Elongation of Axolotl Tailbud Embryos Requires GPI-Linked Proteins and Organizer-Induced, Active, Ventral Trunk Endoderm Cell Rearrangements

Abstract

Application of phosphatidylinositol-specific phospholipase C to early tailbud stage axolotl embryos reveals that a specific subset of morphogenetic movements requires glycosylphosphatidylinositol (GPI)-linked cell-surface proteins. These include pronephric duct extension, "gill bulge" formation, and embryonic elongation along the anteroposterior axis. The work of Kitchin (1949, J. Exp. Zool. 112, 393-416) led to the conclusion that extension of the notochord provided the motive force driving anteroposterior stretching in axolotl embryos, elongation of other tissues being a passive response. We therefore conjectured that axial mesoderm cells might display the GPI-linked proteins required for elongation of the embryo. However, we show here that removal of most of the neural plate and axial and paraxial mesoderm prior to neural tube closure does not prevent elongation of ventrolateral tissues. Tissue-extirpation and tissue-marking experiments indicate that elongation of the ventral trunk occurs via active, directed tissue rearrangements within the endoderm, directed by signals emanating from the blastopore region. Extension of both dorsal and ventral tissues requires GPI-linked proteins. We conclude that elongation of axolotl embryos requires active cell rearrangements within ventral as well as axial tissues. The fact that both types of elongation are prevented by removal of GPI-linked proteins implies that they share a common molecular mechanism.

Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB

“…In Keller explants, both neural and mesodermal tissues undergo active, mechanically independent CE (Keller and Danilchik, 1988), but in whole embryos, the extension of the neural tissue occurs in parallel to and is mechanically coupled to the extension of the underlying mesodermal tissues, particularly during neurulation (Keller et al, 1992b). In tailbud stages, both these dorsal tissues may be mechanically coupled to the ventral part of the embryo, which also extends at these stages, causing a straightening of the trunk in anurans (Larkin and Danilchik, 1999) and in urodeles (Drawbridge and Steinberg, 2000). Thus failure of neural extension, mesodermal extension, or both, could slow extension of the dorsal side relative to the ventral side, and thus result in dorsal flexure.…”

Convergent extension movements in growth plate chondrocytes require gpi-anchored cell surface proteins

“…The requirement for gpi-anchored proteins for polarized cell movements in cartilage and in axis formation in the axolotol and zebrafish suggests that gpi-anchored proteins are general components of polarity pathways (Drawbridge and Steinberg, 2000;Topczewski et al, 2001;Shao et al, 2009). We tested this hypothesis using the sensory epithelium of the vertebrate inner ear.…”

“…Orientation of the division plane and the stacking of chondrocytes depend on non-canonical frizzled (Fzd) signaling and Rho GTPase activity, two components of pathways that additionally regulate CE movements in the neural tube and planar cell polarity (PCP) in epithelial tissues (Klein and Mlodzik, 2005). Proteins displayed on the cell surface via glycosylphosphatidylinositol (gpi) linkages are also important components of the CE pathway (Topoczewski et al, 2001;Shao et al, 2009), and reduction in gpi-anchored proteins affects CE in the axolotl and zebrafish (Drawbridge and Steinberg, 2000;Shao et al, 2009). Therefore, we sought to determine whether gpi-anchored proteins are also key regulators of CE and PCP in other tissues.…”

Tissue fusion and cell sorting in embryonic development and disease: biomedical implications

“…Elongation and straightening of the embryo from gastrula to tailbud stage requires active cell rearrangements within ventral as well as axial tissues. (87) This dynamic movement from organizer to notochord depends largely on prenotochord cell sorting. (88) The process of gastrulation in chordates takes place by various pathways yet the end-product is invariably the same: an embryo composed of three layers each spatially arranged to reflect the basic body plan.…”