Closed mitosis requires local disassembly of the nuclear envelope

Gautam Dey; Siân Culley; Scott Curran; Uwe Schmidt; Ricardo Henriques; Wanda Kukulski; Buzz Baum

doi:10.1038/s41586-020-2648-3

Closed mitosis requires local disassembly of the nuclear envelope

Gautam Dey^*, Siân Culley, Scott Curran, Uwe Schmidt, Ricardo Henriques, Wanda Kukulski, Buzz Baum

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

41 Citations (Scopus)

Abstract

At the end of mitosis, eukaryotic cells must segregate the two copies of their replicated genome into two new nuclear compartments¹. They do this either by first dismantling and later reassembling the nuclear envelope in an ‘open mitosis’ or by reshaping an intact nucleus and then dividing it into two in a ‘closed mitosis’^2,3. Mitosis has been studied in a wide variety of eukaryotes for more than a century⁴, but how the double membrane of the nuclear envelope is split into two at the end of a closed mitosis without compromising the impermeability of the nuclear compartment remains unknown⁵. Here, using the fission yeast Schizosaccharomyces pombe (a classical model for closed mitosis⁵), genetics, live-cell imaging and electron tomography, we show that nuclear fission is achieved via local disassembly of nuclear pores within the narrow bridge that links segregating daughter nuclei. In doing so, we identify the protein Les1, which is localized to the inner nuclear envelope and restricts the process of local nuclear envelope breakdown to the bridge midzone to prevent the leakage of material from daughter nuclei. The mechanism of local nuclear envelope breakdown in a closed mitosis therefore closely mirrors nuclear envelope breakdown in open mitosis³, revealing an unexpectedly high conservation of nuclear remodelling mechanisms across diverse eukaryotes.

Original language	English
Pages (from-to)	119-123
Number of pages	5
Journal	Nature
Volume	585
Issue number	7823
DOIs	https://doi.org/10.1038/s41586-020-2648-3
Publication status	Published - 3 Sept 2020

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title = "Closed mitosis requires local disassembly of the nuclear envelope",

abstract = "At the end of mitosis, eukaryotic cells must segregate the two copies of their replicated genome into two new nuclear compartments1. They do this either by first dismantling and later reassembling the nuclear envelope in an {\textquoteleft}open mitosis{\textquoteright} or by reshaping an intact nucleus and then dividing it into two in a {\textquoteleft}closed mitosis{\textquoteright}2,3. Mitosis has been studied in a wide variety of eukaryotes for more than a century4, but how the double membrane of the nuclear envelope is split into two at the end of a closed mitosis without compromising the impermeability of the nuclear compartment remains unknown5. Here, using the fission yeast Schizosaccharomyces pombe (a classical model for closed mitosis5), genetics, live-cell imaging and electron tomography, we show that nuclear fission is achieved via local disassembly of nuclear pores within the narrow bridge that links segregating daughter nuclei. In doing so, we identify the protein Les1, which is localized to the inner nuclear envelope and restricts the process of local nuclear envelope breakdown to the bridge midzone to prevent the leakage of material from daughter nuclei. The mechanism of local nuclear envelope breakdown in a closed mitosis therefore closely mirrors nuclear envelope breakdown in open mitosis3, revealing an unexpectedly high conservation of nuclear remodelling mechanisms across diverse eukaryotes.",

author = "Gautam Dey and Si{\^a}n Culley and Scott Curran and Uwe Schmidt and Ricardo Henriques and Wanda Kukulski and Buzz Baum",

note = "Funding Information: Acknowledgements We thank M. Balasubramanian, S. Oliferenko, S. Hauf, K. Gould, J. Bahler, P. Nurse and their laboratories for sharing S. pombe strains, plasmids, expertise and S. pombe protocols; J. O. Patterson for the gift of pFA6a-mNeonGreen plasmids; the LMB electron microscopy facility for electron microscopy support; T.-O. Buchholz for advice on the Noise2Noise implementation.; and D. Albrecht, I. Raote, A. Chaigne, P. Pereira, C. Jacobs and members of the Baum laboratory, in particular G. Paci, G. Cazzagon and H. Matthews, for their feedback on this manuscript. G.D. was funded by a European Union Marie Sklodowska-Curie Individual Fellowship (704281-CCDSA) and the Wellcome Trust (203276/Z/16/Z). S. Culley and R.H. were supported by the UK Biotechnology and Biological Sciences Research Council (BB/R021805/1; BB/S507532/1), the UK Medical Research Council (MR/K015826/1) and the Wellcome Trust (203276/Z/16/Z). S. Curran was supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001121), the UK Medical Research Council (FC001121) and the Wellcome Trust (FC001121). W.K. was funded by the Medical Research Council (MC_UP_1201/8). B.B. was supported by UCL{\textquoteright}s Institute for the Physics of Living Systems, the MRC-LMCB, the Wellcome Trust (203276/Z/16/Z) and Cancer Research UK (C1529/A28276). Publisher Copyright: {\textcopyright} 2020, The Author(s), under exclusive licence to Springer Nature Limited.",

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doi = "10.1038/s41586-020-2648-3",

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T1 - Closed mitosis requires local disassembly of the nuclear envelope

AU - Dey, Gautam

AU - Culley, Siân

AU - Curran, Scott

AU - Schmidt, Uwe

AU - Henriques, Ricardo

AU - Kukulski, Wanda

AU - Baum, Buzz

N1 - Funding Information: Acknowledgements We thank M. Balasubramanian, S. Oliferenko, S. Hauf, K. Gould, J. Bahler, P. Nurse and their laboratories for sharing S. pombe strains, plasmids, expertise and S. pombe protocols; J. O. Patterson for the gift of pFA6a-mNeonGreen plasmids; the LMB electron microscopy facility for electron microscopy support; T.-O. Buchholz for advice on the Noise2Noise implementation.; and D. Albrecht, I. Raote, A. Chaigne, P. Pereira, C. Jacobs and members of the Baum laboratory, in particular G. Paci, G. Cazzagon and H. Matthews, for their feedback on this manuscript. G.D. was funded by a European Union Marie Sklodowska-Curie Individual Fellowship (704281-CCDSA) and the Wellcome Trust (203276/Z/16/Z). S. Culley and R.H. were supported by the UK Biotechnology and Biological Sciences Research Council (BB/R021805/1; BB/S507532/1), the UK Medical Research Council (MR/K015826/1) and the Wellcome Trust (203276/Z/16/Z). S. Curran was supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001121), the UK Medical Research Council (FC001121) and the Wellcome Trust (FC001121). W.K. was funded by the Medical Research Council (MC_UP_1201/8). B.B. was supported by UCL’s Institute for the Physics of Living Systems, the MRC-LMCB, the Wellcome Trust (203276/Z/16/Z) and Cancer Research UK (C1529/A28276). Publisher Copyright: © 2020, The Author(s), under exclusive licence to Springer Nature Limited.

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N2 - At the end of mitosis, eukaryotic cells must segregate the two copies of their replicated genome into two new nuclear compartments1. They do this either by first dismantling and later reassembling the nuclear envelope in an ‘open mitosis’ or by reshaping an intact nucleus and then dividing it into two in a ‘closed mitosis’2,3. Mitosis has been studied in a wide variety of eukaryotes for more than a century4, but how the double membrane of the nuclear envelope is split into two at the end of a closed mitosis without compromising the impermeability of the nuclear compartment remains unknown5. Here, using the fission yeast Schizosaccharomyces pombe (a classical model for closed mitosis5), genetics, live-cell imaging and electron tomography, we show that nuclear fission is achieved via local disassembly of nuclear pores within the narrow bridge that links segregating daughter nuclei. In doing so, we identify the protein Les1, which is localized to the inner nuclear envelope and restricts the process of local nuclear envelope breakdown to the bridge midzone to prevent the leakage of material from daughter nuclei. The mechanism of local nuclear envelope breakdown in a closed mitosis therefore closely mirrors nuclear envelope breakdown in open mitosis3, revealing an unexpectedly high conservation of nuclear remodelling mechanisms across diverse eukaryotes.

AB - At the end of mitosis, eukaryotic cells must segregate the two copies of their replicated genome into two new nuclear compartments1. They do this either by first dismantling and later reassembling the nuclear envelope in an ‘open mitosis’ or by reshaping an intact nucleus and then dividing it into two in a ‘closed mitosis’2,3. Mitosis has been studied in a wide variety of eukaryotes for more than a century4, but how the double membrane of the nuclear envelope is split into two at the end of a closed mitosis without compromising the impermeability of the nuclear compartment remains unknown5. Here, using the fission yeast Schizosaccharomyces pombe (a classical model for closed mitosis5), genetics, live-cell imaging and electron tomography, we show that nuclear fission is achieved via local disassembly of nuclear pores within the narrow bridge that links segregating daughter nuclei. In doing so, we identify the protein Les1, which is localized to the inner nuclear envelope and restricts the process of local nuclear envelope breakdown to the bridge midzone to prevent the leakage of material from daughter nuclei. The mechanism of local nuclear envelope breakdown in a closed mitosis therefore closely mirrors nuclear envelope breakdown in open mitosis3, revealing an unexpectedly high conservation of nuclear remodelling mechanisms across diverse eukaryotes.

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Closed mitosis requires local disassembly of the nuclear envelope

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