γ-Tubulin is a conserved member of the tubulin superfamily with a function in microtubule nucleation. Proteins of γ-tubulin complexes serve as nucleation templates as well as a majority of other proteins contributing to centrosomal and non-centrosomal nucleation, conserved across eukaryotes. There is a growing amount of evidence of γ-tubulin functions besides microtubule nucleation in transcription, DNA damage response, chromatin remodeling, and on its interactions with tumor suppressors. However, the molecular mechanisms are not well understood. Furthermore, interactions with lamin and SUN proteins of the LINC complex suggest the role of γ-tubulin in the coupling of nuclear organization with cytoskeletons. γ-Tubulin that belongs to the clade of eukaryotic tubulins shows characteristics of both prokaryotic and eukaryotic tubulins. Both human and plant γ-tubulins preserve the ability of prokaryotic tubulins to assemble filaments and higher-order fibrillar networks. γ-Tubulin filaments, with bundling and aggregating capacity, are suggested to perform complex scaffolding and sequestration functions. In this review, we discuss a plethora of γ-tubulin molecular interactions and cellular functions, as well as recent advances in understanding the molecular mechanisms behind them.

Institute of Microbiology of the Czech Academy of Sciences Vídeňská 1083 142 20 Prague Czech Republic

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Pilhofer M., Ladinsky M.S., McDowall A.W., Petroni G., Jensen G.J. Microtubules in bacteria: Ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol. 2011;9:e1001213. doi: 10.1371/journal.pbio.1001213. PubMed DOI PMC

Chumova J., Trogelova L., Kourova H., Volc J., Sulimenko V., Halada P., Kucera O., Benada O., Kucharova A., Klebanovych A., et al. gamma-Tubulin has a conserved intrinsic property of self-polymerization into double stranded filaments and fibrillar networks. Biochim. Biophys. Acta. 2018;1865:734–748. doi: 10.1016/j.bbamcr.2018.02.009. PubMed DOI

Yutin N., Koonin E.V. Archaeal origin of tubulin. Biol. Direct. 2012;7:10. doi: 10.1186/1745-6150-7-10. PubMed DOI PMC

Janke C. The tubulin code: Molecular components, readout mechanisms, and functions. J. Cell Biol. 2014;206:461–472. doi: 10.1083/jcb.201406055. PubMed DOI PMC

Vinopal S., Cernohorska M., Sulimenko V., Sulimenko T., Vosecka V., Flemr M., Draberova E., Draber P. gamma-Tubulin 2 nucleates microtubules and is downregulated in mouse early embryogenesis. PloS ONE. 2012;7:e29919. doi: 10.1371/annotation/5dd084b1-20e6-4e1f-88e0-dfe05289da08. PubMed DOI PMC

Oegema K., Wiese C., Martin O.C., Milligan R.A., Iwamatsu A., Mitchison T.J., Zheng Y. Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubules. J. Cell Biol. 1999;144:721–733. doi: 10.1083/jcb.144.4.721. PubMed DOI PMC

Yuba-Kubo A., Kubo A., Hata M., Tsukita S. Gene knockout analysis of two gamma-tubulin isoforms in mice. Dev. Biol. 2005;282:361–373. doi: 10.1016/j.ydbio.2005.03.031. PubMed DOI

Draberova E., Sulimenko V., Vinopal S., Sulimenko T., Sladkova V., D’Agostino L., Sobol M., Hozak P., Kren L., Katsetos C.D., et al. Differential expression of human gamma-tubulin isotypes during neuronal development and oxidative stress points to a gamma-tubulin-2 prosurvival function. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol. 2017;31:1828–1846. doi: 10.1096/fj.201600846RR. PubMed DOI

Sulimenko V., Sulimenko T., Poznanovic S., Nechiporuk-Zloy V., Bohm K.J., Macurek L., Unger E., Draber P. Association of brain gamma-tubulins with alpha beta-tubulin dimers. Biochem. J. 2002;365:889–895. doi: 10.1042/bj20020175. PubMed DOI PMC

Detraves C., Mazarguil H., Lajoie-Mazenc I., Julian M., Raynaud-Messina B., Wright M. Protein complexes containing gamma-tubulin are present in mammalian brain microtubule protein preparations. Cell Motil. Cytoskeleton. 1997;36:179–189. doi: 10.1002/(SICI)1097-0169(1997)36:2<179::AID-CM7>3.0.CO;2-4. PubMed DOI

Moudjou M., Bordes N., Paintrand M., Bornens M. gamma-Tubulin in mammalian cells: The centrosomal and the cytosolic forms. J. Cell Sci. 1996;109:875–887. PubMed

Stumpff J., Kellogg D.R., Krohne K.A., Su T.T. Drosophila Wee1 interacts with members of the gammaTURC and is required for proper mitotic-spindle morphogenesis and positioning. Curr. Biol. 2005;15:1525–1534. doi: 10.1016/j.cub.2005.07.031. PubMed DOI PMC

Vogel J., Drapkin B., Oomen J., Beach D., Bloom K., Snyder M. Phosphorylation of gamma-tubulin regulates microtubule organization in budding yeast. Dev. Cell. 2001;1:621–631. doi: 10.1016/S1534-5807(01)00073-9. PubMed DOI

Starita L.M., Machida Y., Sankaran S., Elias J.E., Griffin K., Schlegel B.P., Gygi S.P., Parvin J.D. BRCA1-dependent ubiquitination of gamma-tubulin regulates centrosome number. Mol. Cell. Biol. 2004;24:8457–8466. doi: 10.1128/MCB.24.19.8457-8466.2004. PubMed DOI PMC

Lee Y.J., Liu B. Microtubule nucleation for the assembly of acentrosomal microtubule arrays in plant cells. New Phytol. 2019 doi: 10.1111/nph.15705. PubMed DOI

Roostalu J., Surrey T. Microtubule nucleation: Beyond the template. Nat. Rev. Mol. Cell Biol. 2017;18:702–710. doi: 10.1038/nrm.2017.75. PubMed DOI

Erickson H.P., Stoffler D. Protofilaments and rings, two conformations of the tubulin family conserved from bacterial FtsZ to alpha/beta and gamma tubulin. J. Cell Biol. 1996;135:5–8. doi: 10.1083/jcb.135.1.5. PubMed DOI PMC

Pastuglia M., Azimzadeh J., Goussot M., Camilleri C., Belcram K., Evrard J.L., Schmit A.C., Guerche P., Bouchez D. Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell. 2006;18:1412–1425. doi: 10.1105/tpc.105.039644. PubMed DOI PMC

Binarova P., Cenklova V., Prochazkova J., Doskocilova A., Volc J., Vrlik M., Bogre L. Gamma-tubulin is essential for acentrosomal microtubule nucleation and coordination of late mitotic events in Arabidopsis. Plant Cell. 2006;18:1199–1212. doi: 10.1105/tpc.105.038364. PubMed DOI PMC

Kong Z., Hotta T., Lee Y.R., Horio T., Liu B. The gamma-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana. Plant Cell. 2010;22:191–204. doi: 10.1105/tpc.109.071191. PubMed DOI PMC

Nakamura M., Yagi N., Kato T., Fujita S., Kawashima N., Ehrhardt D.W., Hashimoto T. Arabidopsis GCP3-interacting protein 1/MOZART 1 is an integral component of the gamma-tubulin-containing microtubule nucleating complex. Plant J. Cell Mol. Biol. 2012;71:216–225. doi: 10.1111/j.1365-313X.2012.04988.x. PubMed DOI

Binarova P., Hause B., Dolezel J., Draber P. Association of gamma-tubulin with kinetochore/centromeric region of plant chromosomes. Plant J. 1998;14:751–757. doi: 10.1046/j.1365-313x.1998.00166.x. DOI

Mishra R.K., Chakraborty P., Arnaoutov A., Fontoura B.M.A., Dasso M. The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat. Cell Biol. 2010;12:164–169. doi: 10.1038/ncb2016. PubMed DOI PMC

Meunier S., Vernos I. Acentrosomal Microtubule Assembly in Mitosis: The Where, When, and How. Trends Cell Biol. 2016;26:80–87. doi: 10.1016/j.tcb.2015.09.001. PubMed DOI

Lee Y.R.J., Hiwatashi Y., Hotta T., Xie T.T., Doonan J.H., Liu B. The Mitotic Function of Augmin Is Dependent on Its Microtubule-Associated Protein Subunit EDE1 in Arabidopsis thaliana. Curr. Biol. 2017;27:3891–3897. doi: 10.1016/j.cub.2017.11.030. PubMed DOI

Goshima G., Mayer M., Zhang N., Stuurman N., Vale R.D. Augmin: A protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 2008;181:421–429. doi: 10.1083/jcb.200711053. PubMed DOI PMC

Samejima I., Lourenco P.C., Snaith H.A., Sawin K.E. Fission yeast mto2p regulates microtubule nucleation by the centrosomin-related protein mto1p. Mol. Biol. Cell. 2005;16:3040–3051. doi: 10.1091/mbc.e04-11-1003. PubMed DOI PMC

Goshima G., Kimura A. New look inside the spindle: Microtubule-dependent microtubule generation within the spindle. Curr. Opin. Cell Biol. 2010;22:44–49. doi: 10.1016/j.ceb.2009.11.012. PubMed DOI

Liu T., Tian J., Wang G.D., Yu Y.J., Wang C.F., Ma Y.P., Zhang X.X., Xia G.X., Liu B., Kong Z.S. Augmin Triggers Microtubule-Dependent Microtubule Nucleation in Interphase Plant Cells. Curr. Biol. 2014;24:2708–2713. doi: 10.1016/j.cub.2014.09.053. PubMed DOI

Wang Z., Wu T., Shi L., Zhang L., Zheng W., Qu J.Y., Niu R., Qi R.Z. Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J. Biol. Chem. 2010;285:22658–22665. doi: 10.1074/jbc.M110.105965. PubMed DOI PMC

Chabin-Brion K., Marceiller J., Perez F., Settegrana C., Drechou A., Durand G., Pous C. The golgi complex is a microtubule-organizing organelle. Mol. Biol. Cell. 2001;12:2047–2060. doi: 10.1091/mbc.12.7.2047. PubMed DOI PMC

Drykova D., Cenklova V., Sulimenko V., Volc J., Draber P., Binarova P. Plant gamma-tubulin interacts with alphabeta-tubulin dimers and forms membrane-associated complexes. Plant Cell. 2003;15:465–480. doi: 10.1105/tpc.007005. PubMed DOI PMC

Bao X.X., Spanos C., Kojidani T., Lynch E.M., Rappsilber J., Hiraoka Y., Haraguchi T., Sawin K.E. Exportin Crm1 is repurposed as a docking protein to generate microtubule organizing centers at the nuclear pore. Elife. 2018;7:34. doi: 10.7554/eLife.33465. PubMed DOI PMC

Shen Y., Wang K., Qi R.Z. The catalytic subunit of DNA polymerase delta is a nucleocytoplasmic shuttling protein. Exp. Cell Res. 2019 doi: 10.1016/j.yexcr.2019.01.003. PubMed DOI

Shen Y.H., Liu P.F., Jiang T.L., Hu Y., Au F.K.C., Qi R.Z. The catalytic subunit of DNA polymerase delta inhibits gamma TuRC activity and regulates Golgi-derived microtubules. Nat. Commun. 2017;8:13. doi: 10.1038/s41467-017-00694-2. PubMed DOI PMC

Petrovska B., Jerabkova H., Kohoutova L., Cenklova V., Pochylova Z., Gelova Z., Kocarova G., Vachova L., Kurejova M., Tomastikova E., et al. Overexpressed TPX2 causes ectopic formation of microtubular arrays in the nuclei of acentrosomal plant cells. J. Exp. Bot. 2013;64:4575–4587. doi: 10.1093/jxb/ert271. PubMed DOI PMC

Cuschieri L., Miller R., Vogel J. Gamma-tubulin is required for proper recruitment and assembly of Kar9-Bim1 complexes in budding yeast. Mol. Biol. Cell. 2006;17:4420–4434. doi: 10.1091/mbc.e06-03-0245. PubMed DOI PMC

Raynaud-Messina B., Merdes A. Gamma-tubulin complexes and microtubule organization. Curr. Opin. Cell Biol. 2007;19:24–30. doi: 10.1016/j.ceb.2006.12.008. PubMed DOI

Hubert T., Perdu S., Vandekerckhove J., Gettemans J. gamma-Tubulin localizes at actin-based membrane protrusions and inhibits formation of stress-fibers. Biochem. Biophys. Res. Commun. 2011;408:248–252. doi: 10.1016/j.bbrc.2011.04.007. PubMed DOI

Oriolo A.S., Wald F.A., Canessa G., Salas P.J. GCP6 binds to intermediate filaments: A novel function of keratins in the organization of microtubules in epithelial cells. Mol. Biol. Cell. 2007;18:781–794. doi: 10.1091/mbc.e06-03-0201. PubMed DOI PMC

Rossello C.A., Lindstrom L., Glindre J., Eklund G., Alvarado-Kristensson M. Gamma-tubulin coordinates nuclear envelope assembly around chromatin. Heliyon. 2016;2:e00166. doi: 10.1016/j.heliyon.2016.e00166. PubMed DOI PMC

Rios R.M. The centrosome-Golgi apparatus nexus. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2014;369:20130462. doi: 10.1098/rstb.2013.0462. PubMed DOI PMC

Lindström L., Li T., Malycheva D., Kancharla A., Nilsson H., Vishnu N., Mulder H., Johansson M., Rosselló C.A., Alvarado-Kristensson M. The GTPase domain of gamma-tubulin is required for normal mitochondrial function and spatial organization. Commun. Biol. 2018;1:37. doi: 10.1038/s42003-018-0037-3. PubMed DOI PMC

Hehnly H., Doxsey S. Rab11 Endosomes Contribute to Mitotic Spindle Organization and Orientation. Dev. Cell. 2014;28:497–507. doi: 10.1016/j.devcel.2014.01.014. PubMed DOI PMC

Lindstrom L., Alvarado-Kristensson M. Characterization of gamma-tubulin filaments in mammalian cells. Biochim. Biophys. Acta-Mol. Cell Res. 2018;1865:158–171. doi: 10.1016/j.bbamcr.2017.10.008. PubMed DOI

Melki R., Vainberg I.E., Chow R.L., Cowan N.J. Chaperonin-mediated folding of vertebrate actin-related protein and gamma-tubulin. J. Cell Biol. 1993;122:1301–1310. doi: 10.1083/jcb.122.6.1301. PubMed DOI PMC

Inclan Y.F., Nogales E. Structural models for the self-assembly and microtubule interactions of gamma-, delta- and epsilon-tubulin. J. Cell Sci. 2001;114:413–422. PubMed

Vassilev A., Kimble M., Silflow C.D., LaVoie M., Kuriyama R. Identification of intrinsic dimer and overexpressed monomeric forms of gamma-tubulin in Sf9 cells infected with baculovirus containing the Chlamydomonas gamma-tubulin sequence. J. Cell Sci. 1995;108:1083–1092. PubMed

Aldaz H., Rice L.M., Stearns T., Agard D.A. Insights into microtubule nucleation from the crystal structure of human gamma-tubulin. Nature. 2005;435:523–527. doi: 10.1038/nature03586. PubMed DOI

Leguy R., Melki R., Pantaloni D., Carlier M.F. Monomeric gamma-tubulin nucleates microtubules. J. Biol. Chem. 2000;275:21975–21980. doi: 10.1074/jbc.M000688200. PubMed DOI

Pouchucq L., Lobos-Ruiz P., Araya G., Valpuesta J.M., Monasterio O. The chaperonin CCT promotes the formation of fibrillar aggregates of gamma-tubulin. BBA-Proteins Proteom. 2018;1866:519–526. doi: 10.1016/j.bbapap.2018.01.007. PubMed DOI

Pilhofer M., Jensen G.J. The bacterial cytoskeleton: More than twisted filaments. Curr. Opin. Cell Biol. 2013;25:125–133. doi: 10.1016/j.ceb.2012.10.019. PubMed DOI PMC

Ghosal D., Lowe J. Collaborative protein filaments. EMBO J. 2015;34:2312–2320. doi: 10.15252/embj.201591756. PubMed DOI PMC

Strauss M.P., Liew A.T., Turnbull L., Whitchurch C.B., Monahan L.G., Harry E.J. 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: Implications for triggering cytokinesis. PLoS Biol. 2012;10:e1001389. doi: 10.1371/journal.pbio.1001389. PubMed DOI PMC

Kollman J.M., Polka J.K., Zelter A., Davis T.N., Agard D.A. Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature. 2010;466:879–882. doi: 10.1038/nature09207. PubMed DOI PMC

Noble J.W., Hunter D.V., Roskelley C.D., Chan E.K.L., Mills J. Loukoumasomes Are Distinct Subcellular Structures from Rods and Rings and Are Structurally Associated with MAP2 and the Nuclear Envelope in Retinal Cells. PLoS ONE. 2016;11:e0165162. doi: 10.1371/journal.pone.0165162. PubMed DOI PMC

Hendrickson T.W., Yao J., Bhadury S., Corbett A.H., Joshi H.C. Conditional Mutations in gamma-Tubulin Reveal Its Involvement in Chromosome Segregation and Cytokinesis. Mol. Biol. Cell. 2001;12:2469–2481. doi: 10.1091/mbc.12.8.2469. PubMed DOI PMC

Prigozhina N.L., Oakley C.E., Lewis A.M., Nayak T., Osmani S.A., Oakley B.R. Gamma-tubulin plays an essential role in the coordination of mitotic events. Mol. Biol. Cell. 2004;15:1374–1386. doi: 10.1091/mbc.e03-06-0405. PubMed DOI PMC

Nayak T., Edgerton-Morgan H., Horio T., Xiong Y., De Souza C.P., Osmani S.A., Oakley B.R. Gamma-tubulin regulates the anaphase-promoting complex/cyclosome during interphase. J. Cell Biol. 2010;190:317–330. doi: 10.1083/jcb.201002105. PubMed DOI PMC

Binarova P., Cenklova V., Hause B., Kubatova E., Lysak M., Dolezel J., Bogre L., Draber P. Nuclear gamma-tubulin during acentriolar plant mitosis. Plant Cell. 2000;12:433–442. doi: 10.1105/tpc.12.3.433. PubMed DOI PMC

Lesca C., Germanier M., Raynaud-Messina B., Pichereaux C., Etievant C., Emond S., Burlet-Schiltz O., Monsarrat B., Wright M., Defais M. DNA damage induce gamma-tubulin-RAD51 nuclear complexes in mammalian cells. Oncogene. 2005;24:5165–5172. doi: 10.1038/sj.onc.1208723. PubMed DOI

Arquint C., Gabryjonczyk A.M., Nigg E.A. Centrosomes as signalling centres. Philos. Trans. R. Soc. B-Biol. Sci. 2014;369:12. doi: 10.1098/rstb.2013.0464. PubMed DOI PMC

Zhang S., Hemmerich P., Grosse F. Centrosomal localization of DNA damage checkpoint proteins. J. Cell. Biochem. 2007;101:451–465. doi: 10.1002/jcb.21195. PubMed DOI

Matsuzawa A., Kanno S., Nakayama M., Mochiduki H., Wei L., Shimaoka T., Furukawa Y., Kato K., Shibata S., Yasui A., et al. The BRCA1/BARD1-interacting protein OLA1 functions in centrosome regulation. Mol. Cell. 2014;53:101–114. doi: 10.1016/j.molcel.2013.10.028. PubMed DOI

Hubert T., Vandekerckhove J., Gettemans J. Cdk1 and BRCA1 target gamma-tubulin to microtubule domains. Biochem. Biophys. Res. Commun. 2011;414:240–245. doi: 10.1016/j.bbrc.2011.09.064. PubMed DOI

Horejsi B., Vinopal S., Sladkova V., Draberova E., Sulimenko V., Sulimenko T., Vosecka V., Philimonenko A., Hozak P., Katsetos C.D., et al. Nuclear gamma-tubulin associates with nucleoli and interacts with tumor suppressor protein C53. J. Cell Physiol. 2012;227:367–382. doi: 10.1002/jcp.22772. PubMed DOI

Mullee L.I., Morrison C.G. Centrosomes in the DNA damage response--the hub outside the centre. Chromosome Res. 2016;24:35–51. doi: 10.1007/s10577-015-9503-7. PubMed DOI

Vazquez M., Cooper M.T., Zurita M.E., Kennison J.A. gammaTub23C interacts genetically with Brahma chromatin-remodeling complexes in Drosophila melanogaster. Genetics. 2008;180:835–843. doi: 10.1534/genetics.108.093492. PubMed DOI PMC

Hoog G., Zarrizi R., von Stedingk K., Jonsson K., Alvarado-Kristensson M. Nuclear localization of gamma-tubulin affects E2F transcriptional activity and S-phase progression. FASEB J. 2011;25:3815–3827. doi: 10.1096/fj.11-187484. PubMed DOI PMC

Kohoutova L., Kourova H., Nagy S.K., Volc J., Halada P., Meszaros T., Meskiene I., Bogre L., Binarova P. The Arabidopsis mitogen-activated protein kinase 6 is associated with gamma-tubulin on microtubules, phosphorylates EB1c and maintains spindle orientation under nitrosative stress. New Phytol. 2015;207:1061–1074. doi: 10.1111/nph.13501. PubMed DOI

Katsetos C.D., Draberova E., Legido A., Draber P. Tubulin Targets in the Pathobiology and Therapy of Glioblastoma Multiforme. II. gamma-Tubulin. J. Cell. Physiol. 2009;221:514–520. doi: 10.1002/jcp.21884. PubMed DOI

Katsetos C.D., Draberova E., Smejkalova B., Reddy G., Bertrand L., de Chadarevian J.P., Legido A., Nissanov J., Baas P.W., Draber P. Class III beta-tubulin and gamma-tubulin are co-expressed and form complexes in human glioblastoma cells. Neurochem. Res. 2007;32:1387–1398. doi: 10.1007/s11064-007-9321-1. PubMed DOI

Ehlen A., Rossello C.A., von Stedingk K., Hoog G., Nilsson E., Pettersson H.M., Jirstrom K., Alvarado-Kristensson M. Tumors with nonfunctional retinoblastoma protein are killed by reduced gamma-tubulin levels. J. Biol. Chem. 2012;287:17241–17247. doi: 10.1074/jbc.M112.357038. PubMed DOI PMC

Alvarado-Kristensson M. gamma-tubulin as a signal-transducing molecule and meshwork with therapeutic potential. Signal Transduct. Target. Ther. 2018;3:6. doi: 10.1038/s41392-018-0021-x. PubMed DOI PMC

Woodruff J.B., Wueseke O., Viscardi V., Mahamid J., Ochoa S.D., Bunkenborg J., Widlund P.O., Pozniakovsky A., Zanin E., Bahmanyar S., et al. Centrosomes. Regulated assembly of a supramolecular centrosome scaffold in vitro. Science. 2015;348:808–812. doi: 10.1126/science.aaa3923. PubMed DOI PMC

Ramer M.S., Cruz Cabrera M.A., Alan N., Scott A.L., Inskip J.A. A new organellar complex in rat sympathetic neurons. PLoS ONE. 2010;5:e10872. doi: 10.1371/journal.pone.0010872. PubMed DOI PMC

Serebryannyy L., Misteli T. Protein sequestration at the nuclear periphery as a potential regulatory mechanism in premature aging. J. Cell Biol. 2018;217:21–37. doi: 10.1083/jcb.201706061. PubMed DOI PMC

Ciska M., Moreno Diaz de la Espina S. The intriguing plant nuclear lamina. Front. Plant Sci. 2014;5:166. doi: 10.3389/fpls.2014.00166. PubMed DOI PMC

Fiserova J., Kiseleva E., Goldberg M.W. Nuclear envelope and nuclear pore complex structure and organization in tobacco BY-2 cells. Plant J. 2009;59:243–255. doi: 10.1111/j.1365-313X.2009.03865.x. PubMed DOI

Crisp M., Liu Q., Roux K., Rattner J.B., Shanahan C., Burke B., Stahl P.D., Hodzic D. Coupling of the nucleus and cytoplasm: Role of the LINC complex. J. Cell Biol. 2006;172:41–53. doi: 10.1083/jcb.200509124. PubMed DOI PMC

Gundersen G.G., Worman H.J. Nuclear positioning. Cell. 2013;152:1376–1389. doi: 10.1016/j.cell.2013.02.031. PubMed DOI PMC

Haque F., Lloyd D.J., Smallwood D.T., Dent C.L., Shanahan C.M., Fry A.M., Trembath R.C., Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol. Cell. Biol. 2006;26:3738–3751. doi: 10.1128/MCB.26.10.3738-3751.2006. PubMed DOI PMC

Patel J.T., Bottrill A., Prosser S.L., Jayaraman S., Straatman K., Fry A.M., Shackleton S. Mitotic phosphorylation of SUN1 loosens its connection with the nuclear lamina while the LINC complex remains intact. Nucleus. 2014;5:462–473. doi: 10.4161/nucl.36232. PubMed DOI PMC

Zhang X.C., Lei K., Yuan X.B., Wu X.H., Zhuang Y., Xu T., Xu R., Han M. SUN1/2 and Syne/Nesprin-1/2 Complexes Connect Centrosome to the Nucleus during Neurogenesis and Neuronal Migration in Mice. Neuron. 2009;64:173–187. doi: 10.1016/j.neuron.2009.08.018. PubMed DOI PMC

Zhu R.J., Antoku S., Gundersen G.G. Centrifugal Displacement of Nuclei Reveals Multiple LINC Complex Mechanisms for Homeostatic Nuclear Positioning. Curr. Biol. 2017;27:3097–3110. doi: 10.1016/j.cub.2017.08.073. PubMed DOI PMC

Calvi A., Wong A.S.W., Wright G., Wong E.S.M., Loo T.H., Stewart C.L., Burke B. SUN4 is essential for nuclear remodeling during mammalian spermiogenesis. Dev. Biol. 2015;407:321–330. doi: 10.1016/j.ydbio.2015.09.010. PubMed DOI

Lei K., Zhu X.Q., Xu R., Shao C.L., Xu T., Zhuang Y., Han M. Inner Nuclear Envelope Proteins SUN1 and SUN2 Play a Prominent Role in the DNA Damage Response. Curr. Biol. 2012;22:1609–1615. doi: 10.1016/j.cub.2012.06.043. PubMed DOI PMC

Yoshida M., Katsuyama S., Tateho K., Nakamura H., Miyoshi J., Ohba T., Matsuhara H., Miki F., Okazaki K., Haraguchi T., et al. Microtubule-organizing center formation at telomeres induces meiotic telomere clustering. J. Cell Biol. 2013;200:385–395. doi: 10.1083/jcb.201207168. PubMed DOI PMC

Ding X., Xu R., Yu J.H., Xu T., Zhuang Y., Han M. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell. 2007;12:863–872. doi: 10.1016/j.devcel.2007.03.018. PubMed DOI

Varas J., Graumann K., Osman K., Pradillo M., Evans D.E., Santos J.L., Armstrong S.J. Absence of SUN1 and SUN2 proteins in Arabidopsis thaliana leads to a delay in meiotic progression and defects in synapsis and recombination. Plant J. 2015;81:329–346. doi: 10.1111/tpj.12730. PubMed DOI

Murphy S.P., Gumber H.K., Mao Y., Bass H.W. A dynamic meiotic SUN belt includes the zygotene-stage telomere bouquet and is disrupted in chromosome segregation mutants of maize (Zea mays L.) Front. Plant Sci. 2014;5:11. doi: 10.3389/fpls.2014.00314. PubMed DOI PMC

Oda Y., Fukuda H. Dynamics of Arabidopsis SUN proteins during mitosis and their involvement in nuclear shaping. Plant J. 2011;66:629–641. doi: 10.1111/j.1365-313X.2011.04523.x. PubMed DOI

Graumann K., Runions J., Evans D.E. Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 2010;61:134–144. doi: 10.1111/j.1365-313X.2009.04038.x. PubMed DOI

Zhou X., Groves N.R., Meier I. Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1. Nucleus. 2015;6:144–153. doi: 10.1080/19491034.2014.1003512. PubMed DOI PMC

Groves N.R., Biel A.M., Newman-Griffis A.H., Meier I. Dynamic Changes in Plant Nuclear Organization in Response to Environmental and Developmental Signals. Plant Physiol. 2018;176:230–241. doi: 10.1104/pp.17.00788. PubMed DOI PMC

Meier I. LINCing the eukaryotic tree of life—Towards a broad evolutionary comparison of nucleocytoplasmic bridging complexes. J. Cell Sci. 2016;129:3523–3531. doi: 10.1242/jcs.186700. PubMed DOI

Graumann K. Evidence for LINC1-SUN associations at the plant nuclear periphery. PLoS ONE. 2014;9:e93406. doi: 10.1371/journal.pone.0093406. PubMed DOI PMC

Pawar V., Poulet A., Detourne G., Tatout C., Vanrobays E., Evans D.E., Graumann K. A novel family of plant nuclear envelope-associated proteins. J. Exp. Bot. 2016;67:5699–5710. doi: 10.1093/jxb/erw332. PubMed DOI

Gimpel P., Lee Y.L., Sobota R.M., Calvi A., Koullourou V., Patel R., Mamchaoui K., Nedelec F., Shackleton S., Schmoranzer J., et al. Nesprin-1alpha-Dependent Microtubule Nucleation from the Nuclear Envelope via Akap450 Is Necessary for Nuclear Positioning in Muscle Cells. Curr. Biol. 2017;27:2999.e9–3009.e9. doi: 10.1016/j.cub.2017.08.031. PubMed DOI PMC

Larsson V.J. Ph.D. Thesis. Stockholm University; Stockholm, Sweden: 2018. Characterization of the Inner Nuclear Membrane Protein Samp1, during Interphase and Mitosis.

Larsson V.J., Jafferali M.H., Vijayaraghavan B., Figueroa R.A., Hallberg E. Mitotic spindle assembly and gamma-tubulin localisation depend on the integral nuclear membrane protein Samp1. J. Cell Sci. 2018;131 doi: 10.1242/jcs.211664. PubMed DOI PMC

Teixido-Travesa N., Villen J., Lacasa C., Bertran M.T., Archinti M., Gygi S.P., Caelles C., Roig J., Luders J. The gammaTuRC revisited: A comparative analysis of interphase and mitotic human gammaTuRC redefines the set of core components and identifies the novel subunit GCP8. Mol. Biol. Cell. 2010;21:3963–3972. doi: 10.1091/mbc.e10-05-0408. PubMed DOI PMC

Batzenschlager M., Masoud K., Janski N., Houlne G., Herzog E., Evrard J.L., Baumberger N., Erhardt M., Nomine Y., Kieffer B., et al. The GIP gamma-tubulin complex-associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Front. Plant Sci. 2013;4:480. doi: 10.3389/fpls.2013.00480. PubMed DOI PMC

Batzenschlager M., Lermontova I., Schubert V., Fuchs J., Berr A., Koini M.A., Houlne G., Herzog E., Rutten T., Alioua A., et al. Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture. Proc. Natl. Acad. Sci. USA. 2015;112:8656–8660. doi: 10.1073/pnas.1506351112. PubMed DOI PMC

Chaboute M.E., Berr A. GIP Contributions to the Regulation of Centromere at the Interface Between the Nuclear Envelope and the Nucleoplasm. Front. Plant Sci. 2016;7:118. doi: 10.3389/fpls.2016.00118. PubMed DOI PMC

Fal K., Asnacios A., Chaboute M.E., Hamant O. Nuclear envelope: A new frontier in plant mechanosensing? Biophys. Rev. 2017;9:389–403. doi: 10.1007/s12551-017-0302-6. PubMed DOI PMC

Le H.Q., Ghatak S., Yeung C.Y., Tellkamp F., Gunschmann C., Dieterich C., Yeroslaviz A., Habermann B., Pombo A., Niessen C.M., et al. Mechanical regulation of transcription controls Polycomb-mediated gene silencing during lineage commitment. Nat. Cell Biol. 2016;18:864–875. doi: 10.1038/ncb3387. PubMed DOI

Liu B., Zhou Z. Lamin A/C, laminopathies and premature ageing. Histol. Histopathol. 2008;23:747–763. doi: 10.14670/HH-23.747. PubMed DOI

Hamilton E.S., Jensen G.S., Maksaev G., Katims A., Sherp A.M., Haswell E.S. Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science. 2015;350:438–441. doi: 10.1126/science.aac6014. PubMed DOI PMC

Doskocilova A., Plihal O., Volc J., Chumova J., Kourova H., Halada P., Petrovska B., Binarova P. A nodulin/glutamine synthetase-like fusion protein is implicated in the regulation of root morphogenesis and in signalling triggered by flagellin. Planta. 2011;234:459–476. doi: 10.1007/s00425-011-1419-7. PubMed DOI

Nemeth K., Salchert K., Putnoky P., Bhalerao R., Koncz-Kalman Z., Stankovic-Stangeland B., Bako L., Mathur J., Okresz L., Stabel S., et al. Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev. 1998;12:3059–3073. doi: 10.1101/gad.12.19.3059. PubMed DOI PMC

Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI

Curran A., Chang I.F., Chang C.L., Garg S., Miguel R.M., Barron Y.D., Li Y., Romanowsky S., Cushman J.C., Gribskov M., et al. Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Front. Plant Sci. 2011;2:36. doi: 10.3389/fpls.2011.00036. PubMed DOI PMC

Benschop J.J., Mohammed S., O’Flaherty M., Heck A.J., Slijper M., Menke F.L. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell Proteom. 2007;6:1198–1214. doi: 10.1074/mcp.M600429-MCP200. PubMed DOI

Oda Y. Cortical microtubule rearrangements and cell wall patterning. Front. Plant Sci. 2015;6 doi: 10.3389/fpls.2015.00236. PubMed DOI PMC

Tamura K., Fukao Y., Iwamoto M., Haraguchi T., Hara-Nishimura I. Identification and Characterization of Nuclear Pore Complex Components in Arabidopsis thaliana. Plant Cell. 2010;22:4084–4097. doi: 10.1105/tpc.110.079947. PubMed DOI PMC

Bonnet A., Palancade B. Regulation of mRNA Trafficking by Nuclear Pore Complexes. Genes. 2014;5:767–791. doi: 10.3390/genes5030767. PubMed DOI PMC

Lee J.-Y., Lee H.-S., Wi S.-J., Park K.Y., Schmit A.-C., Pai H.-S. Dual functions of Nicotiana benthamiana Rae1 in interphase and mitosis. Plant J. 2009;59:278–291. doi: 10.1111/j.1365-313X.2009.03869.x. PubMed DOI

Wagstaff J., Lowe J. Prokaryotic cytoskeletons: Protein filaments organizing small cells. Nat. Rev. Microbiol. 2018;16:187–201. doi: 10.1038/nrmicro.2017.153. PubMed DOI

Izore T., Kureisaite-Ciziene D., McLaughlin S.H., Lowe J. Crenactin forms actin-like double helical filaments regulated by arcadin-2. Elife. 2016;5 doi: 10.7554/eLife.21600. PubMed DOI PMC

Sakamoto Y., Takagi S. LITTLE NUCLEI 1 and 4 Regulate Nuclear Morphology in Arabidopsis thaliana. Plant Cell Physiol. 2013;54:622–633. doi: 10.1093/pcp/pct031. PubMed DOI

Wang H.Y., Dittmer T.A., Richards E.J. Arabidopsis CROWDED NUCLEI (CRWN) proteins are required for nuclear size control and heterochromatin organization. BMC Plant Biol. 2013;13 doi: 10.1186/1471-2229-13-200. PubMed DOI PMC

Sundararajan K., Miguel A., Desmarais S.M., Meier E.L., Casey Huang K., Goley E.D. The bacterial tubulin FtsZ requires its intrinsically disordered linker to direct robust cell wall construction. Nat. Commun. 2015;6:7281. doi: 10.1038/ncomms8281. PubMed DOI PMC

Magyar Z., Atanassova A., De Veylder L., Rombauts S., Inze D. Characterization of two distinct DP-related genes from Arabidopsis thaliana. FEBS Lett. 2000;486:79–87. doi: 10.1016/S0014-5793(00)02238-9. PubMed DOI

Draberova E., D’Agostino L., Caracciolo V., Sladkova V., Sulimenko T., Sulimenko V., Sobol M., Maounis N.F., Tzelepis E., Mahera E., et al. Overexpression and Nucleolar Localization of gamma-Tubulin Small Complex Proteins GCP2 and GCP3 in Glioblastoma. J. Neuropathol. Exp. Neurol. 2015;74:723–742. doi: 10.1097/NEN.0000000000000212. PubMed DOI

Horvath B.M., Kourova H., Nagy S., Nemeth E., Magyar Z., Papdi C., Ahmad Z., Sanchez-Perez G.F., Perilli S., Blilou I., et al. Arabidopsis RETINOBLASTOMA RELATED directly regulates DNA damage responses through functions beyond cell cycle control. EMBO J. 2017;36:1261–1278. doi: 10.15252/embj.201694561. PubMed DOI PMC

Novakova M., Draberova E., Schurmann W., Czihak G., Viklicky V., Dr-aber P. gamma-Tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil. Cytoskeleton. 1996;33:38–51. doi: 10.1002/(SICI)1097-0169(1996)33:1<38::AID-CM5>3.0.CO;2-E. PubMed DOI

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