Development Genes and Evolution

, Volume 213, Issue 5–6, pp 273–283 | Cite as

A genomewide survey of developmentally relevant genes in Ciona intestinalis

VII. Molecules involved in the regulation of cell polarity and actin dynamics
  • Yasunori Sasakura
  • Lixy Yamada
  • Naohito Takatori
  • Yutaka Satou
  • Nori Satoh
Original Article


In the present study, genes involved in the pathways that establish cell polarity and cascades regulating actin dynamics were identified in the completely sequenced genome of Ciona intestinalis, a basal chordate. It was revealed that the Ciona genome contains orthologous genes of each component of aPKC-Par and PCP pathways and WASP/WAVE/SCAR and ADF/cofilin cascades, with less redundancy than the vertebrate genomes, suggesting that the conserved pathways/cascades function in Ciona development. In addition, the present study found that the orthologous proteins of five gene groups (Tc10, WRCH, RhoD, PLC-L, and PSKH) are conserved in humans and Ciona but not in Drosophila melanogaster, suggesting a similarity in the gene composition of Ciona to that of vertebrates. Ciona intestinalis, therefore, may provide refined clues for the study of vertebrate development and evolution.


Actin dynamics Basal chordates Cell polarity Ciona intestinalis Genomewide survey 

Supplementary material (465 kb)
Supplementary material, approximately 476 KB.


  1. Aelst LV, Symons M (2002) Role of Rho family GTPase in epithelial morphogenesis. Genes Dev 16:1032–1054PubMedCrossRefGoogle Scholar
  2. Blot J, Chartrain I, Roghi C, Philippe M, Tassan JP (2002) Cell cycle regulation of pEg3, a new Xenopus protein kinase of the KIN1/PAR-1/MARK family. Dev Biol 241:327–338PubMedCrossRefGoogle Scholar
  3. 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
  4. Choi S, Han J (2002) Xenopus CDC42 regulates convergent extension movement during gastrulation through Wnt/Ca2+ signaling pathway. Dev Biol 244:342–357PubMedCrossRefGoogle Scholar
  5. Conklin EG (1905a) The organization and cell lineage of the ascidian egg. J Acad Natl Sci 13:1–119Google Scholar
  6. Conklin EG (1905b) Organ-forming substances in the eggs of ascidians. Biol Bull Mar Biol Lab Woods Hole 8:205–230CrossRefGoogle Scholar
  7. Darken RS, Scola AM, Rakeman AS, Das G, Mlodzik M, Wilson PA (2002) The planar polarity gene strabismus regulates convergent extension movement in Xenopus. EMBO J 21:976–985PubMedCrossRefGoogle Scholar
  8. 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
  9. Emmons S, Phan H, Calley J, Chen W, James B, Manseau L (1995) cappuccino, a Drosophila maternal effect gene required for polarity of the egg and embryo, is related to the vertebrate limb deformity locus. Genes Dev 9:2482–2494PubMedCrossRefGoogle Scholar
  10. Erickson JW, Cerione RA (2001) Multiple roles for Cdc42 in cell regulation. Curr Opin Cell Biol 13:153–157PubMedCrossRefGoogle Scholar
  11. Ferl RJ, Manak MS, Reyers MF (2002) The 14-3-3s. Genome Biol 3:3010.1–3010.7CrossRefGoogle Scholar
  12. Habas R, Kato Y, He X (2001) Wnt/Frizzled activation of Rho regulation vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107:843–854PubMedCrossRefGoogle Scholar
  13. 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 (in press)Google Scholar
  14. Hotta K, Takahashi H, Asakura T, Saito 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
  15. Jaffer ZM, Chernoff J (2002) p21-activated kinases; three more join the Pak. Int J Biochem Cell Biol 34:713–717PubMedCrossRefGoogle Scholar
  16. Katoh M (2002) Molecular cloning and characterization of WRCH2 on human chromosome 15q15. Int J Oncol 20:977–982PubMedGoogle Scholar
  17. Kuhl M, Sheldahl LC, Park M, Miller JR, Moon RT (2000) The Wnt/Ca2+ pathway. Trends Genet 16:279–283PubMedCrossRefGoogle Scholar
  18. Kuhl M, Geis K, Sheldahl LC, Pukrop T, Moon RT, Wedlich D (2001) Antagonistic regulation of convergent extension movement in Xenopus by Wnt/β-catenin and Wnt/Ca2+ signaling. Mech Dev 106:61–76PubMedCrossRefGoogle Scholar
  19. Levitan DJ, Boyd L, Mello CC, Kemphues KJ, Stinchcomb DT (1994) par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proc Natl Acad Sci USA 91:6108–6112PubMedCrossRefGoogle Scholar
  20. Machesky LM, Reeves E, Wientjes F, Mattheyse FJ, Grogan A, Totty NF, Burlingame AL, Hsuan JJ, Segal AW (1997) Mammalian actin-related protein 2/3 complex localizes to regions of lamellipodial protrusion and is composed of evolutionarily conserved proteins. Biochem J 328:105–112PubMedGoogle Scholar
  21. Maciver SK, Hussey PJ (2002) The ADF/cofilin family: actin-remodeling proteins. Genome Biol 3:3007.1–3007.12CrossRefGoogle Scholar
  22. Miki H, Suetsugu S, Takenawa T (1998) WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J 17:6932–6941PubMedCrossRefGoogle Scholar
  23. Morton DG, Shakes DC, Nugent S, Dichoso D, Wang W, Golden A, Kemphues KJ (2002) The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev Biol 241: 47–58PubMedCrossRefGoogle Scholar
  24. Moscat J, Diaz-Meco MT (2000) The atypical protein kinase Cs. EMBO Rep 1:399–403PubMedCrossRefGoogle Scholar
  25. Munro EM, Odell GM (2002a) Morphogenetic pattern formation during ascidian notochord formation is regulative and highly robust. Development 129:1–12PubMedGoogle Scholar
  26. Munro EM, Odell GM (2002b) Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord. Development 129:13–24PubMedGoogle Scholar
  27. Myers DC, Sepich DS, Solnica-Krezel L (2002) Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? Trends Genet 18:447–455Google Scholar
  28. Niwa R, Nagata-Ohashi K, Takeichi M, Mizuno K, Uemura T (2002) Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/Cofilin. Cell 108:233–246PubMedCrossRefGoogle Scholar
  29. Ohno S (2001) Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol 13:641–648PubMedCrossRefGoogle Scholar
  30. Palmer RH, Ridden J, Parker PJ (1995) Cloning and expression patterns of two members of a novel protein-kinase-C-related kinase family. Eur J Biochem 15:344–351CrossRefGoogle Scholar
  31. Rappleye CA, Paredez AR, Smith CW, McDonald KL, Aroian RV (1999) The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode Caenorhabditis elegans. Genes Dev 13:2838–2851PubMedCrossRefGoogle Scholar
  32. Reverberi G (1975) Some effects of cytochalasin B on the eggs and tadpoles of ascidians. Acta Embryol Exp 1975:137–158Google Scholar
  33. Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T, Takenawa T, Kirschner MW (1999) The interaction between N-WASP and the Arp2/3 complex links cdc-42-dependent signals to actin assembly. Cell 97:221–231PubMedCrossRefGoogle Scholar
  34. Rose LS, Kemphues KJ (1998) Early patterning of the C. elegans embryo. Annu Rev Genet 32:521–545PubMedCrossRefGoogle Scholar
  35. Sasakura Y, Ogasawara M, Makabe KW (1998) Maternally localized RNA encoding a serine/threonine protein kinase in the ascidian, Halocynthia roretzi. Mech Dev 76:161–163PubMedCrossRefGoogle Scholar
  36. Sasakura Y, Ogasawara M, Makabe KW (2000) Two pathways of maternal RNA localization at the posterior-vegetal cytoplasm in early ascidian embryos. Dev Biol 220:365–378PubMedCrossRefGoogle Scholar
  37. Satou Y, Imai KS, Levine M, Kohara Y, Rokhsar D, Satoh N (2003a) A genomewide survey of developmentally relevant genes in Ciona intestinalis. I. Genes for bHLH transcription factors. Dev Genes Evol DOI 10.1007/s00427-003-0319-7Google Scholar
  38. Satou Y, Sasakura Y, Yamada L, Imai KS, Satoh N, Degnan B (2003b) A genomewide survey of developmentally relevant genes in Ciona intestinalis. V. Genes for receptor tyrosine kinase pathway and Notch signaling pathway. Dev Genes Evol DOI 10.1007/s00427-003-0317-9Google Scholar
  39. Sawada T, Osanai K (1981) The cortical contraction related to the ooplasmid segregation in Ciona intestinalis eggs. Roux's Arch Dev Biol 190:208–214CrossRefGoogle Scholar
  40. Soderling TR (1999) The Ca2+-calmodulin-dependent protein kinase cascade. Trends Biosci 24:232–236CrossRefGoogle Scholar
  41. Suetsugu S, Miki H, Takenawa T (2002) Spatial and temporal regulation of actin polymerization for cytoskeleton formation through Arp2/3 complex and WASP/WAVE proteins. Cell Motil Cytoskel 51:113–122CrossRefGoogle Scholar
  42. Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153–208PubMedGoogle Scholar
  43. Tao W, Pennica D, Xu L, Kalejta RF, Levine AJ (2001) Wrch-1, a novel member of the Rho gene family that is regulated by Wnt-1. Genes Dev 15:1796–1807PubMedCrossRefGoogle Scholar
  44. Tree DRP, Shulman JM, Rousset R, Scott MP, Gubb D, Axelrod JD (2002) Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109:371–381PubMedCrossRefGoogle Scholar
  45. Wallingford JB, Fraser SE, Harland RM (2002a) Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev Cell 2:695–706PubMedCrossRefGoogle Scholar
  46. Wallingford JB, Goto T, Keller R, Harland RM (2002b) Cloning and expression of Xenopus Prickle, an orthologue of a Drosophila planar cell polarity gene. Mech Dev 116:183–186PubMedCrossRefGoogle Scholar
  47. Webb BL, Hirst SJ, Giembycz MA (2000) Protein kinase C isoenzymes: a review of their structure, regulation and role in regulating airways smooth muscle tone and mitogenesis. Br J Pharm 130:1433–1452CrossRefGoogle Scholar
  48. Williams RL (1999) Mammalian phosphoinositide-specific phospholipase C. Biochim Biophys Acta 1441:255–267PubMedCrossRefGoogle Scholar
  49. Yoshida S, Satou Y, Satoh N (1997) Maternal genes with localized mRNA and pattern formation of the ascidian embryo. Cold Spring Harvor Symp Quant Biol 62:89–96CrossRefGoogle Scholar
  50. Zalokar M (1974) Effect of colchicine and cytochalasin B on ooplasmic segregation of ascidian eggs. Roux's Arch Dev Biol 175:243–248CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Yasunori Sasakura
    • 1
  • Lixy Yamada
    • 1
  • Naohito Takatori
    • 1
  • Yutaka Satou
    • 1
  • Nori Satoh
    • 1
  1. 1.Department of Zoology, Graduate School of ScienceKyoto UniversityKyoto 606–8502Japan

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