Department of Anatomy and Cell Biology, Carver College of Medicine, The University of Iowa, Iowa City, IA 52242, USA.
Development. 2021 Jul 15;148(14). doi: 10.1242/dev.199421. Epub 2021 Jul 12.
Noncanonical Wnt/planar cell polarity (Wnt/PCP) signaling has been implicated in endoderm morphogenesis. However, the underlying cellular and molecular mechanisms of this process are unclear. We found that, during convergence and extension (C&E) in zebrafish, gut endodermal cells are polarized mediolaterally, with GFP-Vangl2 enriched at the anterior edges. Endoderm cell polarity is lost and intercalation is impaired in the absence of glypican 4 (gpc4), a heparan-sulfate proteoglycan that promotes Wnt/PCP signaling, suggesting that this signaling is required for endodermal cell polarity. Live imaging revealed that endoderm C&E is accomplished by polarized cell protrusions and junction remodeling, which are impaired in gpc4-deficient endodermal cells. Furthermore, in the absence of gpc4, Cadherin 2 expression on the endodermal cell surface is increased as a result of impaired Rab5c-mediated endocytosis, which partially accounts for the endodermal defects in these mutants. These findings indicate that Gpc4 regulates endodermal planar cell polarity during endoderm C&E by influencing the localization of Cadherin 2. Thus, our study uncovers a new mechanism by which Gpc4 regulates planar cell polarity and reveals the role of Wnt/PCP signaling in endoderm morphogenesis.
非经典 Wnt/平面细胞极性(Wnt/PCP)信号通路参与了内胚层形态发生。然而,这一过程的潜在细胞和分子机制尚不清楚。我们发现,在斑马鱼的会聚延伸(C&E)过程中,肠道内胚层细胞沿中侧方向极化,GFP-Vangl2 在前端边缘富集。在缺乏硫酸乙酰肝素蛋白聚糖 4(gpc4)的情况下,内胚层细胞极性丧失且细胞内陷受损,gpc4 是促进 Wnt/PCP 信号通路的蛋白,表明这一信号通路对内胚层细胞极性的形成是必需的。实时成像显示,内胚层的 C&E 通过极化细胞突起和连接重塑来完成,而 gpc4 缺陷的内胚层细胞中的这些过程受损。此外,在 gpc4 缺失的情况下,内胚层细胞表面 Cadherin 2 的表达增加,这是由于 Rab5c 介导的内吞作用受损所致,这部分解释了这些突变体中内胚层的缺陷。这些发现表明,Gpc4 通过影响 Cadherin 2 的定位来调节内胚层 C&E 期间的内胚层平面细胞极性。因此,我们的研究揭示了 Gpc4 通过影响 Cadherin 2 的定位来调节平面细胞极性的新机制,并揭示了 Wnt/PCP 信号通路在肠内胚层形态发生中的作用。