Alternative RNA Splicing Generates Transcripts Encoding a Thorax-Specific Isoform of Drosophila melanogaster Myosin Heavy Chain

LITERATURE CITED

• Barany, M. 1967. ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 50:197–218.
   PubMed Web of Science ®Google Scholar
• Benoit, R., P. Daubas, M.-A. Akimenko, A. Cohen, I. Garner, J.-L. Guenet, and M. Buckingham. 1984. A single locus in the mouse encodes both myosin light chains 1 and 3, a second locus corresponds to a related pseudogene. Cell 39:129–140.
   PubMedGoogle Scholar
• Benyajati, C., A. R. Place, D. A. Powers, and W. Sofer. 1981. Alcohol dehydrogenase gene of Drosophila melanogaster: relationship of intervening sequences to functional domains in the protein. Proc. Natl. Acad. Sci. USA 78:2717–2721.
   PubMedGoogle Scholar
• Benyajati, C., N. Spoerel, H. Haymerle, and M. Ashburner. 1983. The messenger RNA for alcohol dehydrogenase in Drosophila melanogaster differs in its 5′ end in different developmental stages. Cell 33:125–133.
   PubMed Web of Science ®Google Scholar
• Bernstein, S. I., and J. J. Donady. 1980. RNA synthesis and coding capacity of polyadenylated and nonpolyadenylated mRNA from cultures of differentiating Drosophila melanogaster myoblasts. Dev. Biol. 79:388–398.
   PubMed Web of Science ®Google Scholar
• Bernstein, S. I., E. A. Fyrberg, and J. J. Donady. 1978. Isolation and partial characterization of Drosophila myoblasts from primary cultures of embryonic cells. J. Cell Biol. 78:856–865.
   PubMed Web of Science ®Google Scholar
• Bernstein, S. I., K. Mogami, J. J. Donady, and C. P. Emerson, Jr. 1983. Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations. Nature (London) 302:393–397.
   PubMedGoogle Scholar
• Breitbart, R. E., H. T. Nguyen, R. M. Medford, A. T. Destree, V. Mahdavi, and B. Nadal-Ginard. 1985. Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell 41:67–82.
   PubMedGoogle Scholar
• Collins, J. H., G. P. Cote, and E. D. Korn. 1982. Localization of the three phosphorylation sites on each heavy chain of Acanthamoeba myosin II to a segment at the end of the tail. J. Biol. Chem. 257:4529–4534.
   PubMedGoogle Scholar
• Cooper, T. A., and C. P. Ordahl. 1985. A single cardiac troponin T gene generates embryonic and adult isoforms via developmentally regulated alternate splicing. J. Biol. Chem. 260:11140–11148.
   PubMed Web of Science ®Google Scholar
• Crossley, A. C. 1978. The morphology and development of the Drosophila muscular system, p. 499–560. In M. Ashburner and T. R. F. Wright (ed.), The genetics and biology of Drosophila, vol. 2b. Academic Press, Inc. (London), Ltd., London.
   Google Scholar
• Deutscher, S. L., B. M. Bhat, M. H. Pursley, C. Cladaras, and W. S. M. Wold. 1985. Novel deletion mutants that enhance a distant upstream 5′ splice in the E3 transcription unit of adenovirus 2. Nucleic Acids Res. 13:5771–5787.
   PubMedGoogle Scholar
• Dibb, N. J., D. M. Brown, J. Karn, D. G. Moerman, S. L. Bolten, and R. H. Waterston. 1985. Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J. Mol. Biol. 183:543–551.
   PubMedGoogle Scholar
• Falkenthal, S., V. P. Parker, and N. Davidson. 1985. Developmental variations in the splicing pattern of transcripts from the Drosophila gene encoding myosin alkali light chain result in different carboxyl-terminal amino acid sequences. Proc. Natl. Acad. Sci. USA 82:449–453.
   PubMedGoogle Scholar
• Fitzgerald, M., and T. Shenk. 1981. The sequence 5′-AAUAAA-3′ forms part of the recognition site for polyadenylation of late SV40 mRNAs. Cell 24:251–260.
   PubMedGoogle Scholar
• Fyrberg, E. A., B. J. Bond, N. D. Hershey, K. S. Mixter, and N. Davidson. 1981. The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell 24:107–116.
   PubMed Web of Science ®Google Scholar
• Fyrberg, E. A., K. L. Kindle, N. Davidson, and A. Sodja. 1980. The actin genes of Drosophila: a dispersed multigene family. Cell 19:365–378.
   PubMedGoogle Scholar
• Harrington, W. F., and M. Rodgers. 1984. Myosin. Annu. Rev. Biochem. 53:35–73.
   PubMed Web of Science ®Google Scholar
• Hastings, K. E. M., and C. P. Emerson, Jr. 1982. cDNA clone analysis of six co-regulated mRNAs encoding skeletal muscle contractile proteins. Proc. Natl. Acad. Sci. USA 79:1553–1557.
   PubMed Web of Science ®Google Scholar
• Hayashi, K. 1980. A cloning vehicle suitable for strand separation. Gene 11:109–115.
   PubMedGoogle Scholar
• Hayashi, T., R. B. Silver, W. Ip, M. L. Cayer, and D. S. Smith. 1977. Actin-myosin interaction. Self-assembly into a bipolar “contractile unit”. J. Mol. Biol. 111:159–171.
   PubMedGoogle Scholar
• Hayashi, T., P. M. Wozniak, M. L. Cayer, and D. S. Smith. 1983. Actin-myosin interaction: the role of myosin in determining the actin pattern in self-assembled “hybrid” contractile units. Tissue & Cell 15:955–963.
   PubMedGoogle Scholar
• Karn, J., S. Brenner, and L. Barnett. 1983. Protein structural domains in the Caenorhabditis elegans unc-54 myosin heavy chain gene are not separated by introns. Proc. Natl. Acad. Sci. USA 80:4253–4257.
   PubMed Web of Science ®Google Scholar
• Kavinsky, C. J., P. K. Umeda, A. M. Sinha, M. Elzinga, S. W. Tong, R. Zak, S. Jakovcic, and M. Rabinowitz. 1983. Cloned mRNA sequences for two types of embryonic myosin heavy chains from chick skeletal muscle. I. DNA and derived amino acid sequences of light meromyosin. J. Biol. Chem. 258:5196–5205.
   PubMedGoogle Scholar
• Keller, E. B., and W. A. Noon. 1985. Intron splicing: a conserved internal signal in introns of Drosophila pre-mRNAs. Nucleic Acids Res. 13:4971–4981.
   PubMed Web of Science ®Google Scholar
• Kiehart, D. P., D. A. Kaiser, and T. D. Pollard. 1984. Direct localization of monoclonal antibody-binding sites on Acanthamoeba myosin-II and inhibition of filament formation by antibodies that bind to specific sites on the myosin-II tail. J. Cell Biol. 99:1015–1023.
   PubMedGoogle Scholar
• Kiehart, D. P., and T. D. Pollard. 1984. Stimulation of Acanthamoeba actomyosin ATPase activity by myosin-II polymerization. Nature (London) 308:864–866.
   PubMedGoogle Scholar
• Konarska, M. M., P. J. Grabowski, R. A. Padgett, and P. A. Sharp. 1985. Characterization of the branch site in lariat RNAs produced by splicing of mRNA precursors. Nature (London) 313:552–557.
   PubMed Web of Science ®Google Scholar
• Kuczmarski, E. R., and J. A. Spudich. 1980. Regulation of myosin self-assembly: phosphorylation of Dictyostelium heavy chain inhibits formation of thick filaments. Proc. Natl. Acad. Sci. USA 77:7292–7296.
   PubMedGoogle Scholar
• Leinwand, L. A., L. Saez, E. McNally, and B. Nadal-Ginard. 1983. Isolation and characterization of human myosin heavy chain genes. Proc. Natl. Acad. Sci. USA 80:3716–3720.
   PubMedGoogle Scholar
• Lompre, A.-M., K. Schwartz, A. d'Albis, G. Lacombe, N. V. Thiem, and B. Swynghedauw. 1979. Myosin isozyme redistribution in chronic heart overload. Nature (London) 282:105–107.
   PubMed Web of Science ®Google Scholar
• Mahdavi, V., M. Periasamy, and B. Nadal-Ginard. 1982. Molecular characterization of two myosin heavy chain genes expressed in the adult heart. Nature (London) 297:659–664.
   PubMedGoogle Scholar
• Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Maxam, A. M., and W. Gilbert. 1980. Sequencing end-labelled DNA with base-specific chemical cleavages. Methods Enzymol. 65:499–560.
   PubMedGoogle Scholar
• McLachlan, A. D., and J. Karn. 1982. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature (London) 299:226–231.
   PubMed Web of Science ®Google Scholar
• Miller, D. M., I. Ortiz, G. C. Berliner, and H. F. Epstein. 1983. Differential localization of two myosins within nematode thick filaments. Cell 34:477–190.
   PubMed Web of Science ®Google Scholar
• Mogami, K., and Y. Hotta. 1981. Isolation of Drosophila flightless mutants which affect myofibrillar proteins of indirect flight muscle. Mol. Gen. Genet. 183:409–417.
   PubMedGoogle Scholar
• Mogami, K., P. T. O'Donnell, S. I. Bernstein, T. R. F. Wright, and C. P. Emerson, Jr. 1986. Mutations of the Drosophila myosin heavy chain gene: effects on transcription, myosin accumulation and muscle function. Proc. Natl. Acad. Sci. USA 83:1393–1397.
   PubMedGoogle Scholar
• Mount, S. M. 1982. A catalogue of splice junction sequences. Nucleic Acids Res. 10:459–472.
   PubMed Web of Science ®Google Scholar
• Nabeshima, Y., Y. Fujii-Kuriyama, M. Muramatsu, and K. Ogata. 1984. Alternative transcription and two modes of splicing result in two myosin light chains from one gene. Nature (London) 308:333–338.
   PubMed Web of Science ®Google Scholar
• Nawa, H., H. Kotani, and S. Nakanishi. 1984. Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature (London) 312:729–734.
   PubMed Web of Science ®Google Scholar
• Nudel, U., D. Katcoff, Y. Carmon, D. Zevin-Sonkin, Z. Levi, Y. Shaul, M. Shani, and D. Yaffe. 1980. Identification of recombinant phages containing sequences from different rat myosin heavy chain genes. Nucleic Acids Res. 8:2133–2146.
   PubMedGoogle Scholar
• Orkin, S. H., and S. C. Goff. 1981. The duplicated human α-globin genes: their relative expression as measured by RNA analysis. Cell 24:345–351.
   PubMed Web of Science ®Google Scholar
• Peltz, G., E. R. Kuczmarski, and J. A. Spudich. 1981. Dictyostelium myosin: characterization of chymotryptic fragments and localization of the heavy-chain phosphorylation site. J. Cell Biol. 89:104–108.
   PubMedGoogle Scholar
• Poulson, D. F. 1950. Histogenesis, organogenesis and differentiation in the embryo of Drosophila melanogaster meigen, p. 168–274. In M. Demerec (ed.), Biology of Drosophila. John Wiley & Sons, Inc., New York.
   Google Scholar
• Raghaven, K. V. 1981. Evidence for myosin heterogeneity in Drosophila melanogaster. Wilhelm Roux’ Arch. Entwick-lungsmech. Org. 190:297–300.
   Google Scholar
• Robbins, J., G. A. Freyer, D. Chisholm, and T. C. Gilliam. 1982. Isolation of multiple genomic sequences coding for chicken myosin heavy chain protein. J. Biol. Chem. 257:549–556.
   PubMedGoogle Scholar
• Rogers, J., P. Early, C. Carter, K. Calame, M. Bond, L. Hood, and R. Wall. 1980. Two mRNAs with different 3′ ends encode membrane-bound and secreted forms of immunoglobin chain. Cell 20:303–312.
   PubMed Web of Science ®Google Scholar
• Rosenfeld, M. G., S. G. Amara, and R. M. Evans. 1984. Alternative RNA processing: determining neuronal phenotype. Science 225:1315–1320.
   PubMed Web of Science ®Google Scholar
• Rozek, C. E., and N. Davidson. 1983. Drosophila has one myosin heavy chain gene with three developmentally regulated transcripts. Cell 32:23–34.
   PubMed Web of Science ®Google Scholar
• Rozek, C. E., and N. Davidson. 1986. Differential processing of RNA transcribed from the single-copy Drosophila myosin heavy chain gene produces four mRNAs that encode two polypeptides. Proc. Natl. Acad. Sci. USA 83:2128–2132.
   PubMedGoogle Scholar
• Rubin, G. M., and A. C. Spradling. 1982. Genetic transformation of Drosophila using transposable element vectors. Science 218:348–353.
   PubMed Web of Science ®Google Scholar
• Ruskin, B., and M. R. Green. 1985. Role of the 3′ splice site consensus sequence in mammalian pre-mRNA splicing. Nature (London) 317:732–734.
   PubMed Web of Science ®Google Scholar
• Ruskin, B., A. R. Krainer, T. Maniatis, and M. R. Green. 1984. Excision of an intact intron as a novel lariat structure during pre-mRNA splicing in vitro. Cell 38:317–331.
   PubMed Web of Science ®Google Scholar
• Sivaramakrishnan, M., and M. Burke. 1982. The free heavy chain of vertebrate skeletal myosin subfragment I shows full enzymatic activity. J. Biol. Chem. 257:1102–1105.
   PubMedGoogle Scholar
• Solnick, D. 1985. Alternative splicing caused by RNA secondary structure. Cell 43:667–676.
   PubMed Web of Science ®Google Scholar
• Spradling, A. C., and G. M. Rubin. 1982. Transposition of cloned P elements into Drosophila germline chromosomes. Science 218:341–347.
   PubMed Web of Science ®Google Scholar
• Treisman, R., S. H. Orkin, and T. Maniatis. 1983. Specific transcription and RNA splicing defects in five cloned β-thalassaemia genes. Nature (London) 302:591–596.
   PubMed Web of Science ®Google Scholar
• Turner, P. 1985. Controlling role for snurps. Nature (London) 316:105–106.
   PubMedGoogle Scholar
• Umeda, P. K., C. J. Kavinsky, A. M. Sinha, H.-J. Hsu, S. Jakovcic, and M. Rabinowitz. 1983. Cloned mRNA sequences for two types of embryonic myosin heavy chains from chick skeletal muscle. II. Expression during development using SI nuclease mapping. J. Biol. Chem. 258:5206–5214.
   PubMedGoogle Scholar
• Weydert, A., P. Daubas, M. Caravatti, A. Minty, G. Bugaisky, A. Cohen, B. Robert, and M. Buckingham. 1983. Sequential accumulation of mRNAs encoding different myosin heavy chain isoforms during skeletal muscle development in vivo detected with a recombinant plasmid identified as coding for an adult fast myosin heavy chain from mouse skeletal muscle. J. Biol. Chem. 258:13867–13874.
   PubMed Web of Science ®Google Scholar
• Winkelmann, D. A., S. Lowey, and J. L. Press. 1983. Monoclonal antibodies localize change on myosin heavy chain isozymes during avian myogenesis. Cell 34:295–306.
   PubMedGoogle Scholar
• Wydro, R. M., H. T. Nguyen, R. M. Gubits, and B. Nadal-Ginard. 1983. Characterization of sarcomeric myosin heavy chain genes. J. Biol. Chem. 258:670–678.
   PubMedGoogle Scholar
• Young, R. A., O. Hagenbuchle, and U. Schibler. 1981. A single mouse α-amylase gene specifies two different tissue-specific mRNAs. Cell 23:451–458.
   PubMed Web of Science ®Google Scholar