Tubulin is actively exported from the nucleus through the Exportin1/CRM1 pathway
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30952896
PubMed Central
PMC6451007
DOI
10.1038/s41598-019-42056-6
PII: 10.1038/s41598-019-42056-6
Knihovny.cz E-zdroje
- MeSH
- aktivní transport - buněčné jádro fyziologie MeSH
- buněčné jádro metabolismus MeSH
- buněčné linie MeSH
- cytoplazma metabolismus MeSH
- eukaryotické buňky metabolismus MeSH
- karyoferiny metabolismus MeSH
- lidé MeSH
- mikrotubuly metabolismus MeSH
- protein exportin 1 MeSH
- receptory cytoplazmatické a nukleární metabolismus MeSH
- tabák metabolismus MeSH
- transport proteinů fyziologie MeSH
- tubulin metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- karyoferiny MeSH
- receptory cytoplazmatické a nukleární MeSH
- tubulin MeSH
Microtubules of all eukaryotic cells are formed by α- and β-tubulin heterodimers. In addition to the well known cytoplasmic tubulins, a subpopulation of tubulin can occur in the nucleus. So far, the potential function of nuclear tubulin has remained elusive. In this work, we show that α- and β-tubulins of various organisms contain multiple conserved nuclear export sequences, which are potential targets of the Exportin 1/CRM1 pathway. We demonstrate exemplarily that these NES motifs are sufficient to mediate export of GFP as model cargo and that this export can be inhibited by leptomycin B, an inhibitor of the Exportin 1/CRM1 pathway. Likewise, leptomycin B causes accumulation of GFP-tagged tubulin in interphase nuclei, in both plant and animal model cells. Our analysis of nuclear tubulin content supports the hypothesis that an important function of nuclear tubulin export is the exclusion of tubulin from interphase nuclei, after being trapped by nuclear envelope reassembly during telophase.
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Boettcher B, Barral Y. The cell biology of open and closed mitosis. Nucleus. 2013;4:160–165. doi: 10.4161/nucl.24676. PubMed DOI PMC
Akoumianaki T, Kardassis D, Polioudaki H, Georgatos SD, Theodoropoulos PA. Nucleocytoplasmic shuttling of soluble tubulin in mammalian cells. J. Cell Sci. 2009;122:1111–1118. doi: 10.1242/jcs.043034. PubMed DOI
Kırlı K, et al. A deep proteomics perspective on CRM1-mediated nuclear export and nucleocytoplasmic partitioning. Elife. 2015;4:1–28. doi: 10.7554/eLife.11466. PubMed DOI PMC
Hobbs RP, Jacob JT, Coulombe PA. Keratins Are Going Nuclear. Dev. Cell. 2016;38:227–233. doi: 10.1016/j.devcel.2016.07.022. PubMed DOI PMC
Kumeta M, Hirai Y, Yoshimura SH, Horigome T, Takeyasu K. Antibody-based analysis reveals ‘filamentous vs. non-filamentous’ and ‘cytoplasmic vs. nuclear’ crosstalk of cytoskeletal proteins. Exp. Cell Res. 2013;319:3226–3237. doi: 10.1016/j.yexcr.2013.07.021. PubMed DOI
Stüven T, Hartmann E, Görlich D. Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes. EMBO J. 2003;22:5928–40. doi: 10.1093/emboj/cdg565. PubMed DOI PMC
Schwarzerová K, et al. Intranuclear accumulation of plant tubulin in response to low temperature. Protoplasma. 2006;227:185–196. doi: 10.1007/s00709-005-0139-x. PubMed DOI
Chen N, et al. OsRAN2, essential for mitosis, enhances cold tolerance in rice by promoting export of intranuclear tubulin and maintaining cell division under cold stress. Plant, Cell Environ. 2011;34:52–64. doi: 10.1111/j.1365-3040.2010.02225.x. PubMed DOI
Merkle T. Nucleo-cytoplasmic transport of proteins and RNA in plants. Plant Cell Rep. 2011;30:153–76. doi: 10.1007/s00299-010-0928-3. PubMed DOI PMC
Cautain B, Hill R, De Pedro N, Link W. Components and regulation of nuclear transport processes. FEBS J. 2015;282:445–462. doi: 10.1111/febs.13163. PubMed DOI PMC
Cavazza, T. & Vernos, I. The RanGTP Pathway: From Nucleo-Cytoplasmic Transport to Spindle Assembly and Beyond. Front. Cell Dev. Biol. 3 (2016). PubMed PMC
Fornerod M, Ohno M, Yoshida M, Mattaj IW. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell. 1997;90:1051–1060. doi: 10.1016/S0092-8674(00)80371-2. PubMed DOI
Neville M, Stutz F, Lee L, Davis LI, Rosbash M. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 1997;7:767–775. doi: 10.1016/S0960-9822(06)00335-6. PubMed DOI
Ossareh-Nazari B, Bachelerie F, Dargemont C. Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science (80-.). 1997;278:141–144. doi: 10.1126/science.278.5335.141. PubMed DOI
Stade K, Ford CS, Guthrie C, Weis K. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell. 1997;90:1041–1050. doi: 10.1016/S0092-8674(00)80370-0. PubMed DOI
Haasen D, Köhler C, Neuhaus G, Merkle T. Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant J. 1999;20:695–705. doi: 10.1046/j.1365-313X.1999.00644.x. PubMed DOI
Ovechkina Y, et al. Spindle formation in Aspergillus is coupled to tubulin movement into the nucleus. Mol. Biol. Cell. 2003;14:2192–2200. doi: 10.1091/mbc.e02-10-0641. PubMed DOI PMC
Menko AS, Tan KB. Nuclear tubulin of tissue culture cells. Biochim. Biophys. Acta. 1980;629:359–70. doi: 10.1016/0304-4165(80)90108-7. PubMed DOI
Walss-Bass C, Kreisberg JI, Ludueña RF. Mechanism of localization of betaII-tubulin in the nuclei of cultured rat kidney mesangial cells. Cell Motil. Cytoskeleton. 2001;49:208–217. doi: 10.1002/cm.1034. PubMed DOI
Walss-Bass C, Xu K, David S, Fellous A, Ludueña RF. Occurrence of nuclear βII-tubulin in cultured cells. Cell Tissue Res. 2002;308:215–223. doi: 10.1007/s00441-002-0539-6. PubMed DOI
Yeh I-T, Ludueña RF. The betaII isotype of tubulin is present in the cell nuclei of a variety of cancers. Cell Motil. Cytoskeleton. 2004;57:96–106. doi: 10.1002/cm.10157. PubMed DOI
Goo YH, et al. Activating signal cointegrator 2 belongs to a novel steady-state complex that contains a subset of trithorax group proteins. Mol. Cell. Biol. 2003;23:140–149. doi: 10.1128/MCB.23.1.140-149.2003. PubMed DOI PMC
Yeh T-S, et al. Nuclear betaII-tubulin associates with the activated notch receptor to modulate notch signaling. Cancer Res. 2004;64:8334–40. doi: 10.1158/0008-5472.CAN-04-2197. PubMed DOI
Mirski SEL, Bielawski JC, Cole SPC. Identification of functional nuclear export sequences in human topoisomerase II alpha and beta. Biochem. Biophys. Res. Commun. 2003;306:905–911. doi: 10.1016/S0006-291X(03)01077-5. PubMed DOI
La Cour T, et al. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 2004;17:527–536. doi: 10.1093/protein/gzh062. PubMed DOI
Nagata T, Nemoto Y, Hasezawa S. Tobacco BY-2 cell line as the HeLa cell in the cell biology of higher plants. Int. Rev. Cytol. Surv. Cell Biol. 1992;132:1–30. doi: 10.1016/S0074-7696(08)62452-3. DOI
Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 2000;42:819–832. doi: 10.1023/A:1006496308160. PubMed DOI
Nakamura M, Naoi K, Shoji T, Hashimoto T. Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol. 2004;45:1330–1334. doi: 10.1093/pcp/pch300. PubMed DOI
Zuo JR, Niu QW, Chua NH. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 2000;24:265–273. doi: 10.1046/j.1365-313x.2000.00868.x. PubMed DOI
An G. High efficiency transformation of cultured tobacco cells. Plant Physiol. 1985;79:568–70. doi: 10.1104/pp.79.2.568. PubMed DOI PMC
Petrasek J, et al. Do phytotropins inhibit auxin efflux by impairing vesicle traffic? PLANT Physiol. 2003;131:254–263. doi: 10.1104/pp.012740. PubMed DOI PMC
Vos JW, et al. The Plant TPX2 Protein Regulates Prospindle Assembly before Nuclear Envelope Breakdown. Plant Cell Online. 2008;20:2783–2797. doi: 10.1105/tpc.107.056796. PubMed DOI PMC
Kudo N, et al. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp. Cell Res. 1998;242:540–7. doi: 10.1006/excr.1998.4136. PubMed DOI
Hara MR, et al. A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1. Nature. 2011;477:349–53. doi: 10.1038/nature10368. PubMed DOI PMC
Kumagai-Sano F, Hayashi T, Sano T, Hasezawa S. Cell cycle synchronization of tobacco BY-2 cells. Nat. Protoc. 2006;1:2621–2627. doi: 10.1038/nprot.2006.381. PubMed DOI
Macurek L, et al. Downregulation of Wip1 phosphatase modulates the cellular threshold of DNA damage signaling in mitosis. Cell Cycle. 2013;12:251–62. doi: 10.4161/cc.23057. PubMed DOI PMC
Nishi K, et al. Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J. Biol. Chem. 1994;269:6320–4. PubMed
Wolff B, Sanglier JJ, Wang Y. Leptomycin B is an inhibitor of nuclear export: Inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol. 1997;4:139–147. doi: 10.1016/S1074-5521(97)90257-X. PubMed DOI
Singh AM, Trost R, Boward B, Dalton S. Utilizing FUCCI reporters to understand pluripotent stem cell biology. Methods. 2016;101:4–10. doi: 10.1016/j.ymeth.2015.09.020. PubMed DOI PMC
Wei X, Henke VG, Strübing C, Brown EB, Clapham DE. Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys. J. 2003;84:1317–1327. doi: 10.1016/S0006-3495(03)74947-9. PubMed DOI PMC
Seibel NM, Eljouni J, Nalaskowski MM, Hampe W. Nuclear localization of enhanced green fluorescent protein homomultimers. Anal. Biochem. 2007;368:95–99. doi: 10.1016/j.ab.2007.05.025. PubMed DOI
Fung HYJ, Fu SC, Brautigam CA, Chook YM. Structural determinants of nuclear export signal orientation in binding to exportin CRM1. Elife. 2015;4:1–19. PubMed PMC
Freitas N, Cunha C. Mechanisms and Signals for the Nuclear Import of Proteins. Curr. Genomics. 2009;10:550–557. doi: 10.2174/138920209789503941. PubMed DOI PMC
Kumeta, M., Yoshimura, S. H., Hejna, J. & Takeyasu, K. Nucleocytoplasmic shuttling of cytoskeletal proteins: Molecular mechanism and biological significance. Int. J. Cell Biol. 2012, (2012). PubMed PMC
Binarová P, et al. Nuclear gamma-tubulin during acentriolar plant mitosis. Plant Cell. 2000;12:433–442. PubMed PMC
Lesca C, et al. DNA damage induce γ-tubulin-RAD51 nuclear complexes in mammalian cells. Oncogene. 2005;24:5165–5172. doi: 10.1038/sj.onc.1208723. PubMed DOI
Höög G, Zarrizi R, von Stedingk K, Jonsson K, Alvarado-Kristensson M. Nuclear localization of γ-tubulin affects E2F transcriptional activity and S-phase progression. FASEB J. 2011;25:3815–3827. doi: 10.1096/fj.11-187484. PubMed DOI PMC
Hotta T, Haraguchi T, Mizuno K. A novel function of plant histone H1: microtubule nucleation and continuous plus end association. Cell Struct. Funct. 2007;32:79–87. doi: 10.1247/csf.07031. PubMed DOI
Xu K, Ludueña RF. Characterization of nuclear betaII-tubulin in tumor cells: a possible novel target for taxol. Cell Motil. Cytoskeleton. 2002;53:39–52. doi: 10.1002/cm.10060. PubMed DOI
Spichal M, Fabre E. The emerging role of the cytoskeleton in chromosome dynamics. Front. Genet. 2017;8:1–12. doi: 10.3389/fgene.2017.00060. PubMed DOI PMC
Xu X, Walter WJ, Liu Q, Machens I, Nick P. A rice class-XIV kinesin enters the nucleus in response to cold. Sci. Rep. 2018;8:3588. doi: 10.1038/s41598-018-21816-w. PubMed DOI PMC