Department of Cell Biology, University of Virginia Health System, Charlottesville, VA 22908.
Proc Natl Acad Sci U S A. 2024 Aug 27;121(35):e2405217121. doi: 10.1073/pnas.2405217121. Epub 2024 Aug 22.
Intercellular signaling mediated by evolutionarily conserved planar cell polarity (PCP) proteins aligns cell polarity along the tissue plane and drives polarized cell behaviors during tissue morphogenesis. Accumulating evidence indicates that the vertebrate PCP pathway is regulated by noncanonical, β-catenin-independent Wnt signaling; however, the signaling components and mechanisms are incompletely understood. In the mouse hearing organ, both PCP and noncanonical Wnt (ncWnt) signaling are required in the developing auditory sensory epithelium to control cochlear duct elongation and planar polarity of resident sensory hair cells (HCs), including the shape and orientation of the stereociliary hair bundle essential for sound detection. We have recently discovered a Wnt/G-protein/PI3K pathway that coordinates HC planar polarity and intercellular PCP signaling. Here, we identify Wnt7b as a ncWnt ligand acting in concert with Wnt5a to promote tissue elongation in diverse developmental processes. In the cochlea, Wnt5a and Wnt7b are redundantly required for cochlear duct coiling and elongation, HC planar polarity, and asymmetric localization of core PCP proteins Fzd6 and Dvl2. Mechanistically, Wnt5a/Wnt7b-mediated ncWnt signaling promotes membrane recruitment of Daple, a nonreceptor guanine nucleotide exchange factor for Gαi, and activates PI3K/AKT and ERK signaling, which promote asymmetric Fzd6 localization. Thus, ncWnt and PCP signaling pathways have distinct mutant phenotypes and signaling components, suggesting that they act as separate, parallel pathways with nonoverlapping functions in cochlear morphogenesis. NcWnt signaling drives tissue elongation and reinforces intercellular PCP signaling by regulating the trafficking of PCP-specific Frizzled receptors.
细胞间信号转导由进化保守的平面细胞极性(PCP)蛋白介导,沿组织平面排列细胞极性,并在组织形态发生过程中驱动极化细胞行为。越来越多的证据表明,脊椎动物 PCP 途径受非典型、β-连环蛋白非依赖性 Wnt 信号调节;然而,信号成分和机制尚不完全清楚。在小鼠听力器官中,发育中的听觉感觉上皮细胞中既需要 PCP 又需要非典型 Wnt(ncWnt)信号,以控制耳蜗管伸长和驻留感觉毛细胞(HCs)的平面极性,包括对声音检测至关重要的静纤毛毛发束的形状和方向。我们最近发现了一个 Wnt/G 蛋白/PI3K 途径,该途径协调 HC 平面极性和细胞间 PCP 信号转导。在这里,我们鉴定出 Wnt7b 是一种 ncWnt 配体,与 Wnt5a 协同作用,促进各种发育过程中的组织伸长。在耳蜗中,Wnt5a 和 Wnt7b 对于耳蜗管卷曲和伸长、HC 平面极性以及核心 PCP 蛋白 Fzd6 和 Dvl2 的不对称定位都是冗余的。从机制上讲,Wnt5a/Wnt7b 介导的 ncWnt 信号转导促进了 Daple 的膜募集,Daple 是 Gαi 的非受体鸟嘌呤核苷酸交换因子,并激活了 PI3K/AKT 和 ERK 信号转导,促进了 Fzd6 的不对称定位。因此,ncWnt 和 PCP 信号通路具有不同的突变表型和信号成分,表明它们在耳蜗形态发生中作为独立的、平行的途径发挥作用,具有非重叠的功能。ncWnt 信号通过调节 PCP 特异性 Frizzled 受体的运输来驱动组织伸长并增强细胞间 PCP 信号。