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Dynein pulling forces on ruptured nuclei counteract lamin-mediated nuclear envelope repair mechanisms in vivo

Lauren Penfield, Brian Wysolmerski, Reza Farhadifar, Michael Martinez, Ronald Biggs, Hai-Yin Wu, Michael Mauro, Curtis Broberg, Daniel Needleman, Shirin Bahmanyar
doi: https://doi.org/10.1101/138693
Lauren Penfield
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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Brian Wysolmerski
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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Reza Farhadifar
2School of Engineering and Applied Sciences, Department of Molecular and Cellular Biology, FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138
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Michael Martinez
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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Ronald Biggs
3Ludwig Institute for Cancer Research, Department of Cellular & Molecular Medicine, University of California San Diego, La Jolla, CA 92093
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Hai-Yin Wu
2School of Engineering and Applied Sciences, Department of Molecular and Cellular Biology, FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138
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Michael Mauro
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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Curtis Broberg
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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Daniel Needleman
2School of Engineering and Applied Sciences, Department of Molecular and Cellular Biology, FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138
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Shirin Bahmanyar
1Department of Molecular Cellular and Developmental Biology, Yale University, New Haven, CT 06520
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  • For correspondence: shirin.bahmanyar@yale.edu
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Abstract

Recent work done exclusively in tissue culture cells revealed that the nuclear envelope (NE) undergoes ruptures leading to transient mixing of nuclear and cytoplasmic components. The duration of transient NE ruptures depends on lamins, however the underlying mechanisms and the relevance to in vivo events is not known. Here, we use C. elegans embryos to show that dynein forces that position nuclei increase the severity of lamin-induced NE ruptures in vivo. In the absence of dynein forces, lamin prevents nuclear-cytoplasmic mixing caused by NE ruptures. By monitoring the dynamics of NE rupture events, we demonstrate that lamin is required for a distinct phase in NE recovery that restricts nucleocytoplasmic mixing prior to the full restoration of NE rupture sites. We show that laser-induced puncture of the NE recapitulates phenotypes associated with NE recovery in wild type cells. Surprisingly, we find that embryonic lethality does not correlate with the incidence of NE rupture events suggesting that embryos survive transient losses of NE compartmentalization during early embryogenesis. In addition to presenting the first mechanistic analysis of transient NE ruptures in vivo, this work demonstrates that lamin controls the duration of NE ruptures by opposing dynein forces on ruptured nuclei to allow reestablishment of the NE permeability barrier and subsequent restoration of NE rupture sites.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 30, 2017.
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Dynein pulling forces on ruptured nuclei counteract lamin-mediated nuclear envelope repair mechanisms in vivo
Lauren Penfield, Brian Wysolmerski, Reza Farhadifar, Michael Martinez, Ronald Biggs, Hai-Yin Wu, Michael Mauro, Curtis Broberg, Daniel Needleman, Shirin Bahmanyar
bioRxiv 138693; doi: https://doi.org/10.1101/138693
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Dynein pulling forces on ruptured nuclei counteract lamin-mediated nuclear envelope repair mechanisms in vivo
Lauren Penfield, Brian Wysolmerski, Reza Farhadifar, Michael Martinez, Ronald Biggs, Hai-Yin Wu, Michael Mauro, Curtis Broberg, Daniel Needleman, Shirin Bahmanyar
bioRxiv 138693; doi: https://doi.org/10.1101/138693

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