The roles of maternal Vangl2 and aPKC inXenopusoocyte and embryo patterning

Abstract

SUMMARYThe Xenopus oocyte contains components of both the planar cell polarity and apical-basal polarity pathways, but their roles are not known. Here, we examine the distribution, interactions and functions of the maternal planar cell polarity core protein Vangl2 and the apical-basal complex component aPKC. We show that Vangl2 is distributed in animally enriched islands in the subcortical cytoplasm in full-grown oocytes, where it interacts with a post-Golgi v-SNARE protein, VAMP1, and acetylated microtubules. We find that Vangl2 is required for the stability of VAMP1 as well as for the maintenance of the stable microtubule architecture of the oocyte. We show that Vangl2 interacts with atypical PKC, and that both the acetylated microtubule cytoskeleton and the Vangl2-VAMP1 distribution are dependent on the presence of aPKC. We also demonstrate that aPKC and Vangl2 are required for the cell membrane asymmetry that is established during oocyte maturation, and for the asymmetrical distribution of maternal transcripts for the germ layer and dorsal/ventral determinants VegT and Wnt11. This study demonstrates the interaction and interdependence of Vangl2, VAMP1, aPKC and the stable microtubule cytoskeleton in the oocyte, shows that maternal Vangl2 and aPKC are required for specific oocyte asymmetries and vertebrate embryonic patterning, and points to the usefulness of the oocyte as a model to study the polarity problem.

Spatial and temporal aspects of Wnt signaling and planar cell polarity during vertebrate embryonic development

“…Indeed, both cortical and nuclear enrichment of β-catenin is known to take place in worm embryonic cells in response to different Wnt signaling branches (Sawa, 2012; Schneider and Bowerman, 2007; Sugioka et al, 2011). Consistent with the above hypothesis, Vangl2 has been proposed to play a role in Xenopus oocyte polarity (Cha et al, 2011). Additional experiments are warranted to investigate these new functions of PCP proteins in animal-vegetal and dorsal-ventral axis specification.…”

VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration

“…Recruitment of fly Van Gogh to the plasma membrane is thought to be a crucial event for PCP signaling in epithelial cells (Strutt and Strutt, 2009). However, recent in vitro and in vivo studies have identified VANGL2 expression within vesicular compartments (Merte et al, 2010;Cha et al, 2011). VANGL2 and MMP14 colocalization in HT-1080 cells was detected at the plasma membrane ( Fig.…”

Vangl2 cooperates with Rab11 and Myosin V to regulate apical constriction during vertebrate gastrulation

“…These observations further expand the spectrum of PCP-associated morphogenetic processes. Besides planar epithelial polarity, PCP proteins were reported to affect mitotic spindle orientation and cell differentiation (Bellaiche et al, 2004;Cortijo et al, 2012;Lake and Sokol, 2009), cilia positioning (Hashimoto et al, 2010;Song et al, 2010), axon guidance (Lyuksyutova et al, 2003;Tissir and Goffinet, 2013), apical-basal polarity , oocyte development (Cha et al, 2011) and migration of endodermal (Trichas et al, 2012), germ cell (Laird et al, 2011) and neuronal progenitors (Carreira-Barbosa et al, 2003;Glasco et al, 2012;Jessen et al, 2002). Additionally, Vangl2 and Rock are involved in lung branching morphogenesis (Yates et al, 2010b), and both Vangl2 and Daam1 were reported to function in kidney tubulogenesis (Miller et al, 2011;Yates et al, 2010a).…”