Tube formation by complex cellular processes in Ciona intestinalis notochord.

TitleTube formation by complex cellular processes in Ciona intestinalis notochord.
Publication TypeJournal Article
Year of Publication2009
AuthorsDong B, Horie T, Denker E, Kusakabe T, Tsuda M, Smith WC, Jiang D
JournalDev Biol
Volume330
Issue2
Pagination237-49
Date Published2009 Jun 15
ISSN1095-564X
KeywordsAnimals, Base Sequence, Cell Movement, Ciona intestinalis, DNA Primers, Electroporation, Immunohistochemistry, Intercellular Junctions, Microscopy, Confocal, Notochord
Abstract

In the course of embryogenesis multicellular structures and organs are assembled from constituent cells. One structural component common to many organs is the tube, which consists most simply of a luminal space surrounded by a single layer of epithelial cells. The notochord of ascidian Ciona forms a tube consisting of only 40 cells, and serves as a hydrostatic "skeleton" essential for swimming. While the early processes of convergent extension in ascidian notochord development have been extensively studied, the later phases of development, which include lumen formation, have not been well characterized. Here we used molecular markers and confocal imaging to describe tubulogenesis in the developing Ciona notochord. We found that during tubulogenesis each notochord cell established de novo apical domains, and underwent a mesenchymal-epithelial transition to become an unusual epithelial cell with two opposing apical domains. Concomitantly, extracellular luminal matrix was produced and deposited between notochord cells. Subsequently, each notochord cell simultaneously executed two types of crawling movements bi-directionally along the anterior/posterior axis on the inner surface of notochordal sheath. Lamellipodia-like protrusions resulted in cell lengthening along the anterior/posterior axis, while the retraction of trailing edges of the same cell led to the merging of the two apical domains. As a result, the notochord cells acquired endothelial-like shape and formed the wall of the central lumen. Inhibition of actin polymerization prevented the cell movement and tube formation. Ciona notochord tube formation utilized an assortment of common and fundamental cellular processes including cell shape change, apical membrane biogenesis, cell/cell adhesion remodeling, dynamic cell crawling, and lumen matrix secretion.

DOI10.1016/j.ydbio.2009.03.015
Alternate JournalDev. Biol.
PubMed ID19324030
PubMed Central IDPMC2841060
Grant ListHD038701 / HD / NICHD NIH HHS / United States
R01 HD038701-06A1 / HD / NICHD NIH HHS / United States
R01 HD038701-09 / HD / NICHD NIH HHS / United States