Theisen, Ulrike, Straube, Anne and Steinberg, Gero. (2008) Dynamic rearrangement of nucleoporins during fungal "open" mitosis. Molecular Biology of the Cell, Volume 19 (Number 3). pp. 1230-1240. ISSN 1059-1524

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Abstract

Mitosis in animals starts with the disassembly of the nuclear pore complexes and the breakdown of the nuclear envelope. In contrast to many fungi, the corn smut fungus Ustilago maydis also removes the nuclear envelope. Here, we report on the dynamic behavior of the nucleoporins Nup214, Pom152, Nup133, and Nup107 in this "open" fungal mitosis. In prophase, the nuclear pore complexes disassembled and Nup214 and Pom152 dispersed in the cytoplasm and in the endoplasmic reticulum, respectively. Nup107 and Nup133 initially spread throughout the cytoplasm, but in metaphase and early anaphase occurred on the chromosomes. In anaphase, the Nup107-subcomplex redistributed to the edge of the chromosome masses, where the new envelope was reconstituted. Subsequently, Nup214 and Pom152 are recruited to the nuclear pores and protein import starts. Recruitment of nucleoporins and protein import reached a steady state in G2 phase. Formation of the nuclear envelope and assembly of nuclear pores occurred in the absence of microtubules or F-actin, but not if both were disrupted. Thus, the basic principles of nuclear pore complex dynamics seem to be conserved in organisms displaying open mitosis.

Item Type:	Journal Article
Subjects:	Q Science > QH Natural history > QH301 Biology Q Science > QH Natural history > QH426 Genetics Q Science > QK Botany
Divisions:	Faculty of Medicine > Warwick Medical School > Biomedical Cell Biology Faculty of Science > Life Sciences (2010- ) Faculty of Medicine > Warwick Medical School
Library of Congress Subject Headings (LCSH):	Cell cycle, Mitosis, Cell division, Fungi -- Cytology, Microbial genetics, Cytogenetics, Eukaryotic cells -- Genetics
Journal or Publication Title:	Molecular Biology of the Cell
Publisher:	American Society for Cell Biology
ISSN:	1059-1524
Date:	March 2008
Volume:	Volume 19
Number:	Number 3
Page Range:	pp. 1230-1240
Identification Number:	10.1091/mbc.E07-02-0130
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Studienstiftung des Deutschen Volkes
References:	Amor, D. J., Kalitsis, P., Sumer, H., and Choo, K. H. (2004). Building the centromere: from foundation proteins to 3D organization. Trends Cell Biol. 14, 359–368. Bai, S. W., Rouquette, J., Umeda, M., Faigle, W., Loew, D., Sazer, S., and Doye, V. (2004). The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Mol. Cell. Biol. 24, 6379–6392. Beaudouin, J., Gerlich, D., Daigle, N., Eils, R., and Ellenberg, J. (2002). Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108, 83–96. Belgareh, N. et al. (2001). An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154, 1147–1160. Berke, I. C., Boehmer, T., Blobel, G., and Schwartz, T. U. (2004). Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J. Cell Biol. 167, 591–597. Boehmer, T., Enninga, J., Dales, S., Blobel, G., and Zhong, H. (2003). Depletion of a single nucleoporin, Nup107, prevents the assembly of a subset of nucleoporins into the nuclear pore complex. Proc. Natl. Acad. Sci. USA 100, 981–985. Bottin, A., Kamper, J., and Kahmann, R. (1996). Isolation of a carbon sourceregulated gene from Ustilago maydis. Mol. Gen. Genet. 253, 342–352. Castillo-Lluva, S., Alvarez-Tabare´s, I., Weber, I., Steinberg, G., and Pe´rez-Martı´n., J. (2007). Sustained cell polarity and virulence in the phytopathogenic fungus Ustilago maydis depends on an essential cyclin-dependent kinase from the Cdk5/Pho85 family. J. Cell Sci. 120, 1584–1595. Cronshaw, J. M., Krutchinsky, A. N., Zhang, W., Chait, B. T., and Matunis, M. J. (2002). Proteomic analysis of the mammalian nuclear pore complex J. Cell Biol. 158, 915–927. De Souza, C. P., Osmani, A. H., Hashmi, S. B., and Osmani, S. A. (2004). Partial nuclear pore complex disassembly during closed mitosis in Aspergillus nidulans. Curr. Biol. 14, 1973–1984. Devos, D., Dokudovskaya, S., Williams, R., Alber, F., Eswar, N., Chait, B. T., Rout, M. P., and Sali, A. (2006). Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl. Acad. Sci. USA 103, 2172– 2177. Ellenberg, J., Siggia, E. D., Moreira, J. E., Smith, C. L., Presley, J. F., Worman, H. J., and Lippincott-Schwartz, J. (1997). Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138, 1193–1206. Fink, G., Schuchardt, I., Colombelli, J., Stelzer, E., and Steinberg, G. (2006). Dynein-mediated pulling forces drive rapid mitotic spindle elongation in Ustilago maydis. EMBO J. 25, 4897–4908. Fink, G., and Steinberg, G. (2006). Dynein-dependent motility of microtubules and nucleation sites supports polarization of the tubulin array in the fungus Ustilago maydis. Mol. Biol. Cell 17, 3242–3253. Fitzpatrick, D. A., Logue, M. E., Stajich, J. E., and Butler, G. (2006). A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6, 99. Fuchs, U., Hause, G., Schuchardt, I., Steinberg, G. (2006). Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 18, 2066–2081. Fuchs, U., Manns, I., and Steinberg, G. (2005). Microtubules are dispensable for the initial pathogenic development but required for long-distance hyphal growth in the corn smut fungus Ustilago maydis. Mol. Biol. Cell 16, 2746–2758. Goshima, G., Saitoh, S., and Yanagida, M. (1999). Proper metaphase spindle length is determined by centromere proteins Mis12 and Mis6 required for faithful chromosome segregation. Genes Dev. 13, 1664–1677. Harel, A., Orjalo, A. V., Vincent, T., Lachish-Zalait, A., Vasu, S., Shah, S., Zimmerman, E., Elbaum, M., and Forbes, D. J. (2003). Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 11, 853–864. Heath, I. B. (1980). Variant mitosis in lower eukaryotes: indicators of the evolution of mitosis? Int. Rev. Cytol. 64, 1–80. Heath, I. B., Bonham, M., Akram, A., and Gupta, G. D. (2003). The interrelationships of actin and hyphal tip growth in the ascomycete Geotrichum candidum. Fungal Genet. Biol. 38, 85–97. Hetzer, M., Walther, T. C., and Mattaj, I. W. (2005). Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 21, 347–380. Holliday, R. (1974). Molecular aspects of genetic exchange and gene conversion. Genetics 78, 273–287. Loiodice, I., Alves, A., Rabut, G., Van Overbeek, M., Ellenberg, J., Sibarita, J. B., and Doye, V. (2004). The entire Nup107–160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol. Biol. Cell 15, 3333–3344. Lutzmann, M., Kunze, R., Buerer, A., Aebi, U., and Hurt, E. (2002). Modular self-assembly of a Y-shaped multiprotein complex from seven nucleoporins. EMBO J. 21, 387–397. Makhnevych, T., Lusk, C. P., Anderson, A. M., Aitchison, J. D., and Wozniak, R. W. (2003). Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 115, 813–823. Mans, B. J., Anantharaman, V., Aravind, L., and Koonin, E. V. (2004). Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 3, 1612–1637. Margalit, A., Vlcek, S., Gruenbaum, Y., and Foisner, R. (2005). Breaking and making of the nuclear envelope. J. Cell. Biochem. 95, 454–465. O’Donell, K. L., and McLaughlin, D. J. (1984a). Postmeiotic mitosis, basidiospore development, and septation in Ustilago maydis. Mycologia 76, 486–502. O’Donell, K. L., and McLaughlin, D. J. (1984b). Ultrastructure of meiosis in Ustilago maydis. Mycologia 76, 468–485. Orjalo, A. V., Arnaoutov, A., Shen, Z., Boyarchuk, Y., Zeitlin, S. G., Fontoura, B., Briggs, S., Dasso, M., and Forbes, D. J. (2006). The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol. Biol. Cell 17, 3806–3818. Osmani, A. H., Davies, J., Liu, H. L., and Osmani, S. A. (2006). Systematic deletion and mitotic localization of the nuclear pore complex proteins of Aspergillus nidulans. Mol. Biol. Cell. Pemberton, L. F., Rout, M. P., and Blobel, G. (1995). Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc. Natl. Acad. Sci. USA 92, 1187–1191. Rabut, G., Lenart, P., and Ellenberg, J. (2004). Dynamics of nuclear pore complex organization through the cell cycle. Curr. Opin. Cell Biol. 16, 314– 321. Rout, M. P., Aitchison, J. D., Suprapto, A., Hjertaas, K., Zhao, Y., and Chait, B. T. (2000). The yeast nuclear pore complex: composition, architecture, and transport mechanism. J. Cell Biol. 148, 635–651. Salina, D., Bodoor, K., Eckley, D. M., Schroer, T. A., Rattner, J. B., and Burke, B. (2002). Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97–107. Sazer, S. (2005). Nuclear envelope: nuclear pore complexity. Curr. Biol. 15, R23–R26. Siniossoglou, S., Lutzmann, M., Santos-Rosa, H., Leonard, K., Mueller, S., Aebi, U., and Hurt, E. (2000). Structure and assembly of the Nup84p complex. J. Cell Biol. 149, 41–54. Siniossoglou, S., Wimmer, C., Rieger, M., Doye, V., Tekotte, H., Weise, C., Emig, S., Segref, A., and Hurt, E. C. (1996). A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84, 265–275. Snetselaar, K. M., and McCann, M. P. (1997). Using microdensitometry to correlate cell morphology with the nuclear cycle in Ustilago maydis. Mycologia 89, 689–697. Steinberg, G., Wedlich-So¨ldner, R., Brill, M., and Schulz, I. (2001). Microtubules in the fungal pathogen Ustilago maydis are highly dynamic and determine cell polarity. J. Cell Sci. 114, 609–622. Straube, A., Brill, M., Oakley, B. R., Horio, T., and Steinberg, G. (2003). Microtubule organization requires cell cycle-dependent nucleation at dispersed cytoplasmic sites: polar and perinuclear microtubule organizing centers in the plant pathogen Ustilago maydis. Mol. Biol. Cell 14, 642–657. Straube, A., Enard, W., Berner, A., Wedlich-So¨ldner, R., Kahmann, R., and Steinberg, G. (2001). A split motor domain in a cytoplasmic dynein. EMBO J. 20, 5091–5100. Straube, A., Weber, I., and Steinberg, G. (2005). A novel mechanism of nuclear envelope break-down in a fungus: nuclear migration strips off the envelope. EMBO J. 24, 1674–1685. Terasaki, M., Campagnola, P., Rolls, M. M., Stein, P. A., Ellenberg, J., Hinkle, B., and Slepchenko, B. (2001). A new model for nuclear envelope breakdown. Mol. Biol. Cell 12, 503–510. Vasu, S., Shah, S., Orjalo, A., Park, M., Fischer, W. H., and Forbes, D. J. (2001). Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155, 339–354. Walther, T. C. et al. (2003). The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113, 195–206. Wedlich-So¨ldner, R., Schulz, I., Straube, A., and Steinberg, G. (2002). Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis. Mol. Biol. Cell 13, 965–977. Yang, L., Guan, T., and Gerace, L. (1997). Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis. J. Cell Biol. 137, 1199–1210. Zuccolo, M. et al. (2007). The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J. 26, 1853–1864.
URI:	http://wrap.warwick.ac.uk/id/eprint/36916

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