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. 1985 Dec;82(23):8080–8084. doi: 10.1073/pnas.82.23.8080

Structure, evolution, and regulation of a fast skeletal muscle troponin I gene.

A S Baldwin Jr, E L Kittler, C P Emerson Jr
PMCID: PMC391446  PMID: 3865218

Abstract

The complete structure of a quail fast skeletal muscle troponin I gene was determined by nucleotide sequence comparison of troponin I genomic and cDNA sequences. This 4.5-kilobase troponin I gene has eight exons. The actin-binding domain of troponin I is encoded by a single exon, whereas the troponin C-binding domain is split into at least two exons. The exon organization of the fast troponin I gene suggests that gene conversion directs the nonrandom conservation of the carboxyl-terminal halves of troponin I isoforms and that the amino-terminal extension of the cardiac isoform originated by splice-junction sliding. Comparison of the structure of the troponin I gene with the structures of other contractile protein genes reveals homologous sequences in their 5' flanking regions and similar large introns that separate protein-coding exons from 5' nontranslated exons. These common structural features may function to coordinate the activation of contractile-protein genes 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. Baltimore D. Gene conversion: some implications for immunoglobulin genes. Cell. 1981 Jun;24(3):592–594. doi: 10.1016/0092-8674(81)90082-9. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Craik C. S., Rutter W. J., Fletterick R. Splice junctions: association with variation in protein structure. Science. 1983 Jun 10;220(4602):1125–1129. doi: 10.1126/science.6344214. [DOI] [PubMed] [Google Scholar]
  7. Davidson E. H., Jacobs H. T., Britten R. J. Very short repeats and coordinate induction of genes. Nature. 1983 Feb 10;301(5900):468–470. doi: 10.1038/301468a0. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Gilbert W. Why genes in pieces? Nature. 1978 Feb 9;271(5645):501–501. doi: 10.1038/271501a0. [DOI] [PubMed] [Google Scholar]
  11. Grez M., Land H., Giesecke K., Schütz G., Jung A., Sippel A. E. Multiple mRNAs are generated from the chicken lysozyme gene. Cell. 1981 Sep;25(3):743–752. doi: 10.1016/0092-8674(81)90182-3. [DOI] [PubMed] [Google Scholar]
  12. Head J. F., Perry S. V. The interaction of the calcium-binding protein (troponin C) with bivalent cations and the inhibitory protein (troponin I). Biochem J. 1974 Feb;137(2):145–154. doi: 10.1042/bj1370145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Horwitz J., Bullard B., Mercola D. Interaction of troponin subunits. The interaction between the inhibitory and tropomyosin-binding subunits. J Biol Chem. 1979 Jan 25;254(2):350–355. [PubMed] [Google Scholar]
  14. Jung A., Sippel A. E., Grez M., Schütz G. Exons encode functional and structural units of chicken lysozyme. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5759–5763. doi: 10.1073/pnas.77.10.5759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Lawn R. M., Fritsch E. F., Parker R. C., Blake G., Maniatis T. The isolation and characterization of linked delta- and beta-globin genes from a cloned library of human DNA. Cell. 1978 Dec;15(4):1157–1174. doi: 10.1016/0092-8674(78)90043-0. [DOI] [PubMed] [Google Scholar]
  17. Mahdavi V., Chambers A. P., Nadal-Ginard B. Cardiac alpha- and beta-myosin heavy chain genes are organized in tandem. Proc Natl Acad Sci U S A. 1984 May;81(9):2626–2630. doi: 10.1073/pnas.81.9.2626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. 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]
  22. 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]
  23. Naora H., Deacon N. J. Relationship between the total size of exons and introns in protein-coding genes of higher eukaryotes. Proc Natl Acad Sci U S A. 1982 Oct;79(20):6196–6200. doi: 10.1073/pnas.79.20.6196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nudel U., Calvo J. M., Shani M., Levy Z. The nucleotide sequence of a rat myosin light chain 2 gene. Nucleic Acids Res. 1984 Sep 25;12(18):7175–7186. doi: 10.1093/nar/12.18.7175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Pelham H. R. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell. 1982 Sep;30(2):517–528. doi: 10.1016/0092-8674(82)90249-5. [DOI] [PubMed] [Google Scholar]
  27. Potter J. D., Gergely J. Troponin, tropomyosin, and actin interactions in the Ca2+ regulation of muscle contraction. Biochemistry. 1974 Jun 18;13(13):2697–2703. doi: 10.1021/bi00710a007. [DOI] [PubMed] [Google Scholar]
  28. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  29. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  30. Sharp P. A. Speculations on RNA splicing. Cell. 1981 Mar;23(3):643–646. doi: 10.1016/0092-8674(81)90425-6. [DOI] [PubMed] [Google Scholar]
  31. Slightom J. L., Blechl A. E., Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. doi: 10.1016/0092-8674(80)90426-2. [DOI] [PubMed] [Google Scholar]
  32. Solaro R. J., Moir A. J., Perry S. V. Phosphorylation of troponin I and the inotropic effect of adrenaline in the perfused rabbit heart. Nature. 1976 Aug 12;262(5569):615–617. doi: 10.1038/262615a0. [DOI] [PubMed] [Google Scholar]
  33. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  34. Steinmetz M., Moore K. W., Frelinger J. G., Sher B. T., Shen F. W., Boyse E. A., Hood L. A pseudogene homologous to mouse transplantation antigens: transplantation antigens are encoded by eight exons that correlate with protein domains. Cell. 1981 Sep;25(3):683–692. doi: 10.1016/0092-8674(81)90175-6. [DOI] [PubMed] [Google Scholar]
  35. Tate V. E., Finer M. H., Boedtker H., Doty P. Chick pro alpha 2 (I) collagen gene: exon location and coding potential for the prepropeptide. Nucleic Acids Res. 1983 Jan 11;11(1):91–104. doi: 10.1093/nar/11.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. 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]
  38. Wilkinson J. M., Perry S. V., Cole H. A., Trayer I. P. The regulatory proteins of the myofibril. Separation and biological activity of the components of inhibitory-factor preparations. Biochem J. 1972 Mar;127(1):215–228. doi: 10.1042/bj1270215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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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