γ-Tubulin Complexes and Fibrillar Arrays: Two Conserved High Molecular Forms with Many Cellular Functions
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
Grantová podpora
MSM200201901
Akademie Věd České Republiky
2018-00997
Formas project
PubMed
33915825
PubMed Central
PMC8066788
DOI
10.3390/cells10040776
PII: cells10040776
Knihovny.cz E-zdroje
- Klíčová slova
- fibrillar arrays, gamma-tubulin, gamma-tubulin complexes, microtubules, nucleation, plants, sequestration, signaling,
- MeSH
- buňky metabolismus MeSH
- centrozom metabolismus MeSH
- lidé MeSH
- rostliny metabolismus MeSH
- sekvence aminokyselin MeSH
- tubulin chemie metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- tubulin MeSH
Higher plants represent a large group of eukaryotes where centrosomes are absent. The functions of γ-tubulin small complexes (γ-TuSCs) and γ-tubulin ring complexes (γ-TuRCs) in metazoans and fungi in microtubule nucleation are well established and the majority of components found in the complexes are present in plants. However, plant microtubules are also nucleated in a γ-tubulin-dependent but γ-TuRC-independent manner. There is growing evidence that γ-tubulin is a microtubule nucleator without being complexed in γ-TuRC. Fibrillar arrays of γ-tubulin were demonstrated in plant and animal cells and the ability of γ-tubulin to assemble into linear oligomers/polymers was confirmed in vitro for both native and recombinant γ-tubulin. The functions of γ-tubulin as a template for microtubule nucleation or in promoting spontaneous nucleation is outlined. Higher plants represent an excellent model for studies on the role of γ-tubulin in nucleation due to their acentrosomal nature and high abundancy and conservation of γ-tubulin including its intrinsic ability to assemble filaments. The defining scaffolding or sequestration functions of plant γ-tubulin in microtubule organization or in nuclear processes will help our understanding of its cellular roles in eukaryotes.
Institute of Microbiology of the Czech Academy of Sciences Vídeňská1083 142 20 Prague Czech Republic
Zobrazit více v PubMed
Brown R.C., Lemmon B.E., Horio T. Gamma-tubulin localization changes from discrete polar organizers to anastral spindles and phragmoplasts in mitosis of Marchantia polymorpha L. Protoplasma. 2004;224:187–193. doi: 10.1007/s00709-004-0061-7. PubMed DOI
Stearns T., Evans L., Kirschner M. Gamma-tubulin is a highly conserved component of the centrosome. Cell. 1991;65:825–836. doi: 10.1016/0092-8674(91)90390-K. PubMed DOI
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 Mol. Cell Res. 2018;1865:734–748. doi: 10.1016/j.bbamcr.2018.02.009. PubMed DOI
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
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
Liu P., Wurtz M., Zupa E., Pfeffer S., Schiebel E. Microtubule nucleation: The waltz between gamma-tubulin ring complex and associated proteins. Curr. Opin Cell Biol. 2021;68:124–131. doi: 10.1016/j.ceb.2020.10.004. PubMed DOI
Oakley B.R., Oakley C.E., Yoon Y., Jung M.K. Gamma-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell. 1990;61:1289–1301. doi: 10.1016/0092-8674(90)90693-9. PubMed DOI
Liu B., Marc J., Joshi H.C., Palevitz B.A. A gamma-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. J. Cell Sci. 1993;104:1217–1228. PubMed
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
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
Seltzer V., Janski N., Canaday J., Herzog E., Erhardt M., Evrard J.L., Schmit A.C. Arabidopsis GCP2 and GCP3 are part of a soluble gamma-tubulin complex and have nuclear envelope targeting domains. Plant J. 2007;52:322–331. doi: 10.1111/j.1365-313X.2007.03240.x. PubMed DOI
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
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
Espigat-Georger A., Dyachuk V., Chemin C., Emorine L., Merdes A. Nuclear alignment in myotubes requiRes. centrosome proteins recruited by nesprin-1. J. Cell Sci. 2016;129:4227–4237. doi: 10.1242/jcs.191767. PubMed DOI
Mishra R.K., Chakraborty P., Arnaoutov A., Fontoura B.M., 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
Rivero S., Cardenas J., Bornens M., Rios R.M. Microtubule nucleation at the cis-side of the Golgi apparatus requiRes. AKAP450 and GM130. Embo. J. 2009;28:1016–1028. doi: 10.1038/emboj.2009.47. 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
Sanchez A.D., Feldman J.L. Microtubule-organizing centers: From the centrosome to non-centrosomal sites. Curr. Opin Cell Biol. 2017;44:93–101. doi: 10.1016/j.ceb.2016.09.003. PubMed DOI PMC
Tran P.T., Marsh L., Doye V., Inoue S., Chang F. A mechanism for nuclear positioning in fission yeast based on microtubule pushing. J. Cell Biol. 2001;153:397–411. doi: 10.1083/jcb.153.2.397. PubMed DOI PMC
Paz J., Luders J. Microtubule-Organizing Centers: Towards a Minimal Parts List. Trends Cell Biol. 2018;28:176–187. doi: 10.1016/j.tcb.2017.10.005. PubMed DOI
Lee Y.-R.J., Liu B. Microtubule nucleation for the assembly of acentrosomal microtubule arrays in plant cells. New Phytol. 2019;222:1705–1718. doi: 10.1111/nph.15705. PubMed DOI
Oegema K., Wiese C., Martin O.C., Milligan R.A., Iwamatsu A., Mitchison T.J., Zheng Y.X. Characterization of two related Drosophila gamma-tubulin complexes that differ in their ability to nucleate microtubdes. J. Cell Biol. 1999;144:721–733. doi: 10.1083/jcb.144.4.721. PubMed DOI PMC
Zheng Y., Wong M.L., Alberts B., Mitchison T. Nucleation of microtubule assembly by a gamma-tubulin-containing ring complex. Nature. 1995;378:578–583. doi: 10.1038/378578a0. 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
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
Zhang J., Megraw T.L. Proper recruitment of gamma-tubulin and D-TACC/Msps to embryonic Drosophila centrosomes requiRes. Centrosomin Motif 1. Mol. Biol. Cell. 2007;18:4037–4049. doi: 10.1091/mbc.e07-05-0474. PubMed DOI PMC
Leong S.L., Lynch E.M., Zou J., Tay Y.D., Borek W.E., Tuijtel M.W., Rappsilber J., Sawin K.E. Reconstitution of Microtubule Nucleation In Vitro Reveals Novel Roles for Mzt1. Curr. Biol. 2019;29:2199–2207. doi: 10.1016/j.cub.2019.05.058. PubMed DOI PMC
Lin T.C., Neuner A., Schlosser Y.T., Scharf A.N., Weber L., Schiebel E. Cell-cycle dependent phosphorylation of yeast pericentrin regulates gamma-TuSC-mediated microtubule nucleation. eLife. 2014;3:e02208. doi: 10.7554/eLife.02208. PubMed DOI PMC
Liu P., Zupa E., Neuner A., Bohler A., Loerke J., Flemming D., Ruppert T., Rudack T., Peter C., Spahn C., et al. Insights into the assembly and activation of the microtubule nucleator gamma-TuRC. Nature. 2020;578:467–471. doi: 10.1038/s41586-019-1896-6. PubMed DOI
Consolati T., Locke J., Roostalu J., Chen Z.A., Gannon J., Asthana J., Lim W.M., Martino F., Cvetkovic M.A., Rappsilber J., et al. Microtubule Nucleation Properties of Single Human gammaTuRCs Explained by Their Cryo-EM Structure. Dev. Cell. 2020;53:603–617. doi: 10.1016/j.devcel.2020.04.019. PubMed DOI PMC
Wieczorek M., Urnavicius L., Ti S.C., Molloy K.R., Chait B.T., Kapoor T.M. Asymmetric Molecular Architecture of the Human gamma-Tubulin Ring Complex. Cell. 2020;180:165–175. doi: 10.1016/j.cell.2019.12.007. PubMed DOI PMC
Wieczorek M., Ti S.C., Urnavicius L., Molloy K.R., Aher A., Chait B.T., Kapoor T.M. Biochemical reconstitutions reveal principles of human gamma-TuRC assembly and function. J. Cell Biol. 2021;220 doi: 10.1083/jcb.202009146. PubMed DOI PMC
Thawani A., Rale M.J., Coudray N., Bhabha G., Stone H.A., Shaevitz J.W., Petry S. The transition state and regulation of gamma-TuRC-mediated microtubule nucleation revealed by single molecule microscopy. eLife. 2020;9:e54253. doi: 10.7554/eLife.54253. PubMed DOI PMC
Zimmermann F., Serna M., Ezquerra A., Fernandez-Leiro R., Llorca O., Luders J. Assembly of the asymmetric human gamma-tubulin ring complex by RUVBL1-RUVBL2 AAA ATPase. Sci. Adv. 2020;6 doi: 10.1126/sciadv.abe0894. PubMed DOI PMC
Nakamura M., Ehrhardt D.W., Hashimoto T. Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 2010;12:1064–1070. doi: 10.1038/ncb2110. PubMed DOI
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. 2012;71:216–225. doi: 10.1111/j.1365-313X.2012.04988.x. PubMed DOI
Kong Z., Hotta T., Lee Y.-R.J., 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., Hashimoto T. A mutation in the Arabidopsis gamma-tubulin-containing complex causes helical growth and abnormal microtubule branching. J. Cell Sci. 2009;122:2208–2217. doi: 10.1242/jcs.044131. PubMed DOI
Zeng C.J., Lee Y.R., Liu B. The WD40 repeat protein NEDD1 functions in microtubule organization during cell division in Arabidopsis thaliana. Plant Cell. 2009;21:1129–1140. doi: 10.1105/tpc.109.065953. PubMed DOI PMC
Janski N., Masoud K., Batzenschlager M., Herzog E., Evrard J.L., Houlne G., Bourge M., Chaboute M.E., Schmit A.C. The GCP3-interacting proteins GIP1 and GIP2 are required for gamma-tubulin complex protein localization, spindle integrity, and chromosomal stability. Plant Cell. 2012;24:1171–1187. doi: 10.1105/tpc.111.094904. PubMed DOI PMC
Cota R.R., Teixido-Travesa N., Ezquerra A., Eibes S., Lacasa C., Roig J., Luders J. MZT1 regulates microtubule nucleation by linking gammaTuRC assembly to adapter-mediated targeting and activation. J. Cell Sci. 2017;130:406–419. doi: 10.1242/jcs.195321. PubMed DOI
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
Hannak E., Oegema K., Kirkham M., Gonczy P., Habermann B., Hyman A.A. The kinetically dominant assembly pathway for centrosomal asters in Caenorhabditis elegans is gamma-tubulin dependent. J. Cell Biol. 2002;157:591–602. doi: 10.1083/jcb.200202047. PubMed DOI PMC
Rogers G.C., Rusan N.M., Peifer M., Rogers S.L. A multicomponent assembly pathway contributes to the formation of acentrosomal microtubule arrays in interphase Drosophila cells. Mol. Biol. Cell. 2008;19:3163–3178. doi: 10.1091/mbc.e07-10-1069. PubMed DOI PMC
Zheng Y., Buchwalter R.A., Zheng C., Wight E.M., Chen J.V., Megraw T.L. A perinuclear microtubule-organizing centre controls nuclear positioning and basement membrane secretion. Nat. Cell Biol. 2020;22:297–309. doi: 10.1038/s41556-020-0470-7. PubMed DOI PMC
Basnet N., Nedozralova H., Crevenna A.H., Bodakuntla S., Schlichthaerle T., Taschner M., Cardone G., Janke C., Jungmann R., Magiera M.M., et al. Direct induction of microtubule branching by microtubule nucleation factor SSNA1. Nat. Cell Biol. 2018;20:1172–1180. doi: 10.1038/s41556-018-0199-8. PubMed DOI PMC
Llanos R., Chevrier V., Ronjat M., Meurer-Grob P., Martinez P., Frank R., Bornens M., Wade R.H., Wehland J., Job D. Tubulin binding sites on gamma-tubulin: Identification and molecular characterization. Biochemistry. 1999;38:15712–15720. doi: 10.1021/bi990895w. 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., LajoieMazenc I., Julian M., RaynaudMessina B., Wright M. Protein complexes containing gamma-tubulin are present in mammalian brain microtubule protein preparations. Cell Motil. Cytoskelet. 1997;36:179–189. doi: 10.1002/(SICI)1097-0169(1997)36:2<179::AID-CM7>3.0.CO;2-4. 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. Biochim. Biophys. Acta Proteins Proteom. 2018;1866:519–526. doi: 10.1016/j.bbapap.2018.01.007. 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
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
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
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
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
King B.R., Moritz M., Kim H., Agard D.A., Asbury C.L., Davis T.N. XMAP215 and gamma-tubulin additively promote microtubule nucleation in purified solutions. Mol. Biol. Cell. 2020;31:2187–2194. doi: 10.1091/mbc.E20-02-0160. PubMed DOI PMC
Miao H., Guo R., Chen J., Wang Q., Lee Y.J., Liu B. The gamma-tubulin complex protein GCP6 is crucial for spindle morphogenesis but not essential for microtubule reorganization in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2019 doi: 10.1073/pnas.1912240116. PubMed DOI PMC
Beck M., Schmidt A., Malmstroem J., Claassen M., Ori A., Szymborska A., Herzog F., Rinner O., Ellenberg J., Aebersold R. The quantitative proteome of a human cell line. Mol. Syst. Biol. 2011;7:549. doi: 10.1038/msb.2011.82. PubMed DOI PMC
Voter W.A., Erickson H.P. The kinetics of microtubule assembly. Evidence for a two-stage nucleation mechanism. J. Biol. Chem. 1984;259:10430–10438. doi: 10.1016/S0021-9258(18)90982-8. PubMed DOI
Mozziconacci J., Sandblad L., Wachsmuth M., Brunner D., Karsenti E. Tubulin dimers oligomerize before their incorporation into microtubules. PLoS ONE. 2008;3:e3821. doi: 10.1371/journal.pone.0003821. PubMed DOI PMC
Rice L.M., Moritz M., Agard D.A. Microtubules form by progressively faster tubulin accretion, not by nucleation-elongation. bioRxiv. 2020:545236. doi: 10.1101/545236. 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
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
Roostalu J., Cade N.I., Surrey T. Complementary activities of TPX2 and chTOG constitute an efficient importin-regulated microtubule nucleation module. Nat. Cell Biol. 2015;17:1422–1434. doi: 10.1038/ncb3241. PubMed DOI PMC
Gruss O.J., Wittmann M., Yokoyama H., Pepperkok R., Kufer T., Sillje H., Karsenti E., Mattaj I.W., Vernos I. Chromosome-induced microtubule assembly mediated by TPX2 is required for spindle formation in HeLa cells. Nat. Cell Biol. 2002;4:871–879. doi: 10.1038/ncb870. PubMed DOI
Petrovska B., Cenklova V., Pochylova Z., Kourova H., Doskocilova A., Plihal O., Binarova L., Binarova P. Plant Aurora kinases play a role in maintenance of primary meristems and control of endoreduplication. New Phytol. 2012;193:590–604. doi: 10.1111/j.1469-8137.2011.03989.x. PubMed DOI
Oakley B.R., Paolillo V., Zheng Y. gamma-Tubulin complexes in microtubule nucleation and beyond. Mol. Biol. Cell. 2015;26:2957–2962. doi: 10.1091/mbc.E14-11-1514. PubMed DOI PMC
Corvaisier M., Alvarado-Kristensson M. Non-Canonical Functions of the Gamma-Tubulin Meshwork in the Regulation of the Nuclear Architecture. Cancers. 2020;12:3102. doi: 10.3390/cancers12113102. PubMed DOI PMC
Chumova J., Kourova H., Trogelova L., Halada P., Binarova P. Microtubular and Nuclear Functions of gamma-Tubulin: Are They LINCed? Cells. 2019;12:259. doi: 10.3390/cells8030259. PubMed DOI PMC
Kallai B.M., Kourova H., Chumova J., Papdi C., Trogelova L., Kofronova O., Hozak P., Filimonenko V., Meszaros T., Magyar Z., et al. gamma-Tubulin interacts with E2F transcription factors to regulate proliferation and endocycling in Arabidopsis. J. Exp. Bot. 2020;71:1265–1277. doi: 10.1093/jxb/erz498. PubMed DOI
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
Binarova P., Dolezel J., Draber P., Heberle-Bors E., Strnad M., Bogre L. Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant J. 1998;16:697–707. doi: 10.1046/j.1365-313x.1998.00340.x. PubMed DOI
Kohoutova L., Kourova H., Nagy S.K., Volc J., Halada P., Meszaros T., Meskiene I., Boegre L., Binarova P. The Arabidopsis mitogen-activated protein kinase 6 is associated with -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
Lindstrom L., Alvarado-Kristensson M. Characterization of gamma-tubulin filaments in mammalian cells. Biochim. Et Biophys. Acta Mol. Cell Res. 2018;1865:158–171. doi: 10.1016/j.bbamcr.2017.10.008. PubMed DOI
Chiba Y., Takei S., Kawamura N., Kawaguchi Y., Sasaki K., Hasegawa-Ishii S., Furukawa A., Hosokawa M., Shimada A. Immunohistochemical localization of aggresomal proteins in glial cytoplasmic inclusions in multiple system atrophy. Neuropathol. Appl. Neurobiol. 2012;38:559–571. doi: 10.1111/j.1365-2990.2011.01229.x. PubMed DOI
Yam A.Y., Xia Y., Lin H.-T.J., Burlingame A., Gerstein M., Frydman J. Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat. Struct. Mol. Biol. 2008;15:1255–1262. doi: 10.1038/nsmb.1515. PubMed DOI PMC
King M.R., Petry S. Phase separation of TPX2 enhances and spatially coordinates microtubule nucleation. Nat. Commun. 2020;11:270. doi: 10.1038/s41467-019-14087-0. 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
So C., Seres K.B., Steyer A.M., Monnich E., Clift D., Pejkovska A., Mobius W., Schuh M. A liquid-like spindle domain promotes acentrosomal spindle assembly in mammalian oocytes. Science. 2019;364 doi: 10.1126/science.aat9557. 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
Oshidari R., Strecker J., Chung D.K.C., Abraham K.J., Chan J.N.Y., Damaren C.J., Mekhail K. Nuclear microtubule filaments mediate non-linear directional motion of chromatin and promote DNA repair. Nat. Commun. 2018;9:2567. doi: 10.1038/s41467-018-05009-7. PubMed DOI PMC
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
γ-Tubulin in microtubule nucleation and beyond