Gurjar Mansa, Amanipour Reza, Balendran Vinodh, Ghimire Satish, Demirhan Mehmet Alp, Flynn Alexander J, Seernaum Nidhee, Rose Kevin P, Song Yang, Hertzano Ronna, Coate Thomas M
Department of Biology, Georgetown University, Washington DC, United States.
Department of Otorhinolaryngology, University of Maryland School of Medicine, Baltimore, MD, United States; Neurotology Branch, National Institute on Deafness and Other Communication Disorders, Intramural Research Program, Bethesda, MD, United States.
Dev Biol. 2025 Aug;524:176-189. doi: 10.1016/j.ydbio.2025.05.002. Epub 2025 May 7.
During the formation of the auditory system in mammals, spiral ganglion neurons (SGNs) form ribbon-type synapses with hair cells in the cochlea to establish the first "sensorineural" component of sound transduction. Ahead of synapse formation in the cochlea, the SGNs undergo migration and extension with developing Schwann and otic mesenchyme cells to form radial bundles, fasciculated groups of nerve fibers found between the SGN somata and hair cells. Thus far, reports have shown that Eph/Ephrin signaling is important for the formation of radial bundles. Here, we show that EPHRIN-A1 and -A2 are broadly expressed in the developing cochlea during periods of SGN peripheral axon extension. Confronting spiral ganglion explants with either EPHRIN-A1- or -A2-Fc in vitro promoted neurite extension and reduced fasciculation. EPHRIN-A1- or -A2-Fc treatments also led to increased levels of phosphorylated ERBB2 immunoreactivity in Schwann cells, suggesting a role for developing glia. Loss of Efna1 and Efna2 in mouse models led to approximately a 25 % reduction in SGN peripheral axon extension, an effect that was maintained into adulthood. Overall, the data presented here indicate that EPHRIN-A1 and -A2 are important for normal patterns of cochlear innervation in that they serve as positive growth factors for developing radial bundles, possibly by stimulating Schwann cells.
在哺乳动物听觉系统形成过程中,螺旋神经节神经元(SGNs)与耳蜗中的毛细胞形成带状突触,以建立声音传导的首个“感觉神经”成分。在耳蜗突触形成之前,SGNs与发育中的施万细胞和耳间质细胞一起迁移和延伸,形成放射状束,即SGN胞体和毛细胞之间的成束神经纤维群。迄今为止,报告显示Eph/Ephrin信号传导对放射状束的形成很重要。在此,我们表明EPHRIN-A1和-A2在SGN外周轴突延伸期间在发育中的耳蜗中广泛表达。在体外将螺旋神经节外植体与EPHRIN-A1或-A2-Fc接触可促进神经突延伸并减少成束。EPHRIN-A1或-A2-Fc处理还导致施万细胞中磷酸化ERBB2免疫反应性水平升高,提示发育中的神经胶质细胞发挥了作用。小鼠模型中Efna1和Efna2的缺失导致SGN外周轴突延伸减少约25%,这种影响持续到成年期。总体而言,此处呈现的数据表明EPHRIN-A1和-A2对正常耳蜗神经支配模式很重要,因为它们可能通过刺激施万细胞,作为发育中放射状束的正向生长因子。