google Scholar]
  31. Maisonpierre P. C., Hastings K. E., Emerson C. P., Jr The cloning and the codon and amino acid sequence of the quail slow/cardiac troponin C cDNA. Methods Enzymol. 1987;139:326–337. doi: 10.1016/0076-6879(87)39096-2. [DOI] [PubMed] [Google Scholar]
  32. Matsuda R., Obinata T., Shimada Y. Types of troponin components during development of chicken skeletal muscle. Dev Biol. 1981 Feb;82(1):11–19. doi: 10.1016/0012-1606(81)90424-3. [DOI] [PubMed] [Google Scholar]
  33. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. McKnight G. S., Palmiter R. D. Transcriptional regulation of the ovalbumin and conalbumin genes by steroid hormones in chick oviduct. J Biol Chem. 1979 Sep 25;254(18):9050–9058. [PubMed] [Google Scholar]
  35. Medford R. M., Nguyen H. T., Nadal-Ginard B. Transcriptional and cell cycle-mediated regulation of myosin heavy chain gene expression during muscle cell differentiation. J Biol Chem. 1983 Sep 25;258(18):11063–11073. [PubMed] [Google Scholar]
  36. 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]
  37. Mikawa T., Takeda S., Shimizu T., Kitaura T. Gene expression of myofibrillar proteins in single muscle fibers of adult chicken: micro two dimensional gel electrophoretic analysis. J Biochem. 1981 Jun;89(6):1951–1962. doi: 10.1093/oxfordjournals.jbchem.a133397. [DOI] [PubMed] [Google Scholar]
  38. Milner R. J., Brow M. D., Cleveland D. W., Shinnick T. M., Sutcliffe J. G. Glyceraldehyde 3-phosphate dehydrogenase protein and mRNA are both differentially expressed in adult chickens but not chick embryos. Nucleic Acids Res. 1983 May 25;11(10):3301–3315. doi: 10.1093/nar/11.10.3301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. 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]
  41. Pearlstone J. R., Carpenter M. R., Johnson P., Smillie L. B. Amino-acid sequence of tropomyosin-binding component of rabbit skeletal muscle troponin. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1902–1906. doi: 10.1073/pnas.73.6.1902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pearson-White S. H., Emerson C. P., Jr A novel hybrid alpha-tropomyosin in fibroblasts is produced by alternative splicing of transcripts from the skeletal muscle alpha-tropomyosin gene. J Biol Chem. 1987 Nov 25;262(33):15998–16010. [PubMed] [Google Scholar]
  43. Phillips W. D., Bennett M. R. Differentiation of fiber types in wing muscles during embryonic development: effect of neural tube removal. Dev Biol. 1984 Dec;106(2):457–468. doi: 10.1016/0012-1606(84)90245-8. [DOI] [PubMed] [Google Scholar]
  44. Shani M., Dekel I., Yoffe O. Expression of the rat myosin light-chain 2 gene in transgenic mice: stage specificity, developmental regulation, and interrelation with the endogenous gene. Mol Cell Biol. 1988 Feb;8(2):1006–1009. doi: 10.1128/mcb.8.2.1006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. 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]
  46. Shani M., Zevin-Sonkin D., Saxel O., Carmon Y., Katcoff D., Nudel U., Yaffe D. The correlation between the synthesis of skeletal muscle actin, myosin heavy chain, and myosin light chain and the accumulation of corresponding mRNA sequences during myogenesis. Dev Biol. 1981 Sep;86(2):483–492. doi: 10.1016/0012-1606(81)90206-2. [DOI] [PubMed] [Google Scholar]
  47. Taubman M. B., Grant J. W., Nadal-Ginard B. Cloning and characterization of mammalian myosin regulatory light chain (RLC) cDNA: the RLC gene is expressed in smooth, sarcomeric, and nonmuscle tissues. J Cell Biol. 1987 Jun;104(6):1505–1513. doi: 10.1083/jcb.104.6.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Toyota N., Shimada Y. Differentiation of troponin in cardiac and skeletal muscles in chicken embryos as studied by immunofluorescence microscopy. J Cell Biol. 1981 Nov;91(2 Pt 1):497–504. doi: 10.1083/jcb.91.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Toyota N., Shimada Y. Isoform variants of troponin in skeletal and cardiac muscle cells cultured with and without nerves. Cell. 1983 May;33(1):297–304. doi: 10.1016/0092-8674(83)90358-6. [DOI] [PubMed] [Google Scholar]
  50. Vrbová G., Navarrete R., Lowrie M. Matching of muscle properties and motoneurone firing patterns during early stages of development. J Exp Biol. 1985 Mar;115:113–123. doi: 10.1242/jeb.115.1.113. [DOI] [PubMed] [Google Scholar]
  51. Wilkinson J. M., Grand R. J. Comparison of amino acid sequence of troponin I from different striated muscles. Nature. 1978 Jan 5;271(5640):31–35. doi: 10.1038/271031a0. [DOI] [PubMed] [Google Scholar]
  52. Wilkinson J. M. Troponin C from rabbit slow skeletal and cardiac muscle is the product of a single gene. Eur J Biochem. 1980 Jan;103(1):179–188. doi: 10.1111/j.1432-1033.1980.tb04302.x. [DOI] [PubMed] [Google Scholar]
  53. Yates L. D., Greaser M. L. Troponin subunit stoichiometry and content in rabbit skeletal muscle and myofibrils. J Biol Chem. 1983 May 10;258(9):5770–5774. [PubMed] [Google Scholar]
  54. Zot A. S., Potter J. D. Structural aspects of troponin-tropomyosin regulation of skeletal muscle contraction. Annu Rev Biophys Biophys Chem. 1987;16:535–559. doi: 10.1146/annurev.bb.16.060187.002535. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES