Adel Susannah S, Pranske Zachary J, Kowalski Tess F, Kanzler Nicole, Ray Roshni, Carmona Catherine, Paradis Suzanne
Department of Biology, Brandeis University, Waltham, MA 02454, United States.
bioRxiv. 2023 Oct 27:2023.10.27.564428. doi: 10.1101/2023.10.27.564428.
Synapse formation in the mammalian brain is a complex and dynamic process requiring coordinated function of dozens of molecular families such as cell adhesion molecules (CAMs) and ligand-receptor pairs (Ephs/Ephrins, Neuroligins/Neurexins, Semaphorins/Plexins). Due to the large number of molecular players and possible functional redundancies within gene families, it is challenging to determine the precise synaptogenic roles of individual molecules, which is key to understanding the consequences of mutations in these genes for brain function. Furthermore, few molecules are known to exclusively regulate either GABAergic or glutamatergic synapses, and cell and molecular mechanisms underlying GABAergic synapse formation in particular are not thoroughly understood. However, we previously demonstrated that Semaphorin-4D (Sema4D) regulates GABAergic synapse development in the mammalian hippocampus while having no effect on glutamatergic synapse development, and this effect occurs through binding to its high affinity receptor, Plexin-B1. Furthermore, Plexin-B2 contributes to GABAergic synapse formation as well but is not required for GABAergic synapse formation induced by binding to Sema4D. Here, we perform a structure-function study of the Plexin-B1 and Plexin-B2 receptors to identify the protein domains in each receptor that are required for its synaptogenic function. We also provide evidence that Plexin-B2 expression in presynaptic parvalbumin-positive interneurons is required for formation of GABAergic synapses onto excitatory pyramidal neurons in CA1. Our data reveal that Plexin-B1 and Plexin-B2 function non-redundantly to regulate GABAergic synapse formation and suggest that the transmembrane domain may underlie these functional distinctions. These findings lay the groundwork for future investigations into the precise signaling pathways required for synapse formation downstream of Plexin-B receptor signaling.
哺乳动物大脑中的突触形成是一个复杂且动态的过程,需要数十个分子家族的协同作用,如细胞粘附分子(CAMs)和配体 - 受体对(Ephs/Ephrins、Neuroligins/Neurexins、Semaphorins/Plexins)。由于基因家族中分子参与者众多且可能存在功能冗余,确定单个分子的确切突触形成作用具有挑战性,而这对于理解这些基因突变对脑功能的影响至关重要。此外,已知很少有分子专门调节GABA能或谷氨酸能突触,特别是GABA能突触形成的细胞和分子机制尚未完全了解。然而,我们之前证明,Semaphorin - 4D(Sema4D)调节哺乳动物海马体中的GABA能突触发育,而对谷氨酸能突触发育没有影响,并且这种作用是通过与高亲和力受体Plexin - B1结合而发生的。此外,Plexin - B2也有助于GABA能突触形成,但对于与Sema4D结合诱导的GABA能突触形成不是必需的。在这里,我们对Plexin - B1和Plexin - B2受体进行结构 - 功能研究,以确定每个受体中其突触形成功能所需的蛋白质结构域。我们还提供证据表明,突触前小白蛋白阳性中间神经元中Plexin - B2的表达是在CA1区兴奋性锥体神经元上形成GABA能突触所必需的。我们的数据表明,Plexin - B1和Plexin - B2在调节GABA能突触形成方面功能并非冗余,并表明跨膜结构域可能是这些功能差异的基础。这些发现为未来研究Plexin - B受体信号下游突触形成所需的精确信号通路奠定了基础。