Abstract
The microtubule cytoskeleton is critically important for spatio-temporal organization of eukaryotic cells. The nucleation of new microtubules is typically restricted to microtubule organizing centers (MTOCs) and requires γ-tubulin that assembles into multisubunit complexes of various sizes. γ-Tubulin ring complexes (TuRCs) are efficient microtubule nucleators and are associated with large number of targeting, activating and modulating proteins. γ-Tubulin-dependent nucleation of microtubules occurs both from canonical MTOCs, such as spindle pole bodies and centrosomes, and additional sites such as Golgi apparatus, nuclear envelope, plasma membrane-associated sites, chromatin and surface of pre-existing microtubules. Despite many advances in structure of γ-tubulin complexes and characterization of γTuRC interacting factors, regulatory mechanisms of microtubule nucleation are not fully understood. Here, we review recent work on the factors and regulatory mechanisms that are involved in centrosomal and non-centrosomal microtubule nucleation.
Similar content being viewed by others
Abbreviations
- AKAP450:
-
A-kinase anchor protein 450
- Cdk1:
-
Cyclin-dependent kinase 1
- CDK5RAP2:
-
Cyclin-dependent kinase 5 regulatory subunit-associated protein 2
- CLASP:
-
Cytoplasmic linker associated protein
- CM1:
-
Centrosomin (Cnn) motif 1
- EBs:
-
End-binding proteins
- γTuRC:
-
γ-Tubulin ring complex
- γTuSC:
-
γ-Tubulin small complex
- GCPs:
-
γ-Tubulin complex proteins
- GIPs:
-
γ-Tubulin complex protein 3-interacting proteins
- GM130:
-
Golgin subfamily A member 2 protein
- GRIPs:
-
γ-Tubulin ring proteins
- Mozart:
-
Mitotic spindle-organizing protein
- MTOC:
-
Microtubule-organizing center
- NEDD1:
-
Neural precursor cell expressed, developmentally down-regulated protein 1
- NME7:
-
Nucleoside-diphosphate kinase 7
- PCM:
-
Pericentriolar material
- Plk1:
-
Polo-like kinase 1
- Ran:
-
Ras-related nuclear protein
- SAFs:
-
Spindle assembly factors
- SPB:
-
Spindle pole body
- +TIPs:
-
Microtubule plus-end tracking proteins
- TPX2:
-
Targeting protein for Xklp2
References
Akhmanova A, Steinmetz MO (2015) Control of microtubule organization and dynamics: two ends in the limelight. Nat Rev Mol Cell Biol 16:711–726
Ambrose C, Wasteneys GO (2011) Cell edges accumulate gamma tubulin complex components and nucleate microtubules following cytokinesis in Arabidopsis thaliana. PLoS One 6:e27423
Ambrose C, Wasteneys GO (2014) Microtubule initiation from the nuclear surface controls cortical microtubule growth polarity and orientation in Arabidopsis thaliana. Plant Cell Physiol 55:1636–1645
Bartolini F, Gundersen GG (2006) Generation of noncentrosomal microtubule arrays. J Cell Sci 119:4155–4163
Batzenschlager M, Masoud K, Janski N, Houlné G, Herzog E, Evrard JL, Baumberger N, Erhardt M, Nominé Y, Kieffer B, Schmit AC, Chabouté ME (2013) The GIP γ-tubulin complex-associated proteins are involved in nuclear architecture in Arabidopsis thaliana. Front Plant Sci 4:480
Bellouze S, Schäfer MK, Buttigieg D, Baillat G, Rabouille C, Haase G (2014) Golgi fragmentation in pmn mice is due to a defective ARF1/TBCE cross-talk that coordinates COPI vesicle formation and tubulin polymerization. Hum Mol Genet 23:5961–5975
Binarová P, Doležel J, Dráber P, Heberle-Bors E, Strnad M, Bögre L (1998) Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant J 16:697–707
Binarová P, Cenklová V, Hause B, Kubátová E, Lysák M, Doležel J, Bögre L, Dráber P (2000) Nuclear γ-tubulin during acentriolar plant mitosis. Plant Cell 12:433–442
Bugnard E, Zaal KJ, Ralston E (2005) Reorganization of microtubule nucleation during muscle differentiation. Cell Motil Cytoskeleton 60:1–13
Carazo-Salas RE, Guarguaglini G, Gruss OJ, Segref A, Karsenti E, Mattaj IW (1999) Generation of GTP-bound ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400:178–181
Casanova CM, Rybina S, Yokoyama H, Karsenti E, Mattaj IW (2008) Hepatoma up-regulated protein is required for chromatin-induced microtubule assembly independently of TPX2. Mol Biol Cell 19:4900–4908
Černohorská M, Sulimenko V, Hájková Z, Sulimenko T, Sládková V, Vinopal S, Dráberová E, Dráber P (2016) GIT1/βPIX signaling proteins and PAK1 kinase regulate microtubule nucleation. BBA Mol Cell Res 1863:1282–1297
Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, Poüs C (2001) The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12:2047–2060
Choi YK, Liu P, Sze SK, Dai C, Qi RZ (2010) CDK5RAP2 stimulates microtubule nucleation by the γ-tubulin ring complex. J Cell Biol 191:1089–1095
Delgehyr N, Sillibourne J, Bornens M (2005) Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J Cell Sci 118:1565–1575
Dhani DK, Goult BT, George GM, Rogerson DT, Bitton DA, Miller CJ, Schwabe JW, Tanaka K (2013) Mzt1/Tam4, a fission yeast MOZART1 homologue, is an essential component of the γ-tubulin complex and directly interacts with GCP3(Alp6). Mol Biol Cell 24:3337–3349
Dráber P, Dráberová E (2012) Microtubules. In: Kavallaris M (ed) Cytoskeleton and human disease. Humana Press, New York, pp 29–55
Dráberová L, Dráberová E, Surviladze Z, Dráber P, Dráber P (1999) Protein tyrosine kinase p53/p56(lyn) forms complexes with γ-tubulin in rat basophilic leukemia cells. Int Immunol 11:1829–1839
Dráberová E, D'Agostino L, Caracciolo V, Sládková V, Sulimenko T, Sulimenko V, Sobol M, Maounis NF, Tzelepis E, Mahera E, Křen L, Legido A, Giordano A, Mörk S, Hozák P, Dráber P, Katsetos CD (2015) Overexpression and nucleolar localization of γ-tubulin small complex proteins GCP2 and GCP3 in glioblastoma. J Neuropathol Exp Neurol 74:723–742
Dryková D, Cenklová V, Sulimenko V, Volc J, Dráber P, Binarová P (2003) Plant gamma-tubulin interacts with alphabeta-tubulin dimers and forms membrane-associated complexes. Plant Cell 15:465–480
Dyachuk V, Bierkamp C, Merdes A (2016) Non-centrosomal microtubule organization in differentiated cells. In: Lüders J (ed) The microtubule cytoskeleton. Springer-Verlag, Wien, pp 27–42
Edzuka T, Yamada L, Kanamaru K, Sawada H, Goshima G (2014) Identification of the augmin complex in the filamentous fungus Aspergillus nidulans. PLoS One 9:e101471
Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, Gleeson P, Galjart N, Maia AR, McLeod IX, Yates JR 3rd, Maiato H, Khodjakov A, Akhmanova A, Kaverina I (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 12:917–930
Erhardt M, Stoppin-Mellet V, Campagne S, Canaday J, Mutterer J, Fabian T, Sauter M, Muller T, Peter C, Lambert AM, Schmit AC (2002) The plant Spc98p homologue colocalizes with γ-tubulin at microtubule nucleation sites and is required for microtubule nucleation. J Cell Sci 115:2423–2431
Fant X, Gnadt N, Haren L, Merdes A (2009) Stability of the small γ-tubulin complex requires HCA66, a protein of the centrosome and the nucleolus. J Cell Sci 122:1134–1144
Farache D, Jauneau A, Chemin C, Chartrain M, Rémy MH, Merdes A, Haren L (2016) Functional analysis of γ-tubulin complex proteins indicates specific lateral association via their N-terminal domains. J Biol Chem 291:23112–23125
Findeisen P, Mühlhausen S, Dempewolf S, Hertzog J, Zietlow A, Carlomagno T, Kollmar M (2014) Six subgroups and extensive recent duplications characterize the evolution of the eukaryotic tubulin protein family. Genome Biol Evol 6:2274–2288
Fogeron ML, Müller H, Schade S, Dreher F, Lehmann V, Kühnel A, Scholz AK, Kashofer K, Zerck A, Fauler B, Lurz R, Herwig R, Zatloukal K, Lehrach H, Gobom J, Nordhoff E, Lange BM (2013) LGALS3BP regulates centriole biogenesis and centrosome hypertrophy in cancer cells. Nat Commun 4:1531
Fong CS, Sato M, Toda T (2010) Fission yeast Pcp1 links polo kinase-mediated mitotic entry to γ-tubulin-dependent spindle formation. EMBO J 29:120–130
Gaume X, Tassin AM, Ugrinova I, Mongelard F, Monier K, Bouvet P (2015) Centrosomal nucleolin is required for microtubule network organization. Cell Cycle 14:902–919
Gomez-Ferreria MA, Rath U, Buster DW, Chanda SK, Caldwell JS, Rines DR, Sharp DJ (2007) Human Cep192 is required for mitotic centrosome and spindle assembly. Curr Biol 17:1960–1966
Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD (2008) Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 181:421–429
Grimaldi AD, Maki T, Fitton BP, Roth D, Yampolsky D, Davidson MW, Svitkina T, Straube A, Hayashi I, Kaverina I (2014) CLASPs are required for proper microtubule localization of end-binding proteins. Dev Cell 30:343–352
Groen AC, Cameron LA, Coughlin M, Miyamoto DT, Mitchison TJ, Ohi R (2004) XRHAMM functions in ran-dependent microtubule nucleation and pole formation during anastral spindle assembly. Curr Biol 14:1801–1811
Guerin CM, Kramer SG (2009) RacGAP50C directs perinuclear Akhmanova A and Steinmetz MO (2015) Control of microtubule organization and dynamics: two ends in the limelight. Nat Rev Mol Cell Biol 16:711–726
Guillet V, Knibiehler M, Gregory-Pauron L, Remy MH, Chemin C, Raynaud-Messina B, Bon C, Kollman JM, Agard DA, Merdes A, Mourey L (2011) Crystal structure of γ-tubulin complex protein GCP4 provides insight into microtubule nucleation. Nat Struct Mol Biol 18:915–919
Gunawardane RN, Lizarraga SB, Wiese C, Wilde A, Zheng Y (2000) γ-Tubulin complexes and their role in microtubule nucleation. Curr Top Dev Biol 49:55–73
Hořejší B, Vinopal S, Sládková V, Dráberová E, Sulimenko V, Sulimenko T, Vosecká V, Philimonenko A, Hozák P, Katsetos CD, Dráber P (2012) Nuclear γ-tubulin associates with nucleoli and interacts with tumor suppressor protein C53. J Cell Physiol 227:367–382
Hotta T, Kong Z, Ho CM, Zeng CJ, Horio T, Fong S, Vuong T, Lee YR, Liu B (2012) Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 24:1494–1509
Hsia KC, Wilson-Kubalek EM, Dottore A, Hao Q, Tsai KL, Forth S, Shimamoto Y, Milligan RA, Kapoor TM (2014) Reconstitution of the augmin complex provides insights into its architecture and function. Nat Cell Biol 16:852–863
Inukai K, Funaki M, Nawano M, Katagiri H, Ogihara T, Anai M, Onishi Y, Sakoda H, Ono H, Fukushima Y, Kikuchi M, Oka Y, Asano T (2000) The N-terminal 34 residues of the 55 kDa regulatory subunits of phosphoinositide 3-kinase interact with tubulin. Biochem J 346(Pt 2):483–489
Janski N, Masoud K, Batzenschlager M, Herzog E, Evrard JL, Houlné G, Bourge M, Chabouté ME, Schmit AC (2012) The GCP3-interacting proteins GIP1 and GIP2 are required for γ-tubulin complex protein localization, spindle integrity, and chromosomal stability. Plant Cell 24:1171–1187
Jeffery JM, Grigoriev I, Poser I, van der Horst A, Hamilton N, Waterhouse N, Bleier J, Subramaniam VN, Maly IV, Akhmanova A, Khanna KK (2013) Centrobin regulates centrosome function in interphase cells by limiting pericentriolar matrix recruitment. Cell Cycle 12:899–906
Johmura Y, Soung NK, Park JE, Yu LR, Zhou M, Bang JK, Kim BY, Veenstra TD, Erikson RL, Lee KS (2011) Regulation of microtubule-based microtubule nucleation by mammalian polo-like kinase 1. Proc Natl Acad Sci U S A 108:11446–11451
Kalab P, Pralle A, Isacoff EY, Heald R, Weis K (2006) Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 440:697–701
Khodjakov A, Rieder CL (1999) The sudden recruitment of γ-tubulin to the centrosome at the onset of mitosis and its dynamic exchange throughout the cell cycle, do not require microtubules. J Cell Biol 146:585–596
Kilmartin JV, Goh PY (1996) Spc110p: assembly properties and role in the connection of nuclear microtubules to the yeast spindle pole body. EMBO J 15:4592–4602
Kinoshita K, Noetzel TL, Pelletier L, Mechtler K, Drechsel DN, Schwager A, Lee M, Raff JW, Hyman AA (2005) Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis. J Cell Biol 170:1047–1055
Kirik A, Ehrhardt DW, Kirik V (2012) TONNEAU2/FASS regulates the geometry of microtubule nucleation and cortical array organization in interphase Arabidopsis cells. Plant Cell 24:1158–1170
Knop M, Schiebel E (1997) Spc98p and Spc97p of the yeast γ-tubulin complex mediate binding to the spindle pole body via their interaction with Spc110p. EMBO J 16:6985–6995
Kollman JM, Zelter A, Muller EG, Fox B, Rice LM, Davis TN, Agard DA (2008) The structure of the γ-tubulin small complex: implications of its architecture and flexibility for microtubule nucleation. Mol Biol Cell 19:207–215
Kollman JM, Polka JK, Zelter A, Davis TN, Agard DA (2010) Microtubule nucleating γ-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466:879–882
Kollman JM, Merdes A, Mourey L, Agard DA (2011) Microtubule nucleation by γ-tubulin complexes. Nat Rev Mol Cell Biol 12:709–721
Kollman JM, Greenberg CH, Li S, Moritz M, Zelter A, Fong KK, Fernandez JJ, Sali A, Kilmartin J, Davis TN, Agard DA (2015) Ring closure activates yeast γ-TuRC for species-specific microtubule nucleation. Nat Struct Mol Biol 22:132–137
Lawo S, Hasegan M, Gupta GD, Pelletier L (2012) Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 14:1148–1158
Lin TC, Neuner A, Schlosser YT, Scharf AN, Weber L, Schiebel E (2014) Cell-cycle dependent phosphorylation of yeast pericentrin regulates γ-TuSC-mediated microtubule nucleation. Elife 3:e02208
Lin TC, Neuner A, Schiebel E (2015) Targeting of γ-tubulin complexes to microtubule organizing centers: conservation and divergence. Trends Cell Biol 25:296–307
Liu T, Tian J, Wang G, Yu Y, Wang C, Ma Y, Zhang X, Xia G, Liu B, Kong Z (2014) Augmin triggers microtubule-dependent microtubule nucleation in interphase plant cells. Curr Biol 24:2708–2713
Lüders J, Stearns T (2007) Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 8:161–167
Lüders J, Patel UK, Stearns T (2006) GCP-WD is a γ-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat Cell Biol 8:137–147
Ludueña RF, Banerjee A (2008) The isotypes of tubulin: distribution and functional significance. In: Fojo T (ed) The role of microtubules in cell biology, neurobiology and oncology. Humana Press, Totowa, pp 123–175
Lyon AS, Morin G, Moritz M, Yabut KC, Vojnar T, Zelter A, Muller E, Davis TN, Agard DA (2016) Higher-order oligomerization of Spc110p drives γ-tubulin ring complex assembly. Mol Biol Cell 27:2245–2258
Macurek L, Dráberová E, Richterová V, Sulimenko V, Sulimenko T, Dráberová L, Marková V, Dráber P (2008) Regulation of microtubule nucleation from membranes by complexes of membrane-bound γ-tubulin with Fyn kinase and phosphoinositide 3-kinase. Biochem J 416:421–430
Meunier S, Vernos I (2016) Acentrosomal microtubule assembly in mitosis: the where, when, and how. Trends Cell Biol 26:80–87
Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M (2010) The Nup107-160 complex and γ-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 12:164–169
Mogensen MM, Malik A, Piel M, Bouckson-Castaing V, Bornens M (2000) Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J Cell Sci 113(Pt 17):3013–3023
Moreno-Mateos MA, Espina AG, Torres B, Gámez del Estal MM, Romero-Franco A, Ríos RM, Pintor-Toro JA (2011) PTTG1/securin modulates microtubule nucleation and cell migration. Mol Biol Cell 22:4302–4311
Moritz M, Braunfeld MB, Guénebaut V, Heuser J, Agard DA (2000) Structure of the γ-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2:365–370
Murata T, Sonobe S, Baskin TI, Hyodo S, Hasezawa S, Nagata T, Horio T, Hasebe M (2005) Microtubule-dependent microtubule nucleation based on recruitment of γ-tubulin in higher plants. Nat Cell Biol 7:961–968
Muroyama A, Seldin L, Lechler T (2016) Divergent regulation of functionally distinct γ-tubulin complexes during differentiation. J Cell Biol 213:679–692
Nogales E, Wang HW (2006) Structural intermediates in microtubule assembly and disassembly: how and why? Curr Opin Cell Biol 18:179–184
Nováková M, Dráberová E, Schürmann W, Czihak G, Viklický V, Dráber P (1996) γ-tubulin redistribution in taxol-treated mitotic cells probed by monoclonal antibodies. Cell Motil Cytoskeleton 33:38–51
Oakley CE, Oakley BR (1989) Identification of γ-tubulin, a new member of the tubulin superfamily encoded by mipA gene of Aspergillus nidulans. Nature 338:662–664
Oakley BR, Paolillo V, Zheng Y (2015) γ-Tubulin complexes in microtubule nucleation and beyond. Mol Biol Cell 26:2957–2962
Oh SA, Jeon J, Park HJ, Grini PE, Twell D, Park SK (2016a) Analysis of gemini pollen 3 mutant suggests a broad function of AUGMIN in microtubule organization during sexual reproduction in Arabidopsis. Plant J 87:188–201
Oh D, Yu CH, Needleman DJ (2016b) Spatial organization of the Ran pathway by microtubules in mitosis. Proc Natl Acad Sci U S A 113:8729–8734
Oriolo AS, Wald FA, Canessa G, Salas PJ (2007) GCP6 binds to intermediate filaments: a novel function of keratins in the organization of microtubules in epithelial cells. Mol Biol Cell 18:781–794
Petry S, Vale RD (2015) Microtubule nucleation at the centrosome and beyond. Nat Cell Biol 17:1089–1093
Petry S, Groen AC, Ishihara K, Mitchison TJ, Vale RD (2013) Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2. Cell 152:768–777
Pinyol R, Scrofani J, Vernos I (2013) The role of NEDD1 phosphorylation by aurora a in chromosomal microtubule nucleation and spindle function. Curr Biol 23:143–149
Rivero S, Cardenas J, Bornens M, Rios RM (2009) Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 28:1016–1028
Roostalu J, Cade NI, Surrey T (2015) Complementary activities of TPX2 and chTOG constitute an efficient importin-regulated microtubule nucleation module. Nat Cell Biol 17:1422–1434
Roubin R, Acquaviva C, Chevrier V, Sedjaï F, Zyss D, Birnbaum D, Rosnet O (2013) Myomegalin is necessary for the formation of centrosomal and Golgi-derived microtubules. Biol Open 2:238–250
Samejima I, Miller VJ, Groocock LM, Sawin KE (2008) Two distinct regions of Mto1 are required for normal microtubule nucleation and efficient association with the γ-tubulin complex in vivo. J Cell Sci 121:3971–3980
Sánchez-Huertas C, Lüders J (2015) The augmin connection in the geometry of microtubule networks. Curr Biol 25:R294–R299
Sánchez-Huertas C, Freixo F, Viais R, Lacasa C, Soriano E, Lüders J (2016) Non-centrosomal nucleation mediated by augmin organizes microtubules in post-mitotic neurons and controls axonal microtubule polarity. Nat Commun 7:12187
Sanders AA, Kaverina I (2015) Nucleation and dynamics of Golgi-derived microtubules. Front Neurosci 9:431
Sawin KE, Tran PT (2006) Cytoplasmic microtubule organization in fission yeast. Yeast 23:1001–1014
Scrofani J, Sardon T, Meunier S, Vernos I (2015) Microtubule nucleation in mitosis by a RanGTP-dependent protein complex. Curr Biol 25:131–140
Seltzer V, Janski N, Canaday J, Herzog E, Erhardt M, Evrard JL, Schmit AC (2007) Arabidopsis GCP2 and GCP3 are part of a soluble γ-tubulin complex and have nuclear envelope targeting domains. Plant J 52:322–331
Singh P, Thomas GE, Gireesh KK, Manna TK (2014) TACC3 protein regulates microtubule nucleation by affecting γ-tubulin ring complexes. J Biol Chem 289:31719–31735
Soues S, Adams IR (1998) SPC72: a spindle pole component required for spindle orientation in the yeast Saccharomyces cerevisiae. J Cell Sci 111:2809–2818
Sulimenko V, Sulimenko T, Poznanovic S, Nechiporuk-Zloy V, Böhm KJ, Macurek L, Unger E, Dráber P (2002) Association of brain γ-tubulins with αβ-tubulin dimers. Biochem J 365:889–895
Sulimenko V, Dráberová E, Sulimenko T, Macurek L, Richterová V, Dráber P, Dráber P (2006) Regulation of microtubule formation in activated mast cells by complexes of γ-tubulin with Fyn and Syk kinases. J Immunol 176:7243–7253
Sulimenko V, Hájková Z, Černohorská M, Sulimenko T, Sládková V, Dráberová L, Vinopal S, Dráberová E, Dráber P (2015) Microtubule nucleation in mouse bone marrow-derived mast cells is regulated by the concerted action of GIT1/βPIX proteins and calcium. J Immunol 194:4099–4111
Takahashi M, Yamagiwa A, Nishimura T, Mukai H, Ono Y (2002) Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring γ-tubulin ring complex. Mol Biol Cell 13:3235–3245
Teixidó-Travesa N, Villén J, Lacasa C, Bertran MT, Archinti M, Gygi SP, Caelles C, Roig J, Lüders J (2010) The γ-TuRC revisited: a comparative analysis of interphase and mitotic human γ-TuRC redefines the set of core components and identifies the novel subunit GCP8. Mol Biol Cell 21:3963–3972
Teixidó-Travesa N, Roig J, Lüders J (2012) The where, when and how of microtubule nucleation - one ring to rule them all. J Cell Sci 125:4445–4456
Tsai MY, Zheng Y (2005) Aurora a kinase-coated beads function as microtubule-organizing centers and enhance RanGTP-induced spindle assembly. Curr Biol 15:2156–2163
Uehara R, Nozawa RS, Tomioka A, Petry S, Vale RD, Obuse C, Goshima G (2009) The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc Natl Acad Sci U S A 106:6998–7003
Uehara R, Kamasaki T, Hiruma S, Poser I, Yoda K, Yajima J, Gerlich DW, Goshima G (2016) Augmin shapes the anaphase spindle for efficient cytokinetic furrow ingression and abscission. Mol Biol Cell 27:812–827
Usui T, Maekawa H, Pereira G, Schiebel E (2003) The XMAP215 homologue Stu2 at yeast spindle pole bodies regulates microtubule dynamics and anchorage. EMBO J 22:4779–4793
Verhey KJ, Gaertig J (2007) The tubulin code. Cell Cycle 6:2152–2160
Vinopal S, Černohorská M, Sulimenko V, Sulimenko T, Vosecká V, Flemr M, Dráberová E, Dráber P (2012) γ-Tubulin 2 nucleates microtubules and is downregulated in mouse early embryogenesis. PLoS One 7:e29919
Wang Z, Wu T, Shi L, Zhang L, Zheng W, Qu JY, Niu R, Qi RZ (2010) Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J Biol Chem 285:22658–22665
Wang S, Wu D, Quintin S, Green RA, Cheerambathur DK, Ochoa SD, Desai A, Oegema K (2015) NOCA-1 functions with γ-tubulin and in parallel to Patronin to assemble non-centrosomal microtubule arrays in C. elegans. Elife 4:e08649
Wieczorek M, Bechstedt S, Chaaban S, Brouhard GJ (2015) Microtubule-associated proteins control the kinetics of microtubule nucleation. Nat Cell Biol 17:907–916
Yokoyama H, Koch B, Walczak R, Ciray-Duygu F, González-Sánchez JC, Devos DP, Mattaj IW, Gruss OJ (2014) The nucleoporin MEL-28 promotes RanGTP-dependent γ-tubulin recruitment and microtubule nucleation in mitotic spindle formation. Nat Commun 5:3270
Zhang X, Chen Q, Feng J, Hou J, Yang F, Liu J, Jiang Q, Zhang C (2009) Sequential phosphorylation of Nedd1 by Cdk1 and Plk1 is required for targeting of the γ-TuRC to the centrosome. J Cell Sci 122:2240–2251
Zhang T, Braun U, Leitges M (2016) PKD3 deficiency causes alterations in microtubule dynamics during the cell cycle. Cell Cycle 15:1844–1854
Zimmerman WC, Sillibourne J, Rosa J, Doxsey SJ (2004) Mitosis-specific anchoring of γ-tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol Biol Cell 15:3642–3657
Acknowledgements
We thank Dr. Eduarda Dráberová and Tetyana Sulimenko for help with figure preparation. This work was supported by the grant LD13015 for COST action (BM1007 Mast Cells and Basophils-Targets for Innovative Therapies) from the Ministry of Education Youth and Sport and by Institutional Research Support (RVO 68378050).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Reimer Stick
Rights and permissions
About this article
Cite this article
Sulimenko, V., Hájková, Z., Klebanovych, A. et al. Regulation of microtubule nucleation mediated by γ-tubulin complexes. Protoplasma 254, 1187–1199 (2017). https://doi.org/10.1007/s00709-016-1070-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-016-1070-z