Venkataraman Vishruth, McGrory Noel H, Christiansen Theresa J, Acedo Joaquin Navajas, Coates Michael I, Prince Victoria E
Department of Organismal Biology & Anatomy, The University of Chicago, Chicago, IL, 60637, USA.
Stowers Institute for Medical Research, Kansas City, MO, 64110, USA.
Dev Biol. 2025 Sep;525:102-121. doi: 10.1016/j.ydbio.2025.05.025. Epub 2025 May 29.
The mechanosensory lateral line system of aquatic vertebrates comprises a superficial network of distributed sensory organs, the neuromasts, which are arranged over the head and trunk and innervated by lateral line nerves to allow detection of changes in water flow and pressure. While the well-studied zebrafish posterior lateral line has emerged as a powerful model to study collective cell migration, far less is known about development of the anterior lateral line, which produces the supraorbital and infraorbital lines around the eye, as well as mandibular and opercular lines over the jaw and cheek. Here we show that normal development of the zebrafish anterior lateral line system from cranial placodes is dependent on another vertebrate-specific cell type, the cranial neural crest. We find that cranial neural crest and anterior lateral lines develop in close proximity, with absence of neural crest cells leading to major disruptions in the overlying anterior lateral line system. Specifically, in the absence of neural crest neither supraorbital nor infraorbital lateral lines fully extend, such that the most anterior cranial regions remain devoid of neuromasts, while supernumerary ectopic neuromasts form in the posterior supraorbital region. Both neural crest and cranial placodes contribute neurons to the lateral line ganglia that innervate the neuromasts and in the absence of neural crest these ganglia, as well as the lateral line afferent nerves, are disrupted. Finally, we establish that as ontogeny proceeds, the most anterior supraorbital neuromasts come to lie within neural crest-derived frontal and nasal bones in the developing cranium. These are the same anterior supraorbital neuromasts that are absent or mislocated in specimens lacking neural crest cells. Together, our results establish that cranial neural crest and cranial placode derivatives function in concert over the course of ontogeny to build the complex cranial lateral line system.
水生脊椎动物的机械感觉侧线系统由分布的感觉器官——神经丘组成的浅表网络构成，这些神经丘排列在头部和躯干上，并由侧线神经支配，以检测水流和压力的变化。虽然经过充分研究的斑马鱼后侧线已成为研究集体细胞迁移的强大模型，但对于前侧线的发育却知之甚少，前侧线会在眼睛周围产生眶上和眶下线，以及在颌骨和脸颊上产生下颌线和鳃盖线。在这里，我们表明斑马鱼前侧线系统从颅基板正常发育依赖于另一种脊椎动物特有的细胞类型——颅神经嵴。我们发现颅神经嵴和前侧线在附近发育，没有神经嵴细胞会导致覆盖其上的前侧线系统出现重大破坏。具体而言，在没有神经嵴的情况下，眶上和眶下侧线都不能完全延伸，使得最前面的颅部区域仍然没有神经丘，而在眶上后部区域会形成多余的异位神经丘。神经嵴和颅基板都为支配神经丘的侧线神经节贡献神经元，并且在没有神经嵴的情况下，这些神经节以及侧线传入神经都会受到破坏。最后，我们确定随着个体发育的进行，最前面的眶上神经丘会位于发育中的颅骨中神经嵴衍生的额骨和鼻骨内。这些就是在缺乏神经嵴细胞的标本中缺失或位置错误的相同的眶上前神经丘。总之，我们的结果表明颅神经嵴和颅基板衍生物在个体发育过程中协同作用，构建复杂的颅侧线系统。
