Unknown

Dataset Information

0

Dynein pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair.


ABSTRACT: 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 are not known. Here, we use the Caenorhabditis 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 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 tolerates transient losses of NE compartmentalization during early embryogenesis. In sum, we demonstrate that lamin counteracts dynein forces to promote stable NE repair and prevent catastrophic NE collapse, and thus provide the first mechanistic analysis of NE rupture and repair in an organismal context.

SUBMITTER: Penfield L 

PROVIDER: S-EPMC5905298 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

altmetric image

Publications

Dynein pulling forces counteract lamin-mediated nuclear stability during nuclear envelope repair.

Penfield Lauren L   Wysolmerski Brian B   Mauro Michael M   Farhadifar Reza R   Martinez Michael A MA   Biggs Ronald R   Wu Hai-Yin HY   Broberg Curtis C   Needleman Daniel D   Bahmanyar Shirin S  

Molecular biology of the cell 20180401 7


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 are not known. Here, we use the <i>Caenorhabditis elegans</i> 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 engine  ...[more]

Similar Datasets

| S-EPMC1618106 | biostudies-literature
| S-EPMC8657813 | biostudies-literature
| S-EPMC3292199 | biostudies-literature
| S-EPMC6037482 | biostudies-literature
| S-EPMC7403722 | biostudies-literature
| S-EPMC3035127 | biostudies-literature
| S-SCDT-EMBOR-2019-48779-T | biostudies-other
| S-EPMC5829501 | biostudies-literature
| S-EPMC14977 | biostudies-literature
| S-EPMC9670326 | biostudies-literature