Development Genes and Evolution

, Volume 213, Issue 5–6, pp 303–313 | Cite as

A genomewide survey of developmentally relevant genes in Ciona intestinalis

X. Genes for cell junctions and extracellular matrix
  • Yasunori Sasakura
  • Eiichi Shoguchi
  • Naohito Takatori
  • Shuichi Wada
  • Ian A. Meinertzhagen
  • Yutaka Satou
  • Nori SatohEmail author
Original Article


Cell junctions and the extracellular matrix (ECM) are crucial components in intercellular communication. These systems are thought to have become highly diversified during the course of vertebrate evolution. In the present study, we have examined whether the ancestral chordate already had such vertebrate systems for intercellular communication, for which we have searched the genome of the ascidian Ciona intestinalis. From this molecular perspective, the Ciona genome contains genes that encode protein components of tight junctions, hemidesmosomes and connexin-based gap junctions, as well as of adherens junctions and focal adhesions, but it does not have those for desmosomes. The latter omission is curious, and the ascidian type-I cadherins may represent an ancestral form of the vertebrate type-I cadherins and desmosomal cadherins, while Ci-Plakin may represent an ancestral protein of the vertebrate desmoplakins and plectins. If this is the case, then ascidians may have retained ancestral desmosome-like structures, as suggested by previous electron-microscopic observations. In addition, ECM genes that have been regarded as vertebrate-specific were also found in the Ciona genome. These results suggest that the last common ancestor shared by ascidians and vertebrates, the ancestor of the entire chordate clade, had essentially the same systems of cell junctions as those in extant vertebrates. However, the number of such genes for each family in the Ciona genome is far smaller than that in vertebrate genomes. In vertebrates these ancestral cell junctions appear to have evolved into more diverse, and possibly more complex, forms, compared with those in their urochordate siblings.


Basal chordates Ciona intestinalis Genomewide survey Genes Cell junctions 



This research was supported by Grants-in-Aid for Scientific Research from MEXT, Japan to Y. Satou (13044001) and N.S. (12202001), by a CREST project of Japan Science and Technology Corporation (N.S., E.S., and S.W.) and by support from NSERC, Ottawa (to I.A.M.). Y. Sasakura was a Postdoctoral Fellow of JSPS with research grant no. 14000967. We thank Kazuko Hirayama, Chikako Imaizumi, Asako Fujimoto, and Hisayoshi Ishikawa for their technical support.

Supplementary material (274 kb)
Supplementary material, approximately 280 KB.


  1. Aurrand-Lions M, Duncan L, Ballestrem C, Imhof BA (2001a) JAM-2, a novel immunoglobulin superfamily molecule, expressed by endothelial and lymphatic cells. J Biol Chem 276:2733–2741PubMedCrossRefGoogle Scholar
  2. Aurrand-Lions M, Johnson-Leger C, Wong C, Du Pasquier L, Imhof BA (2001b) Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 98:3699–3707PubMedCrossRefGoogle Scholar
  3. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280PubMedCrossRefGoogle Scholar
  4. Bone Q (1972) The origin of chordates. Oxford University Press, LondonGoogle Scholar
  5. Bruzzone R, White TW, Goodenough DA (1996) The cellular Internet: on-line with connexins. BioEssays 18:709–718PubMedCrossRefGoogle Scholar
  6. Burke RD (1999) Invertebrate integrins: structure, function, and evolution. Int Rev Cytol 191:257–284PubMedCrossRefGoogle Scholar
  7. Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469–4474PubMedCrossRefGoogle Scholar
  8. Chervitz SA, Aravind L, Sherlock G, Ball CA, Koonin EV, Dwight SS, Harris MA, Dolinski K, Mohr S, Smith T, Weng S, Cherry JM, Botstein D (1998) Comparison of the complete proteins sets of worm and yeast: orthology and divergence. Science 282:2022–2028PubMedCrossRefGoogle Scholar
  9. Chiba S, Awazu S, Itoh M, Chin-Bow ST, Satoh N, Satou Y, Hastings KEM (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. IX. Genes for muscle structural proteins. Dev Genes Evol DOI 10.1007/s00427-003-0324-xGoogle Scholar
  10. Cloney RA (1972) Cytoplasmic filaments and morphogenesis effects of cytochalasin B on contractile epidermal cells. Z Zellforsch Mikrosk Anat 132:167–192PubMedCrossRefGoogle Scholar
  11. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213–234PubMedCrossRefGoogle Scholar
  12. D'Atri F, Citi S (2002) Molecular complexity of vertebrate tight junctions. Mol Membrane Biol 19:103–112CrossRefGoogle Scholar
  13. Dehal P, Satou Y, Campbell RK, et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167PubMedCrossRefGoogle Scholar
  14. Evans WH, Martin PE (2002) Gap junctions: structure and function. Mol Membrane Biol 19:121–136CrossRefGoogle Scholar
  15. Garrod DR, Merritt AJ, Nie ZX (2002) Desmosomal adhesion: structural basis, molecular mechanism and regulation. Mol Membrane Biol 19:81–94CrossRefGoogle Scholar
  16. Garstang W (1928) The morphology of the Tunicata, and its bearings on the phylogeny of the Chordata. Q J Microsc Sci 72:51–187Google Scholar
  17. Georges D (1979) Gap and tight junctions in tunicates. Study in conventional and freeze-fracture techniques. Tissue Cell 11:781–792PubMedCrossRefGoogle Scholar
  18. Hino K, Satou Y, Yagi K, Satoh N (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. VI. Genes for Wnt, TGFβ, Hedgehog and JAK/STAT signaling pathways. Dev Genes Evol DOI 10.1007/s00427-003-318-8Google Scholar
  19. Horwitz A, Duggan K, Buck C, Beckerle MC, Burridge K (1986) Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature 320:531–533PubMedCrossRefGoogle Scholar
  20. 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 224:69–80PubMedCrossRefGoogle Scholar
  21. Huber JD, Egleton RD, Davis TP (2001) Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24:719–725PubMedCrossRefGoogle Scholar
  22. Hutter H, Vogel BE, Plenefisch JD, Norris CR, Proenca RB, Spieth J, Guo C, Mastwal S, Zhu X, Scheel J, Hedgecock EM (2000) Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287:989–994PubMedCrossRefGoogle Scholar
  23. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687PubMedCrossRefGoogle Scholar
  24. Hynes RO, Zhao Q (2000) The evolution of cell adhesion. J Cell Biol 150:F85–F95CrossRefGoogle Scholar
  25. Imai K, Takada N, Satoh N, Satou Y (2000) β-Catenin mediates the specification of endoderm cells in ascidian embryos. Development 127:3009–3020PubMedGoogle Scholar
  26. Itoh M, Furuse M, Morita K, Kubota K, Saitou M, Tsukita S (1999) Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol 147:1351–1363PubMedCrossRefGoogle Scholar
  27. Janssens B, Goossens S, Staes K, Gilbert B, van Hengel J, Colpaert C, Bruyneel E, Mareel M, van Roy F (2001) αT-Catenin: a novel tissue-specific β-catenin-binding protein mediating strong cell-cell adhesion. J Cell Sci 114:3177–3188PubMedGoogle Scholar
  28. Kaiser D (2001) Building a multicellular organism. Ann Rev Genet 35:103–123PubMedCrossRefGoogle Scholar
  29. Kollmar R, Nakamura SK, Kappler JA, Hudspeth AJ (2001) Expression and phylogeny of claudins in vertebrate primordia. Proc Natl Acad Sci USA 98:10196–10201PubMedCrossRefGoogle Scholar
  30. Kumar NM, Gilula NB (1996) The gap junction communication channel. Cell 84:381–388PubMedCrossRefGoogle Scholar
  31. Lane NJ, Dallai R, Burighel P, Martinucci GB (1986) Tight and gap junctions in the intestinal tract of tunicates (Urochordata): a freeze-fracture study. J Cell Sci 84:1-17PubMedGoogle Scholar
  32. Letunic I, Goodstadt L, Dickens NJ, Doerks T, Schultz J, Mott R, Ciccarelli F, Copley RR, Ponting CP, Bork P (2002) Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res 30:242–244PubMedCrossRefGoogle Scholar
  33. Levi L, Douek J, Osman M, Bosch TC, Rinkevich B (1997) Cloning and characterization of BS-cadherin, a novel cadherin from the colonial urochordate Botryllus schlosseri. Gene 200:117–123PubMedCrossRefGoogle Scholar
  34. Lorber V, Rayns DG (1972) Cellular junctions in the tunicate heart. J Cell Sci 10:211–227PubMedGoogle Scholar
  35. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117–127PubMedCrossRefGoogle Scholar
  36. McMahan UJ (1990) The agrin hypothesis. Cold Spring Harbor Symp Quant Biol 50:407–418CrossRefGoogle Scholar
  37. Meinertzhagen IA, Okamura Y (2001) The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci 24:401–410PubMedCrossRefGoogle Scholar
  38. Miyazawa S, Azumi K, Nonaka M (2001) Cloning and characterization of integrin α subunits from the solitary ascidian, Halocynthia roretzi. J Immunol 166:1710–1715PubMedGoogle Scholar
  39. Moroi S, Saitou M, Fujimoto K, Sakakibara A, Furuse M, Yoshida O, Tsukita S (1998) Occludin is concentrated at tight junctions of mouse/rat but not human/guinea pig Sertoli cells in testes. Am J Physiol 274:C1708–C1717PubMedGoogle Scholar
  40. Nollet F, Kools P, van Roy F (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299:551–572PubMedCrossRefGoogle Scholar
  41. O'Brien J, Bruzzone R, White TW, Al-Ubaidi MR, Ripps H (1998) Cloning and expression of two related connexins from the perch retina define a distinct subgroup of the connexin family. J Neurosci 18:7625–7637PubMedGoogle Scholar
  42. Oda H, Tsukita S (1999) Nonchordate classic cadherins have a structurally and functionally unique domain that is absent from chordate classic cadherins. Dev Biol 216:406–422PubMedCrossRefGoogle Scholar
  43. Oda H, Wada H, Tagawa K, Akiyama-Oda Y, Satoh N, Humphreys T, Zhang S, Tsukita S (2002) A novel amphioxus cadherin that localizes to epithelial adherens junctions has an unusual domain organization with implications for chordate phylogeny. Evol Dev 4:426–434PubMedCrossRefGoogle Scholar
  44. Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S (2000) A ubiquitous family of putative gap junction molecules. Curr Biol 10:R473–474PubMedCrossRefGoogle Scholar
  45. Phelan P, Starich TA (2001) Innexins get into the gap. BioEssays 23:388–396PubMedCrossRefGoogle Scholar
  46. Phelan P, Bacon JP, Davies JA, et al (1999) Innexins: a family of invertebrate gap-junction proteins. Trends Genet 14:348–349CrossRefGoogle Scholar
  47. Rubin GM, Yandell MD, Wortman JR, et al (2000) Comparative genomics of the eukaryotes. Science 287:2204–2215PubMedCrossRefGoogle Scholar
  48. Saitou M, Fujimoto K, Doi Y, Itoh M, Fujimoto T, Furuse M, Takano H, Noda T, Tsukita S (1998) Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J Cell Biol 141:397–408PubMedCrossRefGoogle Scholar
  49. 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/s00427-003-325-9Google Scholar
  50. Satou Y, Chiba S, Satoh N (1999) Expression cloning of an ascidian syndecan suggests its role in embryonic cell adhesion and morphogenesis. Dev Biol 211:198–207PubMedCrossRefGoogle Scholar
  51. Satou Y, Imai KS, Satoh N (2001) Early embryonic expression of a LIM-homeobox gene Cs-lhx3 is downstream of β-catenin and responsible for the endoderm differentiation in Ciona savignyi embryos. Development 128:3559–3570PubMedGoogle Scholar
  52. 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 (2002) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33:153–154PubMedCrossRefGoogle Scholar
  53. 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/s00427-003-319-7Google Scholar
  54. Selleck SB (2000) Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. Trends Genet 16:206–212PubMedCrossRefGoogle Scholar
  55. Sharma CP, Ezzell RM, Arnaout MA (1995) Direct interaction of filamin (ABP-280) with the beta 2-integrin subunit CD18. J Immunol 154:3461–3470PubMedGoogle Scholar
  56. Tepass U (2002) Adherens junctions: new insight into assembly, modulation and function. BioEssays 24:690–695PubMedCrossRefGoogle Scholar
  57. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nature Rev Mol Cell Biol 2:285–293CrossRefGoogle Scholar
  58. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, Schwartz TL, Takeichi M, Uemura T (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of frizzled. Cell 98:585–595PubMedCrossRefGoogle Scholar
  59. 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 91:1801–1804PubMedCrossRefGoogle Scholar
  60. Wang J, Karabinos A, Zimek A, Meyer M, Riemer D, Hudson C, Lemaire P, Weber K (2002) Cytoplasmic intermediate filament protein expression in tunicate development: a specific marker for the test cells. Eur J Cell Biol 81:302–311PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Yasunori Sasakura
    • 1
  • Eiichi Shoguchi
    • 1
  • Naohito Takatori
    • 1
  • Shuichi Wada
    • 1
  • Ian A. Meinertzhagen
    • 2
  • Yutaka Satou
    • 1
  • Nori Satoh
    • 1
    Email author
  1. 1.Department of Zoology, Graduate School of ScienceKyoto UniversityKyoto 606-8502Japan
  2. 2.Life Sciences CentreDalhousie UniversityHalifaxCanada B3H 4J1

Personalised recommendations