Committee on Development, Regeneration and Stem Cell Biology, The University of Chicago, USA.
Department of Organismal Biology and Anatomy, The University of Chicago, USA.
Dev Biol. 2019 Apr 1;448(1):16-35. doi: 10.1016/j.ydbio.2019.01.018. Epub 2019 Feb 2.
The neural crest-a key innovation of the vertebrates-gives rise to diverse cell types including melanocytes, neurons and glia of the peripheral nervous system, and chondrocytes of the jaw and skull. Proper development of the cephalic region is dependent on the tightly-regulated specification and migration of cranial neural crest cells (NCCs). The core PCP proteins Frizzled and Disheveled have previously been implicated in NCC migration. Here we investigate the functions of the core PCP proteins Prickle1a and Prickle1b in zebrafish cranial NCC development. Using analysis of pk1a and pk1b mutant embryos, we uncover similar roles for both genes in facilitating cranial NCC migration. Disruption of either gene causes pre-migratory NCCs to cluster together at the dorsal aspect of the neural tube, where they adopt aberrant polarity and movement. Critically, in investigating Pk1-deficient cells that fail to migrate ventrolaterally, we have also uncovered roles for pk1a and pk1b in the epithelial-to-mesenchymal transition (EMT) of pre-migratory NCCs that precedes their collective migration to the periphery. Normally, during EMT, pre-migratory NCCs transition from a neuroepithelial to a bleb-based and subsequently, mesenchymal morphology capable of directed migration. When either Pk1a or Pk1b is disrupted, NCCs continue to perform blebbing behaviors characteristic of pre-migratory cells over extended time periods, indicating a block in a key transition during EMT. Although some Pk1-deficient NCCs transition successfully to mesenchymal, migratory morphologies, they fail to separate from neighboring NCCs. Additionally, Pk1b-deficient NCCs show elevated levels of E-Cadherin and reduced levels of N-Cadherin, suggesting that Prickle1 molecules regulate Cadherin levels to ensure the completion of EMT and the commencement of cranial NCC migration. We conclude that Pk1 plays crucial roles in cranial NCCs both during EMT and migration. These roles are dependent on the regulation of E-Cad and N-Cad.
神经嵴——脊椎动物的关键创新——产生了多种细胞类型,包括黑色素细胞、神经元和周围神经系统的神经胶质细胞,以及颌骨和颅骨的软骨细胞。头部区域的正常发育依赖于颅神经嵴细胞(NCC)的严格调节的特异性和迁移。核心 PCP 蛋白 Frizzled 和 Disheveled 先前被认为参与了 NCC 的迁移。在这里,我们研究了核心 PCP 蛋白 Prickle1a 和 Prickle1b 在斑马鱼颅 NCC 发育中的作用。通过分析 pk1a 和 pk1b 突变体胚胎,我们发现这两个基因在促进颅 NCC 迁移方面具有相似的作用。破坏任一基因都会导致前迁移 NCC 在神经管的背侧聚集在一起,在那里它们采用异常的极性和运动。至关重要的是,在研究未能向腹外侧迁移的 Pk1 缺陷细胞时,我们还发现 pk1a 和 pk1b 在迁移前 NCC 的上皮间质转化(EMT)中发挥作用,该过程先于它们向周围的集体迁移。正常情况下,在 EMT 过程中,前迁移的 NCC 从神经上皮细胞过渡到以小泡为基础的形态,随后过渡到能够定向迁移的间质形态。当 Pk1a 或 Pk1b 被破坏时,NCC 会在较长时间内继续表现出前迁移细胞特有的小泡行为,表明 EMT 过程中的一个关键转变被阻断。尽管一些 Pk1 缺陷的 NCC 成功地过渡到间质、迁移形态,但它们不能与相邻的 NCC 分离。此外,Pk1b 缺陷的 NCC 表现出 E-Cadherin 水平升高和 N-Cadherin 水平降低,表明 Prickle1 分子调节 Cadherin 水平以确保 EMT 的完成和颅 NCC 迁移的开始。我们得出结论,Pk1 在 EMT 和迁移过程中对颅 NCC 发挥着至关重要的作用。这些作用依赖于 E-Cad 和 N-Cad 的调节。