Skip to main content

Advertisement

SpringerLink
Log in

A genomewide survey of developmentally relevant genes in Ciona intestinalis

V. Genes for receptor tyrosine kinase pathway and Notch signaling pathway

  • Original Article
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

In the present survey, we identified most of the genes involved in the receptor tyrosine kinase (RTK), mitogen activated protein kinase (MAPK) and Notch signaling pathways in the draft genome sequence of Ciona intestinalis, a basal chordate. Compared to vertebrates, most of the genes found in the Ciona genome had fewer paralogues, although several genes including ephrin, Eph and fringe appeared to have multiplied or duplicated independently in the ascidian genome. In contrast, some genes including kit/flt, PDGF and Trk receptor tyrosine kinases were not found in the present survey, suggesting that these genes are innovations in the vertebrate lineage or lost in the ascidian lineage. The gene set identified in the present analysis provides an insight into genes for the RTK, MAPK and Notch signaling pathways in the ancient chordate genome and thereby how chordates evolved these signaling pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  • Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–776

    Article  PubMed  CAS  Google Scholar 

  • Chang L, Karin M (2001) Mammalian MAP kinase signalling cascades. Nature 410:37–40

    Article  PubMed  CAS  Google Scholar 

  • Conlon JM (2001) Evolution of the insulin molecule: insights into structure-activity and phylogenetic relationships. Peptides 22:1183–1193

    Article  PubMed  CAS  Google Scholar 

  • Corbo JC, Fujiwara S, Levine M, Di Gregorio A (1998) Suppressor of Hairless activates Brachyury expression in the Ciona embryo. Dev Biol 203:358–368

    Article  PubMed  CAS  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 

  • Dionne CA, Crumley G, Bellot F, Kaplow JM, Searfoss G, Ruta M, Burgess WH, Jaye M, Schlessinger J (1990) Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors. EMBO J 9:2685–2692

    PubMed  CAS  Google Scholar 

  • English J, Pearson G, Wilsbacher J, Swantek J, Karandikar M, Xu S, Cobb MH (1999) New insights into the control of MAP kinase pathways. Exp Cell Res 253:255–270

    Article  PubMed  CAS  Google Scholar 

  • Finlin BS, Gau CL, Murphy GA, Shao H, Kimel T, Seitz RS, Chiu YF, Botstein D, Brown PO, Der CJ, Tamanoi F, Andres DA, Perou CM (2001) RERG is a novel ras-related, estrogen-regulated and growth-inhibitory gene in breast cancer. J Biol Chem 45:42259–42267

    Article  Google Scholar 

  • Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, Apfelstedt-Sylla E, Vollrath D (2000) Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nature Genet 26:270–271

    Article  PubMed  CAS  Google Scholar 

  • Garrett TP, McKern NM, Lou M, Frenkel MJ, Bentley JD, Lovrecz GO, Elleman TC, Cosgrove LJ, Ward CW (1998) Crystal structure of the first three domains of the type-1 insulin-like growth factor receptor. Nature 394:395–399

    Article  PubMed  CAS  Google Scholar 

  • Gotoh I, Adachi M, Nishida E (2001) Identification and characterization of a novel MAP kinase kinase kinase, MLTK. J Biol Chem 6:4276–4286

    Article  Google Scholar 

  • Hagemann C, Blank JL (2001) The ups and downs of MEK kinase interactions. Cell Signal 13:863–875

    Article  PubMed  CAS  Google Scholar 

  • Hori S, Saitoh T, Matsumoto M, Makabe KW, Nishida H (1997) Notch homologue from Halocynthia roretzi is preferentially expressed in the central nervous system during ascidian embryogenesis. Dev Genes Evol 207:371–380

    Article  CAS  Google Scholar 

  • Imai KS, Satoh N, Satou Y (2002) An essential role of a FoxD gene in notochord induction in Ciona embryos. Development 129:3441–3453

    PubMed  CAS  Google Scholar 

  • Kamei S, Yajima I, Yamamoto H, Kobayashi A, Makabe KW, Yamazaki H, Hayashi SI, Kunisada T (2000) Characterization of a novel member of the FGFR family, HrFGFR, in Halocynthia roretzi. Biochem Biophys Res Commun 275:503–508

    Article  PubMed  CAS  Google Scholar 

  • Keegan K, Johnson DE, Williams LT, Hayman MJ (1991) Isolation of an additional member of the fibroblast growth factor receptor family, FGFR-3. Proc Natl Acad Sci USA 88:1095–1099

    Article  PubMed  CAS  Google Scholar 

  • Kishi N, Tang Z, Maeda Y, Hirai A, Mo R, Ito M, Suzuki S, Nakao K, Kinoshita T, Kadesch T, Hui C, Artavanis-Tsakonas S, Okano H, Matsuno K (2001) Murine homologs of deltex define a novel gene family involved in vertebrate Notch signaling and neurogenesis. Int J Dev Neurosci 19:21–35

    Article  PubMed  CAS  Google Scholar 

  • Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nature Rev Mol Cell Biol 3:475–486

    Article  CAS  Google Scholar 

  • Matsui T, Heidaran M, Miki T, Popescu N, La Rochelle W, Kraus M, Pierce J, Aaronson S (1989) Isolation of a novel receptor cDNA establishes the existence of two PDGF receptor genes. Science 243:800–804

    Article  PubMed  CAS  Google Scholar 

  • McRory JE, Sherwood NM (1997) Ancient divergence of insulin and insulin-like growth factor. DNA Cell Biol 16:939–949

    Article  PubMed  CAS  Google Scholar 

  • Minoguchi S, Taniguchi Y, Kato H, Okazaki T, Strobl LJ, Zimber-Strobl U, Bornkamm GW, Honjo T. (1997) RBP-L, a transcription factor related to RBP-Jk. Mol Cell Biol. 17:2679-2687.

    Google Scholar 

  • Mumm JS, Kopan R (2000) Notch signaling: from the outside in. Dev Biol 228:151–165

    Article  PubMed  CAS  Google Scholar 

  • O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C, Espinosa R 3rd, Le Beau MM, Earp HS, Liu ET (1991) axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 11:5016–5031

    PubMed  Google Scholar 

  • Ohashi K, Mizuno K, Kuma K, Miyata T, Nakamura T (1994) Cloning of the cDNA for a novel receptor tyrosine kinase, Sky, predominantly expressed in brain. Oncogene 9:699–705

    PubMed  CAS  Google Scholar 

  • Ornitz DM, Itoh N (2001) Fibroblast growth factors. Genome Biol 2:REVIEWS3005

    Article  PubMed  CAS  Google Scholar 

  • Partanen J, Makela TP, Eerola E, Korhonen J, Hirvonen H, Claesson-Welsh L, Alitalo K (1991) FGFR-4, a novel acidic fibroblast growth factor receptor with a distinct expression pattern. EMBO J 10:1347–1354

    PubMed  CAS  Google Scholar 

  • Sasakura Y, Yamada L, Takatori N, Satou Y, Satoh N (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. VII. Molecules involved in the regulation of cell polarity and actin dynamics. Dev Genes Evol DOI 10.1007/s00427-003-0325-9

  • Satou Y, Imai KS, Satoh N (2002a) Fgf genes in the basal chordate Ciona intestinalis. Dev Genes Evol 9:432–438

    Article  Google Scholar 

  • Satou Y, Yamada L, Mochizuki Y, Takatori N, Kawashima T, Sasaki A, Hamaguchi M, Awazu S, Yagi K, Sasakura Y, Nakayama A, Ishikawa H, Inaba K, Satoh N (2002b) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 4:153–154

    Article  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 factors. Dev Genes Evol DOI 10.1007/s00427-003-0319-7

  • Shelton DL, Sutherland J, Gripp J, Camerato T, Armanini MP, Phillips HS, Carroll K, Spencer SD, Levinson AD (1995) Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J Neurosci 15:477–491

    PubMed  CAS  Google Scholar 

  • Shibuya M, Yamaguchi S, Yamane A, Ikeda T, Tojo A, Matsushime H, Sato M (1990) Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5:519–524

    PubMed  CAS  Google Scholar 

  • Shimauchi Y, Murakami SD, Satoh N (2001) FGF signals are involved in the differentiation of notochord cells and mesenchyme cells of the ascidian Halocynthia roretzi. Development 128:2711–2721

    PubMed  CAS  Google Scholar 

  • Shishido E, Higashijima S, Emori Y, Saigo K (1993) Two FGF-receptor homologues of Drosophila: one is expressed in mesodermal primordium in early embryos. Development 117:751–761

    PubMed  CAS  Google Scholar 

  • Symons M, Takai Y (2001) Ras GTPases: singing in tune. Sci STKE 68:PE1

    Google Scholar 

  • Theodosiou A, Ashworth A (2002) MAP kinase phosphatases. Genome Biol 3:REVIEWS3009

    Article  PubMed  Google Scholar 

  • Treisman R (1996) Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol 8:205–215

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by Grants-in-Aid for Scientific Research from MEXT, Japan to Y.Satou (13044001) and N.S. (12202001). Y.Sasakura was a Postdoctoral Fellow of JSPS with a research grant (14000967). K.S.I. was a Predoctoral Fellow of JSPS with a research grant (12003588). We thank Kazuko Hirayama, Chikako Imaizumi, Asako Fujimoto, and Hisayoshi Ishikawa for their technical support.

Author information

Authors and Affiliations

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

    Yutaka Satou, Yasunori Sasakura, Lixy Yamada, Kaoru S. Imai & Nori Satoh

  2. Department of Zoology and Entomology, University of Queensland, Brisbane, Qld 4072, Australia

    Bernard Degnan

Authors
  1. Yutaka Satou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yasunori Sasakura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lixy Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kaoru S. Imai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nori Satoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bernard Degnan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yutaka Satou.

Additional information

The first three authors equally contributed to this work

Edited by D. Tautz

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Satou, Y., Sasakura, Y., Yamada, L. et al. A genomewide survey of developmentally relevant genes in Ciona intestinalis . Dev Genes Evol 213, 254–263 (2003). https://doi.org/10.1007/s00427-003-0317-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-003-0317-9

Keywords

Search

Navigation