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J Cell Biol. 1986 Apr 1; 102(4): 1485–1493.
PMCID: PMC2114155

Sequential expression of chicken actin genes during myogenesis


Embryonic muscle development permits the study of contractile protein gene regulation during cellular differentiation. To distinguish the appearance of particular actin mRNAs during chicken myogenesis, we have constructed DNA probes from the transcribed 3' noncoding region of the single-copy alpha-skeletal, alpha-cardiac, and beta-cytoplasmic actin genes. Hybridization experiments showed that at day 10 in ovo (stage 36), embryonic hindlimbs contain low levels of actin mRNA, predominantly consisting of the alpha-cardiac and beta-actin isotypes. However, by day 17 in ovo (stage 43), the amount of alpha-skeletal actin mRNA/microgram total RNA increased more than 30-fold and represented approximately 90% of the assayed actin mRNA. Concomitantly, alpha-cardiac and beta-actin mRNAs decreased by 30% and 70%, respectively, from the levels observed at day 10. In primary myoblast cultures, beta-actin mRNA increased sharply during the proliferative phase before fusion and steadily declined thereafter. alpha-Cardiac actin mRNA increased to levels 15-fold greater than alpha-skeletal actin mRNA in prefusion myoblasts (36 h), and remained at elevated levels. In contrast, the alpha-skeletal actin mRNA remained low until fusion had begun (48 h), increased 25-fold over the prefusion level by the completion of fusion, and then decreased at later times in culture. Thus, the sequential accumulation of sarcomeric alpha-actin mRNAs in culture mimics some of the events observed in embryonic limb development. However, maintenance of high levels of alpha-cardiac actin mRNA as well as the transient accumulation of appreciable alpha- skeletal actin mRNA suggests that myoblast cultures lack one or more essential components for phenotypic maturation.

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Selected References

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  • Bains W, Ponte P, Blau H, Kedes L. Cardiac actin is the major actin gene product in skeletal muscle cell differentiation in vitro. Mol Cell Biol. 1984 Aug;4(8):1449–1453. [PMC free article] [PubMed]
  • Bergsma DJ, Chang KS, Schwartz RJ. Novel chicken actin gene: third cytoplasmic isoform. Mol Cell Biol. 1985 May;5(5):1151–1162. [PMC free article] [PubMed]
  • Blau HM, Pavlath GK, Hardeman EC, Chiu CP, Silberstein L, Webster SG, Miller SC, Webster C. Plasticity of the differentiated state. Science. 1985 Nov 15;230(4727):758–766. [PubMed]
  • Breitbart RE, Nguyen HT, Medford RM, Destree AT, Mahdavi V, Nadal-Ginard B. Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell. 1985 May;41(1):67–82. [PubMed]
  • Cahn RD, Zwilling E, Kaplan NO, Levine L. Nature and Development of Lactic Dehydrogenases: The two major types of this enzyme form molecular hybrids which change in makeup during development. Science. 1962 Jun 15;136(3520):962–969. [PubMed]
  • Caplan AI, Fiszman MY, Eppenberger HM. Molecular and cell isoforms during development. Science. 1983 Sep 2;221(4614):921–927. [PubMed]
  • Chamberlin ME, Galau GA, Britten RJ, Davidson EH. Studies on nucleic acid reassociation kinetics: V. Effects of disparity in tracer and driver fragment lengths. Nucleic Acids Res. 1978 Jun;5(6):2073–2094. [PMC free article] [PubMed]
  • Chang KS, Zimmer WE, Jr, Bergsma DJ, Dodgson JB, Schwartz RJ. Isolation and characterization of six different chicken actin genes. Mol Cell Biol. 1984 Nov;4(11):2498–2508. [PMC free article] [PubMed]
  • Chang KS, Rothblum KN, Schwartz RJ. 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. [PMC free article] [PubMed]
  • Cleveland DW, Lopata MA, MacDonald RJ, Cowan NJ, Rutter WJ, Kirschner MW. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. [PubMed]
  • Fischbach GD. Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev Biol. 1972 Jun;28(2):407–429. [PubMed]
  • Fornwald JA, Kuncio G, Peng I, Ordahl CP. 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. [PMC free article] [PubMed]
  • Greenberg ME, Ziff EB. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. [PubMed]
  • Gunning P, Ponte P, Blau H, Kedes L. alpha-skeletal and alpha-cardiac actin genes are coexpressed in adult human skeletal muscle and heart. Mol Cell Biol. 1983 Nov;3(11):1985–1995. [PMC free article] [PubMed]
  • Hamada H, Petrino MG, Kakunaga T. Molecular structure and evolutionary origin of human cardiac muscle actin gene. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5901–5905. [PMC free article] [PubMed]
  • Herrmann H, Heywood SM, Marchok AC. Reconstruction of muscle development as a sequence of macromolecular synthesis. Curr Top Dev Biol. 1970;5:181–234. [PubMed]
  • Katz L, Williams PH, Sato S, Leavitt RW, Helinski DR. Purification and characterization of covalently closed replicative intermediates of ColEl DNA from Escherichia coli. Biochemistry. 1977 Apr 19;16(8):1677–1683. [PubMed]
  • KONIGSBERG IR. Clonal analysis of myogenesis. Science. 1963 Jun 21;140(3573):1273–1284. [PubMed]
  • Kost TA, Theodorakis N, Hughes SH. The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nucleic Acids Res. 1983 Dec 10;11(23):8287–8301. [PMC free article] [PubMed]
  • Matsuda R, Spector DH, Strohman RC. Regenerating adult chicken skeletal muscle and satellite cell cultures express embryonic patterns of myosin and tropomyosin isoforms. Dev Biol. 1983 Dec;100(2):478–488. [PubMed]
  • Mayer Y, Czosnek H, Zeelon PE, Yaffe D, Nudel U. Expression of the genes coding for the skeletal muscle and cardiac actions in the heart. Nucleic Acids Res. 1984 Jan 25;12(2):1087–1100. [PMC free article] [PubMed]
  • McMaster GK, Carmichael GG. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. [PMC free article] [PubMed]
  • Medford RM, Nguyen HT, 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]
  • Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. [PubMed]
  • Minty AJ, Alonso S, Caravatti M, Buckingham ME. A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell. 1982 Aug;30(1):185–192. [PubMed]
  • Mohun TJ, Brennan S, Dathan N, Fairman S, Gurdon JB. Cell type-specific activation of actin genes in the early amphibian embryo. Nature. 1984 Oct 25;311(5988):716–721. [PubMed]
  • Moss M, Schwartz R. Regulation of tropomyosin gene expression during myogenesis. Mol Cell Biol. 1981 Mar;1(3):289–301. [PMC free article] [PubMed]
  • Nguyen HT, Medford RM, Nadal-Ginard B. Reversibility of muscle differentiation in the absence of commitment: analysis of a myogenic cell line temperature-sensitive for commitment. Cell. 1983 Aug;34(1):281–293. [PubMed]
  • Palmiter RD. Magnesium precipitation of ribonucleoprotein complexes. Expedient techniques for the isolation of undergraded polysomes and messenger ribonucleic acid. Biochemistry. 1974 Aug 13;13(17):3606–3615. [PubMed]
  • Paterson BM, Eldridge JD. alpha-Cardiac actin is the major sarcomeric isoform expressed in embryonic avian skeletal muscle. Science. 1984 Jun 29;224(4656):1436–1438. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schwartz RJ, Haron JA, Rothblum KN, Dugaiczyk A. Regulation of muscle differentiation: cloning of sequences from alpha-actin messenger ribonucleic acid. Biochemistry. 1980 Dec 9;19(25):5883–5890. [PubMed]
  • Schwartz RJ, Rothblum KN. Gene switching in myogenesis: differential expression of the chicken actin multigene family. Biochemistry. 1981 Jul 7;20(14):4122–4129. [PubMed]
  • Schwartz RJ, Stone EM. Cloning of contractile protein genes. Cell Muscle Motil. 1983;3:195–257. [PubMed]
  • Southern EM. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. [PubMed]
  • Strohman RC, Micou-Eastwood J, Glass CA, Matsuda R. Human fetal muscle and cultured myotubes derived from it contain a fetal-specific myosin light chain. Science. 1983 Sep 2;221(4614):955–957. [PubMed]
  • Thomas PS. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. [PMC free article] [PubMed]
  • Thomas PS. Hybridization of denatured RNA transferred or dotted nitrocellulose paper. Methods Enzymol. 1983;100:255–266. [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • 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. [PubMed]
  • Vandekerckhove J, Weber K. Actin typing on total cellular extracts: a highly sensitive protein-chemical procedure able to distinguish different actins. Eur J Biochem. 1981 Jan;113(3):595–603. [PubMed]
  • 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. [PubMed]
  • Whalen RG, Sell SM, Eriksson A, Thornell LE. Myosin subunit types in skeletal and cardiac tissues and their developmental distribution. Dev Biol. 1982 Jun;91(2):478–484. [PubMed]
  • White BA, Bancroft FC. Cytoplasmic dot hybridization. Simple analysis of relative mRNA levels in multiple small cell or tissue samples. J Biol Chem. 1982 Aug 10;257(15):8569–8572. [PubMed]
  • Yaffe D, Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. [PubMed]

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