Hoglund Biomedical Imaging Center, University of Kansas Medical Center, Kansas City, Kansas, USA.
Department of Radiology, University of Kansas Medical Center, Kansas City, Kansas, USA.
J Neurochem. 2024 May;168(5):719-727. doi: 10.1111/jnc.16035. Epub 2023 Dec 20.
The excitatory neurotransmitter glutamate has a role in neuronal migration and process elongation in the central nervous system (CNS). The effects of chronic glutamate hyperactivity on vesicular and protein transport within CNS neurons, that is, processes necessary for neurite growth, have not been examined previously. In this study, we measured the effects of lifelong hyperactivity of glutamate neurotransmission on axoplasmic transport in CNS neurons. We compared wild-type (wt) to transgenic (Tg) mice over-expressing the glutamate dehydrogenase gene Glud1 in CNS neurons and exhibiting increases in glutamate transmitter formation, release, and synaptic activation in brain throughout the lifespan. We found that Glud1 Tg as compared with wt mice exhibited increases in the rate of anterograde axoplasmic transport in neurons of the hippocampus measured in brain slices ex vivo, and in olfactory neurons measured in vivo. We also showed that the in vitro pharmacologic activation of glutamate synapses in wt mice led to moderate increases in axoplasmic transport, while exposure to selective inhibitors of ion channel forming glutamate receptors very significantly suppressed anterograde transport, suggesting a link between synaptic glutamate receptor activation and axoplasmic transport. Finally, axoplasmic transport in olfactory neurons of Tg mice in vivo was partially inhibited following 14-day intake of ethanol, a known suppressor of axoplasmic transport and of glutamate neurotransmission. The same was true for transport in hippocampal neurons in slices from Glud1 Tg mice exposed to ethanol for 2 h ex vivo. In conclusion, endogenous activity at glutamate synapses regulates and glutamate synaptic hyperactivity increases intraneuronal transport rates in CNS neurons.
兴奋性神经递质谷氨酸在中枢神经系统(CNS)中神经元迁移和突起伸长过程中起作用。慢性谷氨酸过度活跃对 CNS 神经元囊泡和蛋白质运输的影响,即轴突生长所必需的过程,以前尚未被研究过。在这项研究中,我们测量了一生中谷氨酸神经传递过度活跃对 CNS 神经元轴浆运输的影响。我们比较了野生型(wt)和过表达中枢神经系统神经元谷氨酸脱氢酶基因 Glud1 的转基因(Tg)小鼠,这些小鼠在整个生命过程中表现出谷氨酸递质形成、释放和突触激活增加。我们发现,与 wt 小鼠相比,Glud1 Tg 小鼠在脑片体外测量的海马神经元中顺行轴浆运输速度增加,在体内测量的嗅神经元中也增加。我们还表明,wt 小鼠中谷氨酸突触的体外药理学激活导致轴浆运输适度增加,而离子通道形成谷氨酸受体的选择性抑制剂暴露则显著抑制顺行运输,这表明突触谷氨酸受体激活与轴浆运输之间存在联系。最后,在体内摄入乙醇 14 天后,Tg 小鼠嗅神经元的轴浆运输部分受到抑制,而在 Glud1 Tg 小鼠脑片暴露于乙醇 2 小时后,也观察到类似情况。总之,谷氨酸突触的内源性活动调节和谷氨酸突触的过度活跃增加了中枢神经系统神经元内的运输速度。