Eukaryotic cells typically form a single, round nucleus after mitosis, and failures to do so can compromise genomic integrity. How mammalian cells form such a nucleus remains incompletely understood. NuMA is a spindle protein whose disruption results in nuclear fragmentation. What role NuMA plays in nuclear integrity, and whether its perceived role stems from its spindle function, are unclear. Here, we use live imaging to demonstrate that NuMA plays a spindle-independent role in forming a single, round nucleus. NuMA keeps the decondensing chromosome mass compact at mitotic exit and promotes a mechanically robust nucleus. NuMA’s C terminus binds DNA in vitro and chromosomes in interphase, while its coiled-coil acts as a central regulatory and structural element: it prevents NuMA from binding chromosomes at mitosis, regulates its nuclear mobility, and is essential for nuclear formation. Thus, NuMA plays a structural role over the cell cycle, building and maintaining the spindle and nucleus, two of the cell’s largest structures.
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7 December 2020
Article|
October 12 2020
The mitotic protein NuMA plays a spindle-independent role in nuclear formation and mechanics
Andrea Serra-Marques,
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
2
Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA
Andrea Serra-Marques: andrea.asmarques@gmail.com
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Ronja Houtekamer,
Ronja Houtekamer
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
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Dorine Hintzen,
Dorine Hintzen
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
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John T. Canty,
John T. Canty
3
Biophysics Graduate Group, University of California, Berkeley, Berkeley, CA
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Ahmet Yildiz,
Ahmet Yildiz
3
Biophysics Graduate Group, University of California, Berkeley, Berkeley, CA
4
Department of Molecular and Cellular Biology, University of California, Berkeley, Berkeley, CA
5
Department of Physics, University of California, Berkeley, Berkeley, CA
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Sophie Dumont
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
2
Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA
6Chan Zuckerberg Biohub, San Francisco, CA
Correspondence to Sophie Dumont: sophie.dumont@ucsf.edu
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Andrea Serra-Marques
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
2
Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA
Ronja Houtekamer
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
Dorine Hintzen
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
John T. Canty
3
Biophysics Graduate Group, University of California, Berkeley, Berkeley, CA
Ahmet Yildiz
3
Biophysics Graduate Group, University of California, Berkeley, Berkeley, CA
4
Department of Molecular and Cellular Biology, University of California, Berkeley, Berkeley, CA
5
Department of Physics, University of California, Berkeley, Berkeley, CA
Sophie Dumont
1
Department of Cell and Tissue Biology, University of California, San Francisco, San Francisco, CA
2
Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA
6Chan Zuckerberg Biohub, San Francisco, CA
Andrea Serra-Marques: andrea.asmarques@gmail.com
Correspondence to Sophie Dumont: sophie.dumont@ucsf.edu
Received:
May 04 2020
Revision Received:
August 15 2020
Accepted:
September 11 2020
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding:
Howard Hughes Medical Institute
(NO AWARD)
Human Frontier Science Program
(LT001061/2016-L)
National Institutes of Health
(P30 DK063720, 5R35GM118119)
National Science Foundation
(1548297)
Rita Allen Foundation
(NO AWARD)
Sandler Foundation
(NO AWARD)
© 2020 Serra-Marques et al.
2020
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2020) 219 (12): e202004202.
Article history
Received:
May 04 2020
Revision Received:
August 15 2020
Accepted:
September 11 2020
Citation
Andrea Serra-Marques, Ronja Houtekamer, Dorine Hintzen, John T. Canty, Ahmet Yildiz, Sophie Dumont; The mitotic protein NuMA plays a spindle-independent role in nuclear formation and mechanics. J Cell Biol 7 December 2020; 219 (12): e202004202. doi: https://doi.org/10.1083/jcb.202004202
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