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• W2071494546 abstract "We have isolated and begun characterization of the quail slow myosin heavy chain (MyHC) 3 gene, the first reported avian slow MyHC gene. Expression of slow MyHC 3 in skeletal muscle is restricted to the embryonic period of development, when the fiber pattern of future fast and slow muscle is established. In embryonic hindlimb development, slow MyHC 3 gene expression coincides with slow muscle fiber formation as distinguished by slow MyHC-specific antibody staining. In addition to expression in embryonic appendicular muscle, slow MyHC 3 is expressed continuously in the atria. Transfection of slow MyHC 3 promoter-reporter constructs into embryonic myoblasts that form slow MyHC-expressing fibers identified two regions regulating expression of this gene in skeletal muscle. The proximal promoter, containing potential muscle-specific regulatory motifs, permits expression of a reporter gene in embryonic slow muscle fibers, while a distal element, located greater than 2600 base pairs upstream, further enhances expression 3-fold. The slow muscle fiber-restricted expression of slow MyHC 3 during embryonic development, and expression of slow MyHC 3 promoter-reporter constructs in embryonic muscle fibers in vitro, makes this gene a useful marker to study the mechanism establishing the slow fiber lineage in the embryo. We have isolated and begun characterization of the quail slow myosin heavy chain (MyHC) 3 gene, the first reported avian slow MyHC gene. Expression of slow MyHC 3 in skeletal muscle is restricted to the embryonic period of development, when the fiber pattern of future fast and slow muscle is established. In embryonic hindlimb development, slow MyHC 3 gene expression coincides with slow muscle fiber formation as distinguished by slow MyHC-specific antibody staining. In addition to expression in embryonic appendicular muscle, slow MyHC 3 is expressed continuously in the atria. Transfection of slow MyHC 3 promoter-reporter constructs into embryonic myoblasts that form slow MyHC-expressing fibers identified two regions regulating expression of this gene in skeletal muscle. The proximal promoter, containing potential muscle-specific regulatory motifs, permits expression of a reporter gene in embryonic slow muscle fibers, while a distal element, located greater than 2600 base pairs upstream, further enhances expression 3-fold. The slow muscle fiber-restricted expression of slow MyHC 3 during embryonic development, and expression of slow MyHC 3 promoter-reporter constructs in embryonic muscle fibers in vitro, makes this gene a useful marker to study the mechanism establishing the slow fiber lineage in the embryo. INTRODUCTIONThe myosin heavy chain (MyHC) 1The abbreviations used are: MyHCmyosin heavy chainM-CATmuscle-CAT sequence motifMEFmyocyte-specific enhancer-binding sequence motifbpbase pair(s)kbkilobase pair(s)mAbmonoclonal antibodyCATchloramphenicol acetyltransferaseβ-galβ-galactosidaseEDembryonic day. proteins expressed in striated muscle comprise a family of isoforms, members of which can be distinguished by differences in ATPase activity (1Bárány M. J. Gen. Physiol. 1967; 50: 197-218Crossref PubMed Scopus (1375) Google Scholar, 2Reiser P.J. Greaser M.L. Moss R.L. Dev. Biol. 1988; 129: 400-407Crossref PubMed Scopus (64) Google Scholar) and antibody immunoreactivity (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 4Pierobon Bormioli S. Sartore S. Vitadello M. Schiaffino S. J. Cell Biol. 1980; 85: 672-681Crossref PubMed Scopus (137) Google Scholar, 5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar). The expression of specific MyHC isoform(s) within individual muscle fibers is primarily responsible for the rate of fiber contraction, and, for convenience, each member of the MyHC family can be assigned to either a fast or a slow class based on expression in either fast or slow contracting muscle fibers. Multiple MyHC isoforms of either the fast or slow class can be coexpressed within a single muscle fiber, and some fibers coexpress isoforms of both classes (2Reiser P.J. Greaser M.L. Moss R.L. Dev. Biol. 1988; 129: 400-407Crossref PubMed Scopus (64) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar).Numerous MyHC isoforms of the fast class have been identified in both mammalian and avian striated muscles, and genes encoding many of the fast MyHC isoforms have been isolated (7Parker-Thornburg J. Bauer B. Palermo J. Robbins J. Dev. Biol. 1992; 150: 99-107Crossref PubMed Scopus (26) Google Scholar, 8Strehler E.E. Strehler-Page M.-A. Perriard J.-C. Periasamy M. Nadal-Ginard B. J. Mol. Biol. 1986; 190: 291-317Crossref PubMed Scopus (220) Google Scholar, 9Umeda P.K. Sinha A.M. Jakovcic S. Merten S. Hsu H.-J. Subramanian K.N. Zak R. Rabinowitz M. Proc. Natl. Acad. Sci. U. S. A. 1981; 78: 2843-2847Crossref PubMed Scopus (36) Google Scholar, 10Takeda S. North D.L. Lakich M.M. Russell S.D. Whalen R.G. J. Biol. Chem. 1992; 267: 16957-16967Abstract Full Text PDF PubMed Google Scholar, 11Kropp K.E. Gulick J. Robbins J. J. Biol. Chem. 1987; 262: 16536-16545Abstract Full Text PDF PubMed Google Scholar). In mammals, the only MyHC isoform characterized in slow skeletal muscle is encoded by the β-cardiac/slow MyHC gene (12Liew C.-C. Sole M.J. Yamauchi-Takihara K. Kellam B. Anderson D.H. Lin L. Liew J.C. Nucleic Acids Res. 1990; 18: 3647-3651Crossref PubMed Scopus (106) Google Scholar, 13Mahdavi V. Chambers A.P. Nadal-Ginard B. Proc. Natl. Acad. Sci. U. S. A. 1984; 81: 2626-2630Crossref PubMed Scopus (207) Google Scholar, 14Gulick J. Subramaniam A. Neumann J. Robbins J. J. Biol. Chem. 1991; 266: 9180-9185Abstract Full Text PDF PubMed Google Scholar, 15Friedman D.J. Umeda P.K. Sinha A.M. Hsu H.-J. Jakovcic S. Rabinowitz M. Proc. Natl. Acad. Sci. U. S. A. 1984; 81: 3044-3048Crossref PubMed Scopus (21) Google Scholar), although immunological data suggests that additional slow isoforms may exist (16Hughes S.M. Cho M. Karsch-Mizrachi I. Travis M. Silberstein L. Leinwand L.A. Blau H.M. Dev. Biol. 1993; 158: 183-199Crossref PubMed Scopus (198) Google Scholar). In contrast, using electrophoretic (17Hoh J.F.Y. McGrath P.A. White R.I. Biochem. J. 1976; 157: 87-95Crossref PubMed Scopus (210) Google Scholar, 18Matsuda R. Bandman E. Strohman R.C. Differentiation. 1982; 23: 36-42Crossref PubMed Scopus (51) Google Scholar) and immunological (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 19Kennedy J.M. Kamel S. Tambone W.W. Vrbova G. Zak R. J. Cell Biol. 1986; 103: 977-983Crossref PubMed Scopus (69) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar) techniques, three distinct avian slow MyHC protein isoforms have been described, but none of the genes encoding these slow MyHCs have been previously isolated.Members of the MyHC gene family show developmental stage-specific expression, with different MyHC isoforms expressed in fibers formed during embryonic, fetal, and adult periods of myogenesis (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar, 21Bandman E. Matsuda R. Strohman R.C. Dev. Biol. 1982; 93: 508-518Crossref PubMed Scopus (142) Google Scholar). At each stage of development both intrinsic and extrinsic factors influence the pattern of MyHC isoforms expressed. An intrinsic process has been identified in birds (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 22Schafer D.A. Miller J.B. Stockdale F.E. Cell. 1987; 48: 659-670Abstract Full Text PDF PubMed Scopus (64) Google Scholar, 23DiMario J.X. Fernyak S.E. Stockdale F.E. Nature. 1993; 362: 165-167Crossref PubMed Scopus (97) Google Scholar, 24Miller R.B. Stockdale F.E. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3860-3864Crossref PubMed Scopus (155) Google Scholar) and rats (25Vivarelli E. Brown W.E. Whalen R.G. Cossu G. J. Cell Biol. 1988; 107: 2191-2197Crossref PubMed Scopus (87) Google Scholar) wherein different precursor populations of myoblasts give rise to fibers expressing either exclusively fast or both fast and slow MyHC isoforms, indicating that fibers of different types have different cellular origins. Once formed, skeletal muscle fibers may undergo a process of modulation, whereby extrinsic factors such as innervation and hormones affect changes in the MyHC isoforms expressed (26Stockdale F.E. Dev. Biol. 1992; 154: 284-298Crossref PubMed Scopus (305) Google Scholar, 27Izumo S. Nadal-Ginard B. Mahdavi V. Science. 1986; 231: 597-600Crossref PubMed Scopus (457) Google Scholar).The pattern of fast and slow fiber type distribution, evident in the anatomical muscles of the adult, is established in the limb when the first fibers, primary fibers, differentiate (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar). In both avian and mammalian limbs, this pattern can be discerned early during myogenesis by the differential expression of slow MyHC isoforms in a subset of primary muscle fibers (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 4Pierobon Bormioli S. Sartore S. Vitadello M. Schiaffino S. J. Cell Biol. 1980; 85: 672-681Crossref PubMed Scopus (137) Google Scholar, 5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar, 28Narusawa M. Fitzsimons R.B. Izumo S. Nadal-Ginard B. Rubinstein N.A. Kelly A.M. J. Cell Biol. 1987; 104: 447-459Crossref PubMed Scopus (218) Google Scholar). Based on immunopeptide mapping, the isoform designated slow MyHC 3 is the principle slow MyHC isoform expressed in slow embryonic muscle fibers of the embryonic chick limb (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar). In the limb, expression of slow MyHC 3 is largely restricted to the embryonic stage of myogenesis. As development proceeds, slow MyHC 3 is down-regulated and is replaced by the slow MyHC 1 and 2 isoforms in adult slow skeletal fibers (19Kennedy J.M. Kamel S. Tambone W.W. Vrbova G. Zak R. J. Cell Biol. 1986; 103: 977-983Crossref PubMed Scopus (69) Google Scholar). Similar slow MyHC isoform transitions may occur in mammalian muscle fibers that initially express the β-cardiac/slow gene (16Hughes S.M. Cho M. Karsch-Mizrachi I. Travis M. Silberstein L. Leinwand L.A. Blau H.M. Dev. Biol. 1993; 158: 183-199Crossref PubMed Scopus (198) Google Scholar). Thus, expression of slow MyHC 3 marks commitment of embryonic myoblasts to formation of the slow muscle fiber lineage, and an understanding of the regulation of slow MyHC 3 in the slow-fiber subset of embryonic muscle cells may provide an insight into the mechanism(s) that establishes fiber type patterning in the limbs.We have isolated and sequenced overlapping cDNA clones encoding the complete quail slow MyHC 3 message. From cDNA sequence, isoform-specific probes were used to isolate genomic clones comprising the entire slow MyHC 3 gene which was sequenced in its entirety, including greater than 2.5 kb of DNA upstream of the transcription initiation site. Northern analysis and in situ hybridization demonstrate that expression of slow MyHC 3 in developing limb muscle occurs only during the stages of development when the pattern of slow MyHC expression is established and when distinctions between the fast and slow muscle fibers first become apparent. Similar to mammalian β-cardiac/slow MyHC, quail slow MyHC 3 is also expressed in cardiac as well as slow skeletal muscle. In heart development, slow MyHC 3 is expressed initially in both the atria and ventricles, but as development proceeds, expression becomes restricted to the atria. 2Wang, G. F., Nikovits, W., Schleinitz, M., and Stockdale, F. E. (1996) J. Biol. Chem. 271, in press We have identified a region of the slow MyHC 3 promoter, capable of directing muscle-specific expression in slow MyHC-expressing myotubes following transfection into embryonic quail myoblast cultures, which provides a means of dissecting the mechanism(s) that leads to a commitment of cells to the slow muscle cell lineage.DISCUSSIONA family of myosin heavy chain genes have been identified in mammalian (7Parker-Thornburg J. Bauer B. Palermo J. Robbins J. Dev. Biol. 1992; 150: 99-107Crossref PubMed Scopus (26) Google Scholar, 8Strehler E.E. Strehler-Page M.-A. Perriard J.-C. Periasamy M. Nadal-Ginard B. J. Mol. Biol. 1986; 190: 291-317Crossref PubMed Scopus (220) Google Scholar) and avian (9Umeda P.K. Sinha A.M. Jakovcic S. Merten S. Hsu H.-J. Subramanian K.N. Zak R. Rabinowitz M. Proc. Natl. Acad. Sci. U. S. A. 1981; 78: 2843-2847Crossref PubMed Scopus (36) Google Scholar, 10Takeda S. North D.L. Lakich M.M. Russell S.D. Whalen R.G. J. Biol. Chem. 1992; 267: 16957-16967Abstract Full Text PDF PubMed Google Scholar, 11Kropp K.E. Gulick J. Robbins J. J. Biol. Chem. 1987; 262: 16536-16545Abstract Full Text PDF PubMed Google Scholar) genomes. The expression of different members of this family has been shown to be regulated in developmental stage-specific (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 21Bandman E. Matsuda R. Strohman R.C. Dev. Biol. 1982; 93: 508-518Crossref PubMed Scopus (142) Google Scholar), fiber type-specific (6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar, 53Termin A. Staron R.S. Pette D. Histochemistry. 1989; 92: 453-457Crossref PubMed Scopus (206) Google Scholar), and hormone-dependent (27Izumo S. Nadal-Ginard B. Mahdavi V. Science. 1986; 231: 597-600Crossref PubMed Scopus (457) Google Scholar) fashion. In avian skeletal muscle, three MyHC proteins of the slow class can be distinguished by differences in electrophoretic mobility, peptide maps, and reactivity with monoclonal antibodies (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 18Matsuda R. Bandman E. Strohman R.C. Differentiation. 1982; 23: 36-42Crossref PubMed Scopus (51) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar, 54Hoh J.F.Y. FEBS Lett. 1979; 98: 267-270Crossref PubMed Scopus (71) Google Scholar). Two of the slow MyHC isoforms, slow MyHC 1 and 2, are found in adult slow skeletal fibers (18Matsuda R. Bandman E. Strohman R.C. Differentiation. 1982; 23: 36-42Crossref PubMed Scopus (51) Google Scholar, 54Hoh J.F.Y. FEBS Lett. 1979; 98: 267-270Crossref PubMed Scopus (71) Google Scholar). The third, slow MyHC 3, was detected during the earliest stages of myogenesis in limb muscle (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar), and in atrial muscle throughout development (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar, 52Evans D. Miller J.B. Stockdale F.E. Dev. Biol. 1988; 127: 376-383Crossref PubMed Scopus (55) Google Scholar). This pattern of expression was reproduced by Northern blot analysis using 3′ untranslated sequence of a quail MyHC cDNA as a probe (Fig. 4). The probe does not hybridize with RNA isolated from the early post-hatch anterior latissimus dorsi muscle, a slow skeletal muscle expressing slow MyHC 1 and 2 in roughly equal proportions (19Kennedy J.M. Kamel S. Tambone W.W. Vrbova G. Zak R. J. Cell Biol. 1986; 103: 977-983Crossref PubMed Scopus (69) Google Scholar), nor does it hybridize to RNA from adult pectoralis, a fast fiber muscle (data not shown). Thus, the concordance in the spatial and temporal patterns of expression support the conclusion that the MyHC gene reported here encodes the previously identified slow MyHC 3 protein (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar). We believe that slow MyHC 3 is the first avian slow MyHC gene sequenced, and that investigation of the regulation of its expression may provide information on the origin of the slow skeletal muscle cell lineage.Organization of the Quail Slow MyHC 3 GeneBy comparing cDNA and genomic DNA nucleotide sequences, the exon/intron organization of the slow MyHC 3 gene was determined to consist of 40 exons spanning approximately 16 kb of genomic DNA. The first two exons are untranslated, with the putative ATG methionine initiator codon beginning the sequence of exon 3. The last exon of the slow MyHC 3 gene encodes six amino acids plus approximately 100 base pairs of 3′-untranslated sequence.Nucleotide sequence comparison between slow MyHC 3 and MyHC genes in the GenBank/EBI data bases showed that slow MyHC 3 is more closely related to mammalian α-cardiac and β-cardiac/slow isoforms then to the chicken embryonic fast skeletal MyHC, an isoform also expressed during primary fiber formation (6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar, 55Gulick J. Kropp K. Robbins J. J. Biochem. (Tokyo). 1987; 169: 79-84Google Scholar). Consistent with previous results based on more limited sequence (38Yutzey K.E. Rhee J.T. Bader D. Development. 1994; 120: 871-883Crossref PubMed Google Scholar), nucleotide sequence comparison does not resolve whether quail slow MyHC 3 is more likely to be an avian homologue of one or the other mammalian cardiac MyHC genes. Like the α-cardiac MyHC (56Lyons G.E. Schiaffino S. Sassoon D. Barton P. Buckingham M. J. Cell Biol. 1990; 111: 2427-2436Crossref PubMed Scopus (322) Google Scholar), the quail gene is expressed at high levels in the atria (Fig. 4B), yet similar to β-cardiac/slow MyHC (28Narusawa M. Fitzsimons R.B. Izumo S. Nadal-Ginard B. Rubinstein N.A. Kelly A.M. J. Cell Biol. 1987; 104: 447-459Crossref PubMed Scopus (218) Google Scholar, 57Lompré A.-M. Nadal-Ginard B. Mahdavi V. J. Biol. Chem. 1984; 259: 6437-6446Abstract Full Text PDF PubMed Google Scholar), the quail gene is expressed in slow skeletal muscles (Figs. 4C and 6A).The greatest divergence among MyHC proteins is found in the amino termini, and quail slow MyHC 3 amino acid sequence in this region is strikingly different from both avian fast MyHC and mammalian β-cardiac/slow MyHC isoforms (Fig. 3B). Unambiguous nucleotide sequence, obtained from both cDNA and genomic DNA clones, suggests that translation of slow MyHC 3 mRNA starts with the methionine codon at the beginning of exon 3. The sequence flanking this putative initiator codon includes both the crucial −3 (A) and +4 (G) nucleotides found in vertebrate mRNAs (58Kozak M. Nucleic Acids Res. 1987; 15: 8125-8148Crossref PubMed Scopus (4151) Google Scholar). In contrast, the various avian fast skeletal isoforms show 87-98.5% amino acid homology in this region of the molecule.Regulation of Quail Slow MyHC 3 Gene ExpressionAn examination of sequence in the slow MyHC 3 proximal promoter identified several regions of homology with previously described regulatory elements involved in muscle-specific gene expression. Interestingly, although the 290 bp immediately upstream of the transcription initiation site contains extended homology (10 consecutive nucleotides) to a region (βe2) essential for skeletal and cardiac muscle cell-specific expression of β-cardiac/slow MyHC genes (40Thompson W.R. Nadal-Ginard B. Mahdavi V. J. Biol. Chem. 1991; 266: 22678-22688Abstract Full Text PDF PubMed Google Scholar, 41Flink I.L. Edwards J.G. Bahl J.J. Liew C.-C. Sole M. Morkin E. J. Biol. Chem. 1992; 267: 9917-9924Abstract Full Text PDF PubMed Google Scholar), and significant homology with an essential MEF-2/MHox element in the mouse α-cardiac MyHC promoter (59Adolph E.A. Subramaniam A. Cserjesi P. Olson E.N. Robbins J. J. Biol. Chem. 1993; 268: 5349-5352Abstract Full Text PDF PubMed Google Scholar), this portion of the slow MyHC 3 promoter permits expression of a CAT reporter gene at a low but significant level in fibroblast cells. Transfections of the SM3CAT-290 construct, showed less than 5-fold difference in the level of CAT expression between cardiac myocyte and fibroblast cell cultures,2 and only an 8-fold difference between embryonic skeletal muscle and fibroblast cell cultures (Fig. 7B).A substantial (40-fold) difference in expression between skeletal muscle and fibroblast cells is observed when an additional 390 base pairs of the slow MyHC 3 promoter are included in the SM3CAT-680 construct. This region of the promoter contains an MEF-3 binding site motif (44Parmacek M.S. Ip H.S. Jung F. Shen T. Martin J.F. Vora A.J. Olson E.N. Leiden J.M. Mol. Cell. Biol. 1994; 14: 1870-1885Crossref PubMed Scopus (98) Google Scholar), and a consensus N-box motif (45Asakura A. Fujisawa-Sehara A. Komiya T. Nabeshima Y. Nabeshima Y.-I. Mol. Cell. Biol. 1993; 13: 7153-7162Crossref PubMed Scopus (40) Google Scholar), sequences reported to bind factors that may act as transcriptional inhibitors of contractile protein gene expression in non-muscle and myoblast cells (44Parmacek M.S. Ip H.S. Jung F. Shen T. Martin J.F. Vora A.J. Olson E.N. Leiden J.M. Mol. Cell. Biol. 1994; 14: 1870-1885Crossref PubMed Scopus (98) Google Scholar, 45Asakura A. Fujisawa-Sehara A. Komiya T. Nabeshima Y. Nabeshima Y.-I. Mol. Cell. Biol. 1993; 13: 7153-7162Crossref PubMed Scopus (40) Google Scholar, 60Sasai Y. Kageyama R. Tagawa Y. Shigemoto R. Nakanishi S. Genes Dev. 1992; 6: 2620-2634Crossref PubMed Scopus (576) Google Scholar). Thus, the MEF-3 and N-box motifs may be important elements in restricting expression of slow MyHC 3 to striated muscle. While the sequence between −680 and −290 has no demonstrable effect on expression in embryonic muscle cultures (Fig. 7B), in cardiac muscle cultures this region dramatically reduces expression when compared with a construct containing only 290 bp of the slow MyHC 3 promoter.2 Thus, sequence elements that confer high level expression of the slow MyHC 3 gene in skeletal muscle fibers appear to differ, in part, from those that are required for expression in cardiac muscle cells.Additional sequence, located more than 2.6 kb upstream of the transcription initiation site, further enhances expression of the reporter in skeletal muscle cultures (Fig. 7, SM3CAT-4500 construct). Experiments in transgenic mice have demonstrated the importance of genomic sequence located many kilobase pairs distal to the transcription initiation site for muscle-specific expression of the mouse α-cardiac MyHC gene (61Subramaniam Jones W.K. Gulick J. Wert S. Neumann J. Robbins J. J. Biol. Chem. 1991; 266: 24613-24620Abstract Full Text PDF PubMed Google Scholar).Developmental Expression of MyHC GenesDuring skeletal muscle development, a series of MyHC isoform transitions occur in which one member of the family is replaced by another. Although there is no single pattern, sequential expression of different fast MyHC isoforms has been described for all fast muscles (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 21Bandman E. Matsuda R. Strohman R.C. Dev. Biol. 1982; 93: 508-518Crossref PubMed Scopus (142) Google Scholar, 54Hoh J.F.Y. FEBS Lett. 1979; 98: 267-270Crossref PubMed Scopus (71) Google Scholar). In birds, a series of transitions in the expression of the three currently recognized slow MyHC isoforms have also been documented (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar, 54Hoh J.F.Y. FEBS Lett. 1979; 98: 267-270Crossref PubMed Scopus (71) Google Scholar). Furthermore, recent studies suggest that mammals may also express multiple slow MyHC isoforms, and that transitions may occur among various isoforms during development (16Hughes S.M. Cho M. Karsch-Mizrachi I. Travis M. Silberstein L. Leinwand L.A. Blau H.M. Dev. Biol. 1993; 158: 183-199Crossref PubMed Scopus (198) Google Scholar). A previous study of slow MyHC protein isoforms present in the early avian limb (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar), as well as results on RNA accumulation presented here (Fig. 5A), establish slow MyHC 3 as the first slow MyHC isoform expressed in limb muscles. An analysis of the time course of slow MyHC 3 expression showed a peak at around ED10, coincident with the period of maximal primary skeletal muscle fiber formation in the developing hindlimb musculature.In vitro analyses have shown that the fast and slow muscle phenotypes present in developing avian limbs arise from two distinct populations of embryonic myoblasts: those that form fibers expressing slow MyHC isoforms and those that do not (22Schafer D.A. Miller J.B. Stockdale F.E. Cell. 1987; 48: 659-670Abstract Full Text PDF PubMed Scopus (64) Google Scholar, 23DiMario J.X. Fernyak S.E. Stockdale F.E. Nature. 1993; 362: 165-167Crossref PubMed Scopus (97) Google Scholar, 24Miller R.B. Stockdale F.E. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3860-3864Crossref PubMed Scopus (155) Google Scholar). Clonal populations of embryonic myoblasts, when allowed to differentiate, give rise to homogeneous colonies in which every muscle fiber either does or does not express a slow MyHC isoform. Furthermore, when cloned embryonic myoblasts are injected into embryonic limb buds, the introduced cells form a single fiber type regardless of their final position in slow or fast muscle (23DiMario J.X. Fernyak S.E. Stockdale F.E. Nature. 1993; 362: 165-167Crossref PubMed Scopus (97) Google Scholar).Immunohistological staining of early hindlimb muscle with mAb S58 (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar), Northern blot analysis using a slow MyHC 3-specific nucleic acid probe (Fig. 4), and in situ hybridization (Fig. 6A) provide evidence that slow MyHC 3 expression in the embryonic hindlimb is limited to regions that in the adult contain slow muscle fibers. Secondary muscle fibers, which form from the second, or fetal myoblast population, emerging during the fetal phase of muscle development (ED10 to hatching), express predominately fast MyHC isoforms (24Miller R.B. Stockdale F.E. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3860-3864Crossref PubMed Scopus (155) Google Scholar). During fetal development, expression of slow MyHC 3 in the hindlimb rapidly declines as the gene is down-regulated and/or the percentage of the message decreases as a result of an increase in the amount of fast MyHC mRNA produced in newly forming secondary fibers (Fig. 5B). Together these results distinguish slow MyHC 3 as an exceptional genetic marker of commitment to the slow muscle cell lineage during the earliest stage of myogenesis in the limb.Slow MyHC 3 as a Probe for a Slow Myoblast-specific FactorBy using embryonic myoblasts isolated from ED6 hindlimbs in transfection studies, we have attempted to mimic in vitro events occurring in the early embryo. In our culture system, nearly all of the muscle fibers that form express a slow MyHC reactive with mAb S58 (Fig. 8C). Thus, it is not surprising that muscle fibers in this culture setting express slow MyHC 3 promoter-CAT reporter constructs. Double staining of SM3CAT-680-transfected hindlimb cultures with mAb S58 and a polyclonal antibody against CAT (Fig. 8, C and D), demonstrated that cis-elements in the proximal promoter of the slow MyHC 3 gene are sufficient to direct expression of the CAT reporter in embryonic skeletal muscle fibers.Using sequences in the proximal promoter as a probe, we have now begun to search for factors regulating expression of the slow MyHC 3 gene during embryonic fiber formation. The identification of MEF-3 and N-box sequence motifs in a functionally defined region of the gene, and extended homology between slow MyHC 3 and a region (βe2) essential for muscle cell-specific expression of β-cardiac/slow MyHC genes (40Thompson W.R. Nadal-Ginard B. Mahdavi V. J. Biol. Chem. 1991; 266: 22678-22688Abstract Full Text PDF PubMed Google Scholar, 41Flink I.L. Edwards J.G. Bahl J.J. Liew C.-C. Sole M. Morkin E. J. Biol. Chem. 1992; 267: 9917-9924Abstract Full Text PDF PubMed Google Scholar), suggest candidates for testing. We believe that an understanding of slow MyHC 3 gene regulation will provide clues to distinguish differences in the myoblast precursors of fast and slow fibers, and thus provide insight into the mechanism by which different muscle cell lineages are established. INTRODUCTIONThe myosin heavy chain (MyHC) 1The abbreviations used are: MyHCmyosin heavy chainM-CATmuscle-CAT sequence motifMEFmyocyte-specific enhancer-binding sequence motifbpbase pair(s)kbkilobase pair(s)mAbmonoclonal antibodyCATchloramphenicol acetyltransferaseβ-galβ-galactosidaseEDembryonic day. proteins expressed in striated muscle comprise a family of isoforms, members of which can be distinguished by differences in ATPase activity (1Bárány M. J. Gen. Physiol. 1967; 50: 197-218Crossref PubMed Scopus (1375) Google Scholar, 2Reiser P.J. Greaser M.L. Moss R.L. Dev. Biol. 1988; 129: 400-407Crossref PubMed Scopus (64) Google Scholar) and antibody immunoreactivity (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 4Pierobon Bormioli S. Sartore S. Vitadello M. Schiaffino S. J. Cell Biol. 1980; 85: 672-681Crossref PubMed Scopus (137) Google Scholar, 5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar). The expression of specific MyHC isoform(s) within individual muscle fibers is primarily responsible for the rate of fiber contraction, and, for convenience, each member of the MyHC family can be assigned to either a fast or a slow class based on expression in either fast or slow contracting muscle fibers. Multiple MyHC isoforms of either the fast or slow class can be coexpressed within a single muscle fiber, and some fibers coexpress isoforms of both classes (2Reiser P.J. Greaser M.L. Moss R.L. Dev. Biol. 1988; 129: 400-407Crossref PubMed Scopus (64) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar).Numerous MyHC isoforms of the fast class have been identified in both mammalian and avian striated muscles, and genes encoding many of the fast MyHC isoforms have been isolated (7Parker-Thornburg J. Bauer B. Palermo J. Robbins J. Dev. Biol. 1992; 150: 99-107Crossref PubMed Scopus (26) Google Scholar, 8Strehler E.E. Strehler-Page M.-A. Perriard J.-C. Periasamy M. Nadal-Ginard B. J. Mol. Biol. 1986; 190: 291-317Crossref PubMed Scopus (220) Google Scholar, 9Umeda P.K. Sinha A.M. Jakovcic S. Merten S. Hsu H.-J. Subramanian K.N. Zak R. Rabinowitz M. Proc. Natl. Acad. Sci. U. S. A. 1981; 78: 2843-2847Crossref PubMed Scopus (36) Google Scholar, 10Takeda S. North D.L. Lakich M.M. Russell S.D. Whalen R.G. J. Biol. Chem. 1992; 267: 16957-16967Abstract Full Text PDF PubMed Google Scholar, 11Kropp K.E. Gulick J. Robbins J. J. Biol. Chem. 1987; 262: 16536-16545Abstract Full Text PDF PubMed Google Scholar). In mammals, the only MyHC isoform characterized in slow skeletal muscle is encoded by the β-cardiac/slow MyHC gene (12Liew C.-C. Sole M.J. Yamauchi-Takihara K. Kellam B. Anderson D.H. Lin L. Liew J.C. Nucleic Acids Res. 1990; 18: 3647-3651Crossref PubMed Scopus (106) Google Scholar, 13Mahdavi V. Chambers A.P. Nadal-Ginard B. Proc. Natl. Acad. Sci. U. S. A. 1984; 81: 2626-2630Crossref PubMed Scopus (207) Google Scholar, 14Gulick J. Subramaniam A. Neumann J. Robbins J. J. Biol. Chem. 1991; 266: 9180-9185Abstract Full Text PDF PubMed Google Scholar, 15Friedman D.J. Umeda P.K. Sinha A.M. Hsu H.-J. Jakovcic S. Rabinowitz M. Proc. Natl. Acad. Sci. U. S. A. 1984; 81: 3044-3048Crossref PubMed Scopus (21) Google Scholar), although immunological data suggests that additional slow isoforms may exist (16Hughes S.M. Cho M. Karsch-Mizrachi I. Travis M. Silberstein L. Leinwand L.A. Blau H.M. Dev. Biol. 1993; 158: 183-199Crossref PubMed Scopus (198) Google Scholar). In contrast, using electrophoretic (17Hoh J.F.Y. McGrath P.A. White R.I. Biochem. J. 1976; 157: 87-95Crossref PubMed Scopus (210) Google Scholar, 18Matsuda R. Bandman E. Strohman R.C. Differentiation. 1982; 23: 36-42Crossref PubMed Scopus (51) Google Scholar) and immunological (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 19Kennedy J.M. Kamel S. Tambone W.W. Vrbova G. Zak R. J. Cell Biol. 1986; 103: 977-983Crossref PubMed Scopus (69) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar) techniques, three distinct avian slow MyHC protein isoforms have been described, but none of the genes encoding these slow MyHCs have been previously isolated.Members of the MyHC gene family show developmental stage-specific expression, with different MyHC isoforms expressed in fibers formed during embryonic, fetal, and adult periods of myogenesis (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar, 21Bandman E. Matsuda R. Strohman R.C. Dev. Biol. 1982; 93: 508-518Crossref PubMed Scopus (142) Google Scholar). At each stage of development both intrinsic and extrinsic factors influence the pattern of MyHC isoforms expressed. An intrinsic process has been identified in birds (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 22Schafer D.A. Miller J.B. Stockdale F.E. Cell. 1987; 48: 659-670Abstract Full Text PDF PubMed Scopus (64) Google Scholar, 23DiMario J.X. Fernyak S.E. Stockdale F.E. Nature. 1993; 362: 165-167Crossref PubMed Scopus (97) Google Scholar, 24Miller R.B. Stockdale F.E. Proc. Natl. Acad. Sci. U. S. A. 1986; 83: 3860-3864Crossref PubMed Scopus (155) Google Scholar) and rats (25Vivarelli E. Brown W.E. Whalen R.G. Cossu G. J. Cell Biol. 1988; 107: 2191-2197Crossref PubMed Scopus (87) Google Scholar) wherein different precursor populations of myoblasts give rise to fibers expressing either exclusively fast or both fast and slow MyHC isoforms, indicating that fibers of different types have different cellular origins. Once formed, skeletal muscle fibers may undergo a process of modulation, whereby extrinsic factors such as innervation and hormones affect changes in the MyHC isoforms expressed (26Stockdale F.E. Dev. Biol. 1992; 154: 284-298Crossref PubMed Scopus (305) Google Scholar, 27Izumo S. Nadal-Ginard B. Mahdavi V. Science. 1986; 231: 597-600Crossref PubMed Scopus (457) Google Scholar).The pattern of fast and slow fiber type distribution, evident in the anatomical muscles of the adult, is established in the limb when the first fibers, primary fibers, differentiate (5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar). In both avian and mammalian limbs, this pattern can be discerned early during myogenesis by the differential expression of slow MyHC isoforms in a subset of primary muscle fibers (3Miller J.B. Crow M.T. Stockdale F.E. J. Cell Biol. 1985; 101: 1643-1650Crossref PubMed Scopus (145) Google Scholar, 4Pierobon Bormioli S. Sartore S. Vitadello M. Schiaffino S. J. Cell Biol. 1980; 85: 672-681Crossref PubMed Scopus (137) Google Scholar, 5Crow M.T. Stockdale F.E. Dev. Biol. 1986; 113: 238-254Crossref PubMed Scopus (253) Google Scholar, 6Crow M.T. Stockdale F.E. Dev. Biol. 1986; 118: 333-342Crossref PubMed Scopus (91) Google Scholar, 28Narusawa M. Fitzsimons R.B. Izumo S. Nadal-Ginard B. Rubinstein N.A. Kelly A.M. J. Cell Biol. 1987; 104: 447-459Crossref PubMed Scopus (218) Google Scholar). Based on immunopeptide mapping, the isoform designated slow MyHC 3 is the principle slow MyHC isoform expressed in slow embryonic muscle fibers of the embryonic chick limb (20Page S. Miller J.B. DiMario J.X. Hager E.J. Moser A. Stockdale F.E. Dev. Biol. 1992; 154: 118-128Crossref PubMed Scopus (54) Google Scholar). In the limb, expression of slow MyHC 3 is largely restricted to the embryonic stage of myogenesis. As development proceeds, slow MyHC 3 is down-regulated and is replaced by the slow MyHC 1 and 2 isoforms in adult slow skeletal fibers (19Kennedy J.M. Kamel S. Tambone W.W. Vrbova G. Zak R. J. Cell Biol. 1986; 103: 977-983Crossref PubMed Scopus (69) Google Scholar). Similar slow MyHC isoform transitions may occur in mammalian muscle fibers that initially express the β-cardiac/slow gene (16Hughes S.M. Cho M. Karsch-Mizrachi I. Travis M. Silberstein L. Leinwand L.A. Blau H.M. Dev. Biol. 1993; 158: 183-199Crossref PubMed Scopus (198) Google Scholar). Thus, expression of slow MyHC 3 marks commitment of embryonic myoblasts to formation of the slow muscle fiber lineage, and an understanding of the regulation of slow MyHC 3 in the slow-fiber subset of embryonic muscle cells may provide an insight into the mechanism(s) that establishes fiber type patterning in the limbs.We have isolated and sequenced overlapping cDNA clones encoding the complete quail slow MyHC 3 message. From cDNA sequence, isoform-specific probes were used to isolate genomic clones comprising the entire slow MyHC 3 gene which was sequenced in its entirety, including greater than 2.5 kb of DNA upstream of the transcription initiation site. Northern analysis and in situ hybridization demonstrate that expression of slow MyHC 3 in developing limb muscle occurs only during the stages of development when the pattern of slow MyHC expression is established and when distinctions between the fast and slow muscle fibers first become apparent. Similar to mammalian β-cardiac/slow MyHC, quail slow MyHC 3 is also expressed in cardiac as well as slow skeletal muscle. In heart development, slow MyHC 3 is expressed initially in both the atria and ventricles, but as development proceeds, expression becomes restricted to the atria. 2Wang, G. F., Nikovits, W., Schleinitz, M., and Stockdale, F. E. (1996) J. Biol. Chem. 271, in press We have identified a region of the slow MyHC 3 promoter, capable of directing muscle-specific expression in slow MyHC-expressing myotubes following transfection into embryonic quail myoblast cultures, which provides a means of dissecting the mechanism(s) that leads to a commitment of cells to the slow muscle cell lineage." @default.
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• W2071494546 title "Isolation and Characterization of an Avian Slow Myosin Heavy Chain Gene Expressed during Embryonic Skeletal Muscle Fiber Formation" @default.
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