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A genomewide survey of developmentally relevant genes in Ciona intestinalis

IX. Genes for muscle structural proteins

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Abstract

Ascidians are simple chordates that are related to, and may resemble, vertebrate ancestors. Comparison of ascidian and vertebrate genomes is expected to provide insight into the molecular genetic basis of chordate/vertebrate evolution. We annotated muscle structural (contractile protein) genes in the completely determined genome sequence of the ascidian Ciona intestinalis, and examined gene expression patterns through extensive EST analysis. Ascidian muscle protein isoform families are generally of similar, or lesser, complexity in comparison with the corresponding vertebrate isoform families, and are based on gene duplication histories and alternative splicing mechanisms that are largely or entirely distinct from those responsible for generating the vertebrate isoforms. Although each of the three ascidian muscle types – larval tail muscle, adult body-wall muscle and heart – expresses a distinct profile of contractile protein isoforms, none of these isoforms are strictly orthologous to the smooth-muscle-specific, fast or slow skeletal muscle-specific, or heart-specific isoforms of vertebrates. Many isoform families showed larval-versus-adult differential expression and in several cases numerous very similar genes were expressed specifically in larval muscle. This may reflect different functional requirements of the locomotor larval muscle as opposed to the non-locomotor muscles of the sessile adult, and/or the biosynthetic demands of extremely rapid larval development.

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References

  • Araki I, Satoh N (1996) Cis-regulatory elements conserved in the proximal promoter region of an ascidian embryonic muscle myosin heavy chain gene. Dev Genes Evol 206:54–63

    Article  CAS  Google Scholar 

  • Araki I, Saiga H, Makabe KW, Satoh N (1994) Expression of AMD1, a gene for a MyoD-related factor in the ascidian Halocynthia roretzi. Roux's Arch Dev Biol 203:320–327

    Article  CAS  Google Scholar 

  • Ausoni S, Campione M, Picard A, Moretti P, Vitadello M, De Nardi C, Schiaffino S (1994) Structure and regulation of the mouse cardiac troponin I gene. J Biol Chem 269:339–346

    PubMed  CAS  Google Scholar 

  • Banerjee-Basu S, Buonanno A (1993) cis-acting sequences of the rat troponin I slow gene confer tissue- and development-specific transcription in cultured muscle cells as well as fiber type specificity in transgenic mice. Mol Cell Biol 13:7019–7028

    PubMed  CAS  Google Scholar 

  • Barbas JA, Galceran J, Krah-Jentgens I, de la Pompa JL, Canal I, Pongs O, Ferrus A (1991) Troponin I is encoded in the haplolethal region of the Shaker gene complex of Drosophila. Genes Dev 5:5132–5140

    Article  Google Scholar 

  • Beall CJ, Fyrberg E (1991) Muscle abnormalities in Drosophila melanogaster heldup mutants are caused by missing or aberrant troponin-I isoforms. J Cell Biol 114:941–951

    Article  PubMed  CAS  Google Scholar 

  • Beggs AH, Byers TJ, Knoll JH, Boyce FM, Bruns GA, Kunkel LM (1992) Cloning and characterization of two human skeletal muscle α-actinin genes located on chromosomes 1 and 11. J Biol Chem 267:9281–9288

    PubMed  CAS  Google Scholar 

  • Bodmer R, Venkatesh TV (1998) Heart development in Drosophila and vertebrates: conservation of molecular mechanisms. Dev Genet 22:181–186

    Article  PubMed  CAS  Google Scholar 

  • Breitbart RE, Nguyen HT, Medford RM, Destree AT, Mahdavi V, Nadal-Ginard B (1985) Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell 41:67–82

    Article  PubMed  CAS  Google Scholar 

  • Chiba S, Satou Y, Nishikata T, Satoh N (1998) Isolation and characterization of cDNA clones for epidermis-specific and muscle-specific genes in Ciona savignyi embryos. Zool Sci 15:239–246

    Article  CAS  Google Scholar 

  • Coté GP (1983) Structural and functional properties of the non-muscle tropomyosins. Mol Cell Biochem 57:127–146

    Article  PubMed  Google Scholar 

  • Dehal P, Satou Y, Campbell RK et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167

    Article  PubMed  CAS  Google Scholar 

  • Di Gregorio A, Levine M (1999) Regulation of Ci-tropomyosin-like, a Brachyury target gene in the ascidian, Ciona intestinalis. Development 126:5599–5609

    Google Scholar 

  • Endo T, Matsumoto K, Hama T, Ohtsuka Y, Katsura G, Obinata T (1996) Distinct troponin T genes are expressed in embryonic/larval tail striated muscle and adult body wall smooth muscle of ascidian. J Biol Chem 271:27855–27862

    Article  PubMed  CAS  Google Scholar 

  • Falkenthal S, Graham M, Wilkinson J (1987) The indirect flight muscle of Drosophila accumulates a unique myosin alkali light chain isoform. Dev Biol 121:263–272

    Article  PubMed  CAS  Google Scholar 

  • Farah CS, Reinach FC (1995) The troponin complex and regulation of muscle contraction. FASEB J 9:755–767

    PubMed  CAS  Google Scholar 

  • Fyrberg C, Parker H, Hutchison B, Fyrberg E (1994) Drosophila melanogaster genes encoding three troponin-C isoforms and a calmodulin-related protein. Biochem Genet 32:119–135

    Article  PubMed  CAS  Google Scholar 

  • Fyrberg EA, Bond BJ, Hershey ND, Mixter KS, Davidson N (1981) The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell 24:107–116

    Article  PubMed  CAS  Google Scholar 

  • Fyrberg E, Fyrberg CC, Beall C, Saville DL (1990a) Drosophila melanogaster troponin-T mutations engender three distinct syndromes of myofibrillar abnormalities. J Mol Biol 216:657–675

    Article  PubMed  CAS  Google Scholar 

  • Fyrberg E, Kelly M, Ball E, Fyrberg C, Reedy MC (1990b) Molecular genetics of Drosophila α-actinin: mutant alleles disrupt Z disc integrity and muscle insertions. J Cell Biol 110:1999–2011

    Article  PubMed  CAS  Google Scholar 

  • Gahlmann R, Kedes L (1990) Cloning, structural analysis, and expression of the human fast twitch skeletal muscle troponin C gene. J Biol Chem 265:12520–12528

    PubMed  CAS  Google Scholar 

  • Goodbody I (1974) The physiology of ascidians. Adv Mar Biol 12:1–149

    Article  Google Scholar 

  • Guénet JL, Simon-Chazottes D, Gravel M, Hastings KEM, Schiaffino S (1996) Cardiac and skeletal muscle troponin I isoforms are encoded by a dispersed gene family on mouse chromosomes 1 and 7. Mamm Genome 7:13–15

    Article  PubMed  Google Scholar 

  • Hallauer PL, Bradshaw HL, Hastings KEM (1993) Complex fiber-type-specific expression of fast skeletal muscle troponin I gene constructs in transgenic mice. Development 119:691–701

    PubMed  CAS  Google Scholar 

  • Hotta K, Takahashi H, Asakura T, Saitoh B, Takatori N, Satou Y, Satoh N (2000) Characterization of Brachyury-downstream notochord genes in the Ciona intestinalis embryo. Dev Biol 224:69–80

    Article  PubMed  CAS  Google Scholar 

  • Imamura M, Sakurai T, Ogawa Y, Ishikawa T, Goto K, Masaki T (1994) Molecular cloning of low-Ca2+-sensitive-type non-muscle α-actinin. Eur J Biochem 223:395–401

    Article  PubMed  CAS  Google Scholar 

  • Karlik CC, Fyrberg EA (1986) Two Drosophila melanogaster tropomyosin genes: structural and functional aspects. Mol Cell Biol 6:1965–1973

    PubMed  CAS  Google Scholar 

  • Katz MJ (1983) Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biol Bull 164:1–27

    Article  Google Scholar 

  • Kusakabe T (1997) Ascidian actin genes: developmental regulation of gene expression and molecular evolution. Zool Sci 14:707–718

    Article  PubMed  CAS  Google Scholar 

  • Kusakabe T, Suzuki J, Saiga H, Jeffery WR, Makabe KW, Satoh N (1991) Temporal and spatial expression of a muscle actin gene during embryogenesis of the ascidian Halocynthia roretzi. Dev Growth Differ 33:227–234

    Article  Google Scholar 

  • Kusakabe T, Yoshida R, Kawakami I, Kusakabe R, Mochizuki Y, Yamada L, Shin-i T, Kohara Y, Satoh N, Tsuda M, Satou Y (2002) Gene expression profiles in tadpole larvae of Ciona intestinalis. Dev Biol 242:188–203

    Article  PubMed  Google Scholar 

  • Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Article  PubMed  CAS  Google Scholar 

  • Lees-Miller JP, Helfman DM (1991) The molecular basis for tropomyosin isoform diversity. BioEssays 13:429–437

    Article  PubMed  CAS  Google Scholar 

  • Lenz S, Lohse P, Seidel U, Arnold HH (1989) The alkali light chains of human smooth and nonmuscle myosins are encoded by a single gene. Tissue-specific expression by alternative splicing pathways. J Biol Chem 264:9009–9015

    PubMed  CAS  Google Scholar 

  • Levitt LK, O'Mahoney JV, Brennan KJ, Joya JE, Zhu L, Wade RP, Hardeman EC (1995) The human troponin I slow promoter directs slow fiber-specific expression in transgenic mice. DNA Cell Biol 14:599–607

    Article  PubMed  CAS  Google Scholar 

  • MacLean DW, Meedel TH, Hastings KEM (1997) Tissue-specific alternative splicing of ascidian troponin I isoforms. Redesign of a protein isoform-generating mechanism during chordate evolution. J Biol Chem 272:32115–32120

    Article  PubMed  CAS  Google Scholar 

  • Makabe KW, Fujiwara S, Saiga H, Satoh N (1990) Specific expression of myosin heavy chain gene in muscle lineage cells of the ascidian embryo. Roux's Arch Dev Biol 199:307–313

    Article  CAS  Google Scholar 

  • Meedel TH (1998) Development of ascidian muscles and their evolutionary relationship to other chordate muscle types. In: Adiyodi KG, Adiyodi RG (eds) Progress in developmental biology, reproductive biology of invertebrates, Volume VII. Wiley-Interscience, New York, pp 305–330

  • Meedel TH, Hastings KEM (1993) Striated muscle-type tropomyosin in a chordate smooth muscle, ascidian body-wall muscle. J Biol Chem 268:6755–6764

    PubMed  CAS  Google Scholar 

  • Meedel TH, Farmer SC, Lee JJ (1997) The single MyoD family gene of Ciona intestinalis encodes two differentially expressed proteins: implications for the evolution of chordate muscle gene regulation. Development 124:1711–1721

    PubMed  CAS  Google Scholar 

  • Mesnard L, Samson F, Espinasse I, Durand J, Neveux JY, Mercadier JJ (1993) Molecular cloning and developmental expression of human cardiac troponin T. FEBS Lett 328:139–144

    Article  PubMed  CAS  Google Scholar 

  • Millake DB, Blanchard AD, Patel B, Critchley DR (1989) The cDNA sequence of a human placental α-actinin. Nucleic Acids Res 17:6725

    Article  PubMed  CAS  Google Scholar 

  • Molkentin JD, Black BL, Martin JF, Olson EN (1995) Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125–1136

    CAS  Google Scholar 

  • Moncrief ND, Kretsinger RH, Goodman M (1990) Evolution of EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J Mol Evol 30:522–562

    Article  PubMed  CAS  Google Scholar 

  • Morad M, Cleemann L (1980) Tunicate heart as a possible model for the vertebrate heart. Fed Proc 39:3188–3194

    PubMed  CAS  Google Scholar 

  • Nevitt G, Gilly WF (1986) Morphological and physiological properties of non-striated muscle from the tunicate, Ciona intestinalis: parallels with vertebrate skeletal muscle. Tissue Cell 18:341–360

    Article  PubMed  CAS  Google Scholar 

  • Nishida H (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol 121:526–541

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, Berlin Heidelberg New York

  • Oshima S, Komiya T, Takeuchi K, Endo K, Obinata T (1988) Generation of multiple troponin T isoforms is a common feature of the muscles of various chordate animals. Comp Biochem Physiol 90B:779–784

    Google Scholar 

  • Robert B, Daubas P, Akimenko MA, Cohen A, Garner I, Guenet JL, Buckingham ME (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

    Article  PubMed  CAS  Google Scholar 

  • Satoh N (1994) Developmental biology of ascidians. Cambridge University Press, New York

  • Satou Y, Takatori N, Yamada L, Mochizuki Y, Hamaguchi M, Ishikawa H, Chiba S, Imai K, Kano S, Murakami SD, Nakayama A, Nishino A, Sasakura Y, Satoh G, Shimotori T, Shin-i T, Shoguchi E, Suzuki MM, Takada N, Utsumi N, Yoshida N, Saiga H, Kohara Y, Satoh N (2001) Gene expression profiles in Ciona intestinalis tailbud embryos. Development 128:2893–2904

    PubMed  Google Scholar 

  • Satou Y, Takatori N, Fujiwara S, Nishikata T, Saiga H, Kusakabe T, Shin-i T, Kohara Y, Satoh N (2002) Ciona intestinalis cDNA projects: expressed sequence tag analyses and gene expression profiles during embryogenesis. Gene 287:83–96

    Article  PubMed  CAS  Google Scholar 

  • Satou Y, Imai KS, Levine M, Kohara Y, Rokhsar D, Satoh N (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. I. Genes for bHLH transcription factor. Dev Genes Evol DOI 10.1007/s00427-003-319-7

  • Schiaffino S, Reggiani C (1996) Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76:371–423

    CAS  Google Scholar 

  • Schreier T, Kedes L, Gahlmann R (1990) Cloning, structural analysis, and expression of the human slow twitch skeletal muscle/cardiac troponin C gene. J Biol Chem 265:21247–21253

    PubMed  CAS  Google Scholar 

  • Seidel U, Bober E, Winter B, Lenz S, Lohse P, Arnold HH (1987) The complete nucleotide sequences of cDNA clones coding for human myosin light chains 1 and 3. Nucleic Acids Res 15:4989

    Article  PubMed  CAS  Google Scholar 

  • Sellers JR (2000) Myosins: a diverse superfamily. Biochim Biophys Acta 1496:3–22

    Article  PubMed  CAS  Google Scholar 

  • Shinohara Y, Konishi K (1982) Ultrastructure of the body-wall muscle of the ascidian Halocynthia roretzi: smooth muscle cell with multiple nuclei. J Exp Zool 221:137–142

    Article  Google Scholar 

  • Smillie LB (1979) Structure and functions of tropomyosins from muscle and non-muscle sources. Trends Biochem Sci 4:151–155

    Article  CAS  Google Scholar 

  • Takagi T, Kudoh S, Konishi K (1986) The amino acid sequence of ascidian (Halocynthia roretzi) myosin light chains. Biochim Biophys Acta 874:318–325

    Article  CAS  Google Scholar 

  • Terakado K, Obinata T (1987) Structure of multinucleated smooth muscle cells of the ascidian Halocynthia roretzi. Cell Tissue Res 247:85–94

    Google Scholar 

  • Toyota NT, Obinata T, Terakado K (1979) Isolation of troponin-tropomyosin-containing thin filaments from ascidian smooth muscle. Comp Biochem Physiol 62B:433–441

    CAS  Google Scholar 

  • Vandekerckhove J, Weber K (1979) 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 14:123–133

    Article  PubMed  CAS  Google Scholar 

  • Venter JC, Adams MD, Myers EW et al (2001) The sequence of the human genome. Science 291:1304–1351

    Article  PubMed  CAS  Google Scholar 

  • Wada H (1998) Evolutionary history of free-swimming and sessile lifestyles in urochordates as deduced from 18S rDNA molecular phylogeny. Mol Biol Evol 15:1189–1194

    Article  PubMed  CAS  Google Scholar 

  • Wada H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc Natl Acad Sci USA 91:1801–1804

    Article  PubMed  CAS  Google Scholar 

  • Waterston RH, Lindblad-Toh K, Birney E et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562

    Article  PubMed  CAS  Google Scholar 

  • Weiss A, McDonough D, Wertman B, Acakpo-Satchivi L, Montgomery K, Kucherlapati R, Leinwand L, Krauter K (1999) Organization of human and mouse skeletal myosin heavy chain gene clusters is highly conserved. Proc Natl Acad Sci USA 96:2958–2963

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson JM, Grand RJA (1978) Comparison of amino acid sequence of troponin I from different striated muscles. Nature 271:31–35

    Article  PubMed  CAS  Google Scholar 

  • Wu QL, Jha PK, Raychowdhury MK, Du Y, Leavis PC, Sarkar S (1994) Isolation and characterization of human fast skeletal β troponin T cDNA: comparative sequence analysis of isoforms and insight into the evolution of members of a multigene family. DNA Cell Biol 13:217–233

    Article  PubMed  CAS  Google Scholar 

  • Yuasa HJ, Sato S, Yamamoto H, Takagi T (1997) Structure of the ascidian, Halocynthia roretzi, troponin C gene. J Biochem (Tokyo) 121:671–676

  • Zhang JM, Chen L, Krause M, Fire A, Paterson BM (1999) Evolutionary conservation of MyoD function and differential utilization of E proteins. Dev Biol 208:465–472

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by Grants-in-Aid for Scientific Research from MEXT, Japan to Y.S. (13044001) and N.S. (12202001). S.C. was a Postdoctoral Fellow of JSPS with a research grant (12060102). We thank Kazuko Hirayama, Chikako Imaizumi, Asako Fujimoto, and Hisayoshi Ishikawa for their technical support.

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Authors and Affiliations

  1. Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606–8502, Japan

    Shota Chiba, Satoko Awazu, Machiko Itoh, Nori Satoh & Yutaka Satou

  2. Bioinformatics and Pattern Discovery Group, IBM T. J. Watson Research Center, PO Box 218, Yorktown Heights, NY 10598, USA

    Stephen T. Chin-Bow

  3. Montreal Neurological Institute and Department of Biology, McGill University, Montreal, Quebec, Canada H3A 2B4

    Kenneth E. M. Hastings

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  1. Shota Chiba
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  2. Satoko Awazu
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  3. Machiko Itoh
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Correspondence to Nori Satoh.

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Edited by D. Tautz

The first three authors contributed equally to this work.

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Chiba, S., Awazu, S., Itoh, M. et al. A genomewide survey of developmentally relevant genes in Ciona intestinalis . Dev Genes Evol 213, 291–302 (2003). https://doi.org/10.1007/s00427-003-0324-x

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