Spiess Keeley L, Geden Matthew J, Romero Selena E, Hollville Emilie, Hammond Elizabeth S, Patterson Rachel L, Girardi Quintin B, Deshmukh Mohanish
Neuroscience Center; University of North Carolina, Chapel Hill, NC, USA.
Department of Cell Biology and Physiology, University of North Carolina, Chapel Hill, NC, USA.
Cell Death Differ. 2025 Mar;32(3):521-529. doi: 10.1038/s41418-024-01403-5. Epub 2024 Oct 26.
Apoptosis is a fundamental process of all mammalian cells but exactly how it is regulated in different primary cells remains less explored. In most contexts, apoptosis is engaged to eliminate cells. However, postmitotic cells such as neurons must efficiently balance the need for developmental apoptosis versus the physiological needs for their long-term survival. Neurons are capable of reversing the commitment to death even after the point of cytochrome c release. This ability of neurons to recover from an apoptotic signal suggests that activation of the apoptotic pathway in neurons could be much more transient than is currently recognized. Here, we investigated whether the apoptotic pathway in neurons is a persistent signal or a transient pulse in continuous presence of apoptotic stimulus. We have examined this at three key steps in apoptotic signaling: phosphorylation of c-Jun, induction of the BH3-only family proteins and Bax activation. Strikingly, we found all three of these events occur as transient signals following Nerve Growth Factor (NGF) deprivation-induced apoptosis in sympathetic neurons. This transient apoptosis signal would effectively allow neurons to reset and permit recovery if the apoptotic stimulus is reversed. Excitingly, we have also discovered that a neuron's ability to recover from an apoptotic signal is dependent on expression of the anti-apoptotic Bcl-2 family protein Bcl-xL. Bcl-xL-deficient neurons lose the ability to recover from NGF deprivation even if NGF is restored. Additionally, we show that recovery from a previous exposure to NGF deprivation is protective against subsequent deprivation. Together, these results define a novel mechanism by which apoptosis is regulated in neurons where the transient pulse of the apoptotic signaling supports neuronal resilience.
细胞凋亡是所有哺乳动物细胞的一个基本过程,但在不同原代细胞中其具体调控方式仍有待深入研究。在大多数情况下,细胞凋亡是为了清除细胞。然而,有丝分裂后细胞,如神经元,必须在发育性细胞凋亡的需求与它们长期存活的生理需求之间有效地取得平衡。即使在细胞色素c释放之后,神经元仍能够逆转死亡的进程。神经元从凋亡信号中恢复的这种能力表明,神经元中凋亡途径的激活可能比目前所认识的更加短暂。在这里,我们研究了在持续存在凋亡刺激的情况下,神经元中的凋亡途径是一个持续信号还是一个短暂脉冲。我们在凋亡信号传导的三个关键步骤对此进行了研究:c-Jun的磷酸化、仅含BH3结构域蛋白家族的诱导以及Bax的激活。令人惊讶的是,我们发现,在交感神经元中,神经生长因子(NGF)剥夺诱导的细胞凋亡后,所有这三个事件均作为短暂信号发生。如果凋亡刺激被逆转,这种短暂的凋亡信号将有效地使神经元重置并得以恢复。令人兴奋的是,我们还发现,神经元从凋亡信号中恢复过来的能力取决于抗凋亡Bcl-2家族蛋白Bcl-xL的表达。即使恢复了NGF,Bcl-xL缺陷的神经元也失去了从NGF剥夺中恢复的能力。此外,我们表明,从先前暴露于NGF剥夺中恢复过来具有保护作用,可抵御随后的剥夺。总之,这些结果定义了一种在神经元中调控细胞凋亡的新机制,其中凋亡信号传导的短暂脉冲支持神经元的恢复能力。