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Review

Not just binary: embracing the complexity of nuclear division dynamics

ORCID Icon, ORCID Icon & ORCID Icon
Article: 2360601 | Received 09 Feb 2024, Accepted 22 May 2024, Published online: 06 Jun 2024

References

  • Lin DH, Hoelz A. The structure of the nuclear pore complex (an update). Annu Revi Biochem. 2019;88(June):725–12. doi: 10.1146/annurev-biochem-062917-011901
  • Frey S, Görlich D. Asaturated FG-Repeat hydrogel can reproduce the permeability properties of nuclear pore complexes. Cell. 2007;130(3):512–523. doi: 10.1016/j.cell.2007.06.024
  • Popken P, Ghavami A, Onck PR, et al. Size-dependent leak of soluble and membrane proteins through the yeast nuclear pore complex. Mol Biol Cell. 2015;26(7):1386–1394. doi: 10.1091/mbc.E14-07-1175
  • Timney BL, Raveh B, Mironska R, et al. Simple rules for passive diffusion through the nuclear pore complex. J Cell Bio. 2016;215(1):57–76. doi: 10.1083/jcb.201601004
  • Wing CE, Yee Joyce Fung H, Min Chook Y. Karyopherin-mediated nucleocytoplasmic transport. Nat Rev Mol Cell Biol. 2022;23(5):307–328. doi: 10.1038/s41580-021-00446-7
  • Liu J, Hetzer MW. Nuclear pore complex maintenance and implications for age-related diseases. Trends Cell Biol. 2022;32(3):216–227. doi: 10.1016/j.tcb.2021.10.001
  • Martins F, Sousa J, Pereira CD, et al. Nuclear envelope dysfunction and its contribution to the aging process. Aging Cell. 2020;19(5):e13143. doi: 10.1111/acel.13143
  • Dey G, Baum B. Nuclear envelope remodelling during mitosis. Curr Opinion Cell Biol. 2021;70(June):67–74. doi: 10.1016/j.ceb.2020.12.004
  • Neumann FR, Nurse P. Nuclear size control in fission yeast. J Cell Bio. 2007;179(4):593–600. doi: 10.1083/jcb.200708054
  • Ungricht R, Kutay U. Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol. 2017;18(4):229–245. doi: 10.1038/nrm.2016.153
  • Sazer S, Lynch M, Needleman D. Deciphering the evolutionary history of open and closed mitosis. Curr Biol. 2014;24(22):R1099–1103. doi: 10.1016/j.cub.2014.10.011
  • Boettcher B, Barral Y. The cell biology of open and closed mitosis. Nucleus. 2013;4(3):160–165. doi: 10.4161/nucl.24676
  • De Souza Colin PC, Osmani SA. Mitosis, not just open or closed. Eukaryot Cell. 2007;6(9):1521–1527. doi: 10.1128/EC.00178-07
  • Hauke D, McAinsh AD. Exotic Mitotic Mechanisms. Open Biol. 2012;2(12):120140. doi: 10.1098/rsob.120140
  • Heath IB. Variant mitoses in lower eukaryotes: Indicators of the evolution of mitosis. Int Rev Cytol. 1980;64:1–80. doi: 10.1016/s0074-7696(08)60235-1
  • Makarova M, Oliferenko S. Mixing and matching nuclear envelope remodeling and spindle assembly strategies in the evolution of mitosis. Curr Opinion Cell Biol. 2016;41(August):43–50. doi: 10.1016/j.ceb.2016.03.016
  • King GA, Goodman JS, Schick JG, et al. Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast.” edited by Noboru mizushima, Vivek Malhotra, Noboru mizushima, tokuko haraguchi, and c Patrick lusk. Elife. 2019a;8(August):e47156. doi: 10.7554/eLife.47156
  • Duan T, Cupp R, Geyer PK. Drosophila female germline stem cells undergo mitosis without nuclear breakdown. Curr Biol. 2021;31(7):1450–1462.e3. doi: 10.1016/j.cub.2021.01.033
  • Roubinet C, White IJ, Baum B. Asymmetric nuclear division in neural stem cells generates sibling nuclei that differ in size, envelope composition, and chromatin organization. Curr Biol. 2021;31(18):3973–3983.e4. doi: 10.1016/j.cub.2021.06.063
  • Stafstrom JP, Staehelin LA. Dynamics of the nuclear envelope and of nuclear pore complexes during mitosis in the drosophila embryo. Eur J Cell Biol. 1984;34(1):179–189.
  • Ferrandiz N, Downie L, Starling GP, et al. Endomembranes promote chromosome missegregation by ensheathing misaligned chromosomes. J Cell Bio. 2022;221(6):e202203021. doi: 10.1083/jcb.202203021
  • Lang C, Grava S, van den Hoorn T, et al. Mobility, microtubule nucleation and structure of microtubule-organizing centers in multinucleated hyphae of ashbya gossypii. Mol Biol Cell. 2010;21(1):18–28. doi: 10.1091/mbc.e09-01-0063
  • Fujita I, Nishihara Y, Tanaka M, et al. Telomere-nuclear envelope dissociation promoted by rap1 phosphorylation ensures faithful chromosome segregation. Curr Biol. 2012;22(20):1932–1937. doi: 10.1016/j.cub.2012.08.019
  • Pieper GH, Sprenger S, Teis D, et al. ESCRT-III/Vps4 controls heterochromatin-nuclear envelope attachments. Dev Cell. 2020;53(1):27–41.e6. doi: 10.1016/j.devcel.2020.01.028
  • Ptak C, Saik NO, Premashankar A, et al. Phosphorylation-dependent mitotic SUMOylation drives nuclear envelope–chromatin Interactions. J Cell Bio. 2021;220(12):e202103036. doi: 10.1083/jcb.202103036
  • Yam C, Gu Y, Oliferenko S. Partitioning and remodeling of the Schizosaccharomyces Japonicus mitotic nucleus require chromosome tethers. Curr Biol. 2013;23(22):2303–2310. doi: 10.1016/j.cub.2013.09.057
  • Castagnetti S, Oliferenko S, Nurse P. Fission yeast cells undergo nuclear division in the absence of spindle microtubules. PLOS Biol. 2010;8(10):e1000512. doi: 10.1371/journal.pbio.1000512
  • Yam C, He Y, Zhang D, et al. Divergent strategies for controlling the nuclear membrane satisfy geometric constraints during nuclear division. Curr Biol. 2011;21(15):1314–1319. doi: 10.1016/j.cub.2011.06.052
  • Zhang D, Oliferenko S. Remodeling the nuclear membrane during closed mitosis. Curr Opinion Cell Biol. 2013;25(1):142–148. doi: 10.1016/j.ceb.2012.09.001
  • Makarova M, Gu Y, Chen J-S, et al. Temporal regulation of lipin activity diverged to account for differences in mitotic programs. Curr Biol. 2016;26(2):237–243. doi: 10.1016/j.cub.2015.11.061
  • Shah H, Olivetta M, Bhickta C, et al. Life cycle-coupled evolution of mitosis in close relatives of animals. 2023. bioRxiv. doi: 10.1101/2023.05.10.540163.
  • Sagolla MS, Dawson SC, Mancuso JJ, et al. Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasite giardia intestinalis. J Cell Sci. 2006;119(23):4889–4900. doi: 10.1242/jcs.03276
  • Straube A, Weber I, Steinberg G. A novel mechanism of nuclear envelope break-down in a fungus: Nuclear migration strips off the envelope. Embo J. 2005;24(9):1674–1685. doi: 10.1038/sj.emboj.7600644
  • Cuylen S, Blaukopf C, Politi AZ, et al. Ki-67 acts as a biological surfactant to disperse mitotic chromosomes. Nature. 2016;535(7611):308–312. doi: 10.1038/nature18610
  • Cuylen-Haering S, Petrovic M, Hernandez-Armendariz A, et al. Chromosome clustering by ki-67 excludes cytoplasm during nuclear assembly. Nature. 2020;587(7833):285–290. doi: 10.1038/s41586-020-2672-3
  • Margalit A, Segura-Totten M, Gruenbaum Y, et al. Barrier-to-autointegration factor is required to segregate and enclose chromosomes within the nuclear envelope and assemble the nuclear lamina. Proc Nat Acad Sci. 2005;102(9):3290–3295. doi: 10.1073/pnas.0408364102
  • Samwer M, Schneider MWG, Hoefler R, et al. DNA cross-bridging shapes a single nucleus from a set of mitotic chromosomes. Cell. 2017;170(5):956–972.e23. doi: 10.1016/j.cell.2017.07.038
  • Olmos Y, Hodgson L, Mantell J, et al. ESCRT-III controls nuclear envelope reformation. Nature. 2015;522(7555):236–239. doi: 10.1038/nature14503
  • Vietri M, Schink KO, Campsteijn C, et al. Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature. 2015;522(7555):231–235. doi: 10.1038/nature14408
  • Leadbeater BSC. The Choanoflagellates: evolution, Biology and Ecology. Cambridge: Cambridge University Press; 2015. doi: 10.1017/CBO9781139051125
  • Lee KK, Gruenbaum Y, Spann P, et al. C. Elegans nuclear envelope proteins emerin, man1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol Biol Cell. 2000;11(9):3089–3099. doi: 10.1091/mbc.11.9.3089
  • Ding R, McDonald KL, McIntosh JR. Three-dimensional reconstruction and analysis of mitotic spindles from the yeast, schizosaccharomyces pombe. J Cell Bio. 1993;120(1):141–151. doi: 10.1083/jcb.120.1.141
  • West RR, Vaisberg EV, Ding R, et al. cut11 +: A gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in schizosaccharomyces pombe. Mol Biol Cell. 1998;9(10):2839–2855. doi: 10.1091/mbc.9.10.2839
  • Fernández-Álvarez A, Bez C, O’Toole ET, et al. Mitotic nuclear envelope breakdown and spindle nucleation are controlled by interphase contacts between centromeres and the nuclear envelope. Dev Cell. 2016;39(5):544–559. doi: 10.1016/j.devcel.2016.10.021
  • Ader NR, Chen L, Surovtsev IV, et al. An ESCRT grommet cooperates with a diffusion barrier to maintain nuclear integrity. Nat Cell Biol. 2023;25(10):1465–1477. doi: 10.1038/s41556-023-01235-4
  • Dey G, Culley S, Curran S, et al. Closed mitosis requires local disassembly of the nuclear envelope. Nature. 2020;585(7823):119–123. doi: 10.1038/s41586-020-2648-3
  • De Souza Colin PC, Osmani AH, Hashmi SB, et al. Partial nuclear pore complex disassembly during closed mitosis in aspergillus nidulans. Current Biology: CB. 2004;14(22):1973–1984. doi: 10.1016/j.cub.2004.10.050
  • Suresh S, Markossian S, Osmani AH, et al. Mitotic nuclear pore complex segregation involves nup2 in aspergillus nidulans. J Cell Bio. 2017;216(9):2813–2826. doi: 10.1083/jcb.201610019
  • Mitic K, Meyer I, Gräf R, et al. Temporal changes in nuclear envelope permeability during semi-closed mitosis in dictyostelium amoebae. Cells. 2023;12(10):1380. doi: 10.3390/cells12101380
  • Theisen U, Straube A, Steinberg G, et al. Dynamic rearrangement of nucleoporins during fungal “open” mitosis. Mol Biol Cell. 2008;19(3):1230–1240. doi: 10.1091/mbc.E07-02-0130
  • Lénárt P, Rabut G, Daigle N, et al. Nuclear envelope breakdown in starfish oocytes proceeds by partial NPC disassembly followed by a rapidly spreading fenestration of nuclear membranes. J Cell Bio. 2003;160(7):1055–1068. doi: 10.1083/jcb.200211076
  • Winey M, Yarar D, Giddings TH, et al. Nuclear pore complex number and distribution throughout the saccharomyces cerevisiae cell cycle by three-dimensional reconstruction from electron micrographs of nuclear envelopes. Mol Biol Cell. 1997;8(11):2119–2132. doi: 10.1091/mbc.8.11.2119
  • Shelton SN, Smith SE, Unruh JR, et al. A distinct inner nuclear membrane proteome in saccharomyces cerevisiae gametes. G3: Genes | Genomes | Genetics. 2021;11(12):jkab345. doi: 10.1093/g3journal/jkab345
  • Solnica-Krezel L, Burland TG, Dove WF. Variable pathways for developmental changes of mitosis and cytokinesis in physarum polycephalum. J Cell Bio. 1991;113(3):591–604. doi: 10.1083/jcb.113.3.591
  • Arai K, Sato M, Tanaka K, et al. Nuclear compartmentalization is abolished during fission yeast meiosis. Curr Biol. 2010;20(21):1913–1918. doi: 10.1016/j.cub.2010.09.004
  • Asakawa H, Kojidani T, Mori C, et al. Virtual breakdown of the nuclear envelope in fission yeast meiosis. Curr Biol. 2010;20(21):1919–1925. doi: 10.1016/j.cub.2010.09.070
  • King GA, Wettstein R, Varberg JM, et al. Meiotic nuclear pore complex remodeling provides key insights into nuclear basket organization. J Cell Bio. 2022;222(2):e202204039. doi: 10.1083/jcb.202204039
  • Sipiczki M. Where does fission yeast sit on the tree of life? Genome Bio. 2000;1(2):reviews1011.1–reviews1011.4. doi: 10.1186/gb-2000-1-2-reviews1011
  • Flor-Parra I, Belén Iglesias-Romero A, Salas-Pino S, et al. Importin α and vNEBD control meiotic spindle disassembly in fission yeast. Cell Rep. 2018;23(4):933–941. doi: 10.1016/j.celrep.2018.03.073
  • Ünal E, Kinde B, Amon A. Gametogenesis eliminates age-induced cellular damage and resets lifespan in yeast. Science. 2011;332(6037):1554–1557. doi: 10.1126/science.1204349
  • Chu DB, Gromova T, Newman TAC, et al. The nucleoporin nup2 contains a meiotic-autonomous region that promotes the dynamic chromosome events of meiosis. Genetics. 2017;206(3):1319–1337. doi: 10.1534/genetics.116.194555
  • Komachi K, Burgess SM. The Nup2 meiotic-autonomous region relieves inhibition of nup60 to promote progression of meiosis and sporulation in Saccharomyces Cerevisiae. Genetics. 2022;221(1):iyac045. doi: 10.1093/genetics/iyac045
  • Iwamoto M, Mori C, Kojidani T, et al. Two distinct repeat sequences of nup98 nucleoporins characterize dual nuclei in the binucleated ciliate tetrahymena. Curr Biol. 2009;19(10):843–847. doi: 10.1016/j.cub.2009.03.055
  • Iwamoto M, Osakada H, Mori C, et al. Compositionally distinct nuclear pore complexes of functionally distinct dimorphic nuclei in the ciliate tetrahymena. J Cell Sci. 2017;130(10):1822–1834. doi: 10.1242/jcs.199398
  • Patterson DJ. The diversity of eukaryotes. Am Natur. 1999;154(S4):S96–124. doi: 10.1086/303287
  • Knott GJ, Doudna JA. CRISPR-Cas guides the future of genetic engineering. Science. 2018;361(6405):866–869. doi: 10.1126/science.aat5011
  • O’Donnell KL, McLaughlin DJ. Ultrastructure of meiosis in Ustilago maydis. Mycologia. 1984;76(3):468–485. doi: 10.1080/00275514.1984.12023868
  • Speijer D, Lukeš J, Eliáš M. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci USA. 2015;112(29):8827–8834. doi: 10.1073/pnas.1501725112