Begley Marcus A, Mahoney Taylor, Medina Christian Pagán, Zareiesfandabadi Parsa, Rapp Matthew B, Tirfe Mastawal, LeBlanc Sharonda J, Betterton Meredith D, Elting Mary Williard
Physics, North Carolina State University, Raleigh, North Carolina, USA.
Genetics, Rutgers University, Piscataway, NJ, USA.
Cytoskeleton (Hoboken). 2025 May 10. doi: 10.1002/cm.22035.
The fission yeast Schizosaccharomyces pombe divides via closed mitosis, meaning that spindle elongation and chromosome segregation transpire entirely within the closed nuclear envelope. Both the spindle and nuclear envelope must undergo shape changes and exert varying forces on each other during this process. Previous work has demonstrated that nuclear envelope expansion (Yam, He, Zhang, Chiam, & Oliferenko, 2011; Mori & Oliferenko, 2020) and spindle pole body (SPB) embedding in the nuclear envelope are required for normal S. pombe mitosis, and mechanical modeling has described potential contributions of the spindle to nuclear morphology (Fang et al., 2020; Zhu et al., 2016). However, it is not yet fully clear how and to what extent the nuclear envelope and mitotic spindle each directly shape each other during closed mitosis. Here, we investigate this relationship by observing the behaviors of spindles and nuclei in live mitotic fission yeast following laser ablation. First, we characterize these dynamics in mitotic S. pombe nuclei with increased envelope tension, finding that nuclear envelope tension can both bend the spindle and slow elongation. Next, we directly probe the mechanical connection between spindles and nuclear envelopes by ablating each structure. We demonstrate that envelope tension can be relieved by severing spindles and that spindle compression can be relieved by rupturing the envelope. We interpret our experimental data via two quantitative models that demonstrate that fission yeast spindles and nuclear envelopes are a mechanical pair that can each shape the other's morphology.
裂殖酵母粟酒裂殖酵母通过封闭有丝分裂进行分裂,这意味着纺锤体伸长和染色体分离完全在封闭的核膜内发生。在此过程中,纺锤体和核膜都必须经历形状变化并相互施加不同的力。先前的研究表明,核膜扩张(Yam、He、Zhang、Chiam和Oliferenko,2011年;Mori和Oliferenko,2020年)以及纺锤极体(SPB)嵌入核膜是粟酒裂殖酵母正常有丝分裂所必需的,并且力学模型已经描述了纺锤体对核形态的潜在影响(Fang等人,2020年;Zhu等人,2016年)。然而,在封闭有丝分裂过程中,核膜和有丝分裂纺锤体如何以及在多大程度上直接相互塑造对方,目前尚不完全清楚。在这里,我们通过观察激光消融后活的有丝分裂裂殖酵母中纺锤体和细胞核的行为来研究这种关系。首先,我们在核膜张力增加的有丝分裂粟酒裂殖酵母细胞核中表征这些动态,发现核膜张力既能使纺锤体弯曲又能减缓伸长。接下来,我们通过消融每个结构直接探测纺锤体和核膜之间的机械连接。我们证明切断纺锤体可以缓解核膜张力,而破坏核膜可以缓解纺锤体压缩。我们通过两个定量模型解释我们的实验数据,这两个模型表明裂殖酵母纺锤体和核膜是一对机械结构,它们可以相互塑造对方的形态。