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Dynein-pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair.
Molecular Biology of the Cell 2018 January 32
Recent work done exclusively in tissue culture cells revealed that the nuclear envelope (NE) ruptures and repairs in interphase. The duration of NE ruptures depends on lamins, however the underlying mechanisms and relevance to in vivo events is not known. Here, we use the C. elegans zygote to analyze lamin's role in NE rupture and repair in vivo Transient NE ruptures and subsequent NE collapse are induced by weaknesses in the nuclear lamina caused by expression of an engineered hypomorphic C. elegans lamin allele. Dynein-generated forces that position nuclei enhance the severity of transient NE ruptures and cause NE collapse. Reduction of dynein forces allows the weakened lamin network, but not lamin-deficient nuclei, to restrict nucleo-cytoplasmic mixing and support stable NE recovery. Surprisingly, the high incidence of transient NE ruptures does not contribute to embryonic lethality, which is instead correlated with stochastic chromosome scattering resulting from premature NE collapse, suggesting that C. elegans tolerate transient losses of NE compartmentalization during early embryogenesis. In sum, we demonstrate that lamin counteracts dynein forces and supports stable NE repair to prevent catastrophic loss of the nuclear permeability barrier, and thus provide the first mechanistic analysis of NE ruptures in an organismal context.
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