Abstract
Centrosome serves as the primary site of microtubule organization in a majority of animal cells. These microtubules carry out several significant functions in the cell such as cell division, chromosome segregation, mechanical support and cellular transport. Proteins localized at the centrosome play extensive role in orchestrating the process of microtubule organization, growth and stabilization in space and time. Anomalies in centrosome number, structure and functioning disturb microtubule organization and lead to several human diseases. Advancements in proteomics and microscopy methods have been instrumental in identifying molecular mechanisms pertaining to the microtubule organizing function of centrosomes. This review focuses on the involvement of centrosome as a microtubule nucleating center of the cell. We present the major molecular mechanisms at the centrosome which affect microtubule nucleation and activation. Finally, we discuss human diseases associated with defective microtubule organization resulting from centrosome abnormalities.
Similar content being viewed by others
Abbreviations
- MTOC:
-
Microtubule Organizing Center
- MT:
-
Microtubule
- PCM:
-
Pericentriolar material
- γ-TuRC:
-
Gamma-tubulin ring complex
- γ-TuSC:
-
Gamma-tubulin small complex
- MAP:
-
Microtubule-associated protein
- GCP:
-
Gamma complex protein
References
Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426(6966):570–574. https://doi.org/10.1038/nature02166
Arquint C, Gabryjonczyk A-M, Nigg EA (2014) Centrosomes as signalling centres. Philos Trans R Soc B Biol Sci 369(1650):20130464. https://doi.org/10.1098/rstb.2013.0464
Bauer M, Cubizolles F, Schmidt A, Nigg EA (2016) Quantitative analysis of human centrosome architecture by targeted proteomics and fluorescence imaging. EMBO J 35(19):2152–2166. https://doi.org/10.15252/embj.201694462
Bernhard W, De Harven E (1956) Etude au microscope électronique de l’ultrastructure du centriole chez les vertébrés [Electron microscopic study of the ultrastructure of centrioles in vertebra]. Zeitschrift Fur Zellforschung Und Mikroskopische Anatomie (Vienna, Austria: 1948), 45(3):378–398.
Bettencourt-Dias M, Rodrigues-Martins A, Carpenter L, Riparbelli M, Lehmann L, Gatt MK, Carmo N, Balloux F, Callaini G, Glover DM (2005) SAK/PLK4 Is required for centriole duplication and flagella development. Curr Biol 15(24):2199–2207. https://doi.org/10.1016/j.cub.2005.11.042
Burton PR, Hinkley RE, Pierson GB (1975) Tannic acid-stained microtubules with 12, 13, and 15 protofilaments. J Cell Biol 65(1):227–233. https://doi.org/10.1083/jcb.65.1.227
Casenghi M, Meraldi P, Weinhart U, Duncan PI, Körner R, Nigg EA (2003) Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev Cell 5(1):113–125. https://doi.org/10.1016/s1534-5807(03)00193-x
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. Biochim Biophys Acta (BBA) Mol Cell Res 1863(6, Part A):1282–1297. https://doi.org/10.1016/j.bbamcr.2016.03.016
Chan JY (2011) A clinical overview of centrosome amplification in human cancers. Int J Biol Sci 7(8):1122–1144
Chang C-W, Hsu W-B, Tsai J-J, Tang C-JC, Tang TK (2016) CEP295 interacts with microtubules and is required for centriole elongation. J Cell Sci 129(13):2501–2513. https://doi.org/10.1242/jcs.186338
Chou E-J, Hung L-Y, Tang C-JC, Hsu W-B, Wu H-Y, Liao P-C, Tang TK (2016) Phosphorylation of CPAP by Aurora-A maintains spindle pole integrity during mitosis. Cell Rep 14(12):2975–2987. https://doi.org/10.1016/j.celrep.2016.02.085
Cota RR, Teixidó-Travesa N, Ezquerra A, Eibes S, Lacasa C, Roig J, Lüders J (2017) MZT1 regulates microtubule nucleation by linking γTuRC assembly to adapter-mediated targeting and activation. J Cell Sci 130(2):406–419. https://doi.org/10.1242/jcs.195321
Dammermann A, Desai A, Oegema K (2003) The minus end in sight. Curr Biol CB 13(15):R614-624. https://doi.org/10.1016/s0960-9822(03)00530-x
Dammermann A, Merdes A (2002) Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159(2):255–266. https://doi.org/10.1083/jcb.200204023
Davis C, Gull K (1983) Protofilament number in microtubules in cells of two parasitic nematodes. J Parasitol 69(6):1094–1099
Delattre M, Canard C, Gönczy P (2006) Sequential protein recruitment in C. elegans centriole formation. Curr Biol CB 16(18):1844–1849. https://doi.org/https://doi.org/10.1016/j.cub.2006.07.059
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(Pt 8):1565–1575. https://doi.org/10.1242/jcs.02302
Dobbelaere J, Josué F, Suijkerbuijk S, Baum B, Tapon N, Raff J (2008) A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol. https://doi.org/10.1371/journal.pbio.0060224
Erez A, Perelman M, Hewitt SM, Cojacaru G, Goldberg I, Shahar I, Yaron P, Muler I, Campaner S, Amariglio N, Rechavi G, Kirsch IR, Krupsky M, Kaminski N, Izraeli S (2004) Sil overexpression in lung cancer characterizes tumors with increased mitotic activity. Oncogene 23(31):5371–5377. https://doi.org/10.1038/sj.onc.1207685
Farache D, Emorine L, Haren L, Merdes A (2018) Assembly and regulation of γ-tubulin complexes. Open Biol. https://doi.org/10.1098/rsob.170266
Farache D, Jauneau A, Chemin C, Chartrain M, Rémy M-H, 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(44):23112–23125. https://doi.org/10.1074/jbc.M116.744862
Fırat-Karalar EN, Stearns T (2014) The centriole duplication cycle. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2013.0460
Fogeron M-L, Müller H, Schade S, Dreher F, Lehmann V, Kühnel A, Scholz A-K, Kashofer K, Zerck A, Fauler B, Lurz R, Herwig R, Zatloukal K, Lehrach H, Gobom J, Nordhoff E, Lange BMH (2013) LGALS3BP regulates centriole biogenesis and centrosome hypertrophy in cancer cells. Nat Commun 4(1):1531. https://doi.org/10.1038/ncomms2517
Fong K-W, Choi Y-K, Rattner JB, Qi RZ (2007) CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the γ-tubulin ring complex. Mol Biol Cell 19(1):115–125. https://doi.org/10.1091/mbc.e07-04-0371
Fu J, Glover DM (2012) Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2(8):120104. https://doi.org/10.1098/rsob.120104
Gergely F, Draviam VM, Raff JW (2003) The ch-TOG/XMAP215 protein is essential for spindle pole organization in human somatic cells. Genes Dev 17(3):336–341. https://doi.org/10.1101/gad.245603
Gomez-Ferreria MA, Bashkurov M, Helbig AO, Larsen B, Pawson T, Gingras A-C, Pelletier L (2012) Novel NEDD1 phosphorylation sites regulate γ-tubulin binding and mitotic spindle assembly. J Cell Sci 125(Pt 16):3745–3751. https://doi.org/10.1242/jcs.105130
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(22):1960–1966. https://doi.org/10.1016/j.cub.2007.10.019
Gupta GD, Coyaud É, Gonçalves J, Mojarad BA, Liu Y, Wu Q, Gheiratmand L, Comartin D, Tkach JM, Cheung SWT, Bashkurov M, Hasegan M, Knight JD, Lin Z-Y, Schueler M, Hildebrandt F, Moffat J, Gingras A-C, Raught B, Pelletier L (2015) A dynamic protein interaction landscape of the human centrosome-cilium interface. Cell 163(6):1484–1499. https://doi.org/10.1016/j.cell.2015.10.065
Haren L, Remy M-H, Bazin I, Callebaut I, Wright M, Merdes A (2006) NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172(4):505–515. https://doi.org/10.1083/jcb.200510028
Haren L, Stearns T, Lüders J (2009) Plk1-dependent recruitment of γ-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS ONE 4(6):e5976. https://doi.org/10.1371/journal.pone.0005976
van Haren J, Wittmann T (2019) Microtubule plus end dynamics − do we know how microtubules grow? BioEssays 41(3):1800194. https://doi.org/10.1002/bies.201800194
Hiraki M, Nakazawa Y, Kamiya R, Hirono M (2007) Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr Biol CB 17(20):1778–1783. https://doi.org/10.1016/j.cub.2007.09.021
Hung H-F, Hehnly H, Doxsey S (2016) The mother centriole appendage protein cenexin modulates lumen formation through spindle orientation. Curr Biol CB 26(6):793–801. https://doi.org/10.1016/j.cub.2016.01.025
Hung LY, Tang CJ, Tang TK (2000) Protein 4.1 R-135 interacts with a novel centrosomal protein (CPAP) which is associated with the gamma-tubulin complex. Mol Cell Biol 20(20):7813–7825. https://doi.org/https://doi.org/10.1128/mcb.20.20.7813-7825.2000
Hung L-Y, Chen H-L, Chang C-W, Li B-R, Tang TK (2004) Identification of a novel microtubule-destabilizing motif in CPAP that binds to tubulin heterodimers and inhibits microtubule assembly. Mol Biol Cell 15(6):2697–2706. https://doi.org/10.1091/mbc.E04-02-0121
Ikeda T (2010) NDP Kinase 7 is a conserved microtubule-binding protein preferentially expressed in ciliated cells. Cell Struct Funct 35:23–30. https://doi.org/10.1247/csf.09016
Jaiswal S, Singh P (2020) Centrosome dysfunction in human diseases. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2020.04.019
Jakobsen L, Vanselow K, Skogs M, Toyoda Y, Lundberg E, Poser I, Falkenby LG, Bennetzen M, Westendorf J, Nigg EA, Uhlen M, Hyman AA, Andersen JS (2011) Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J 30(8):1520–1535. https://doi.org/10.1038/emboj.2011.63
Jayaraman D, Bae B-I, Walsh CA (2018) The genetics of primary microcephaly. Annu Rev Genom Hum Genet 19(1):177–200. https://doi.org/10.1146/annurev-genom-083117-021441
Jeffery JM, Urquhart AJ, Subramaniam VN, Parton RG, Khanna KK (2010) Centrobin regulates the assembly of functional mitotic spindles. Oncogene 29(18):2649–2658. https://doi.org/10.1038/onc.2010.37
Jerka-Dziadosz M, Gogendeau D, Klotz C, Cohen J, Beisson J, Koll F (2010) Basal body duplication in paramecium: the key role of Bld10 in assembly and stability of the cartwheel. Cytoskeleton (Hoboken, N.J.), 67(3):161–171. https://doi.org/10.1002/cm.20433
Joukov V, Walter J, De Nicolo A (2014) The Cep192-organized Aurora A-Plk1 cascade is essential for centrosome cycle and bipolar spindle assembly. Mol Cell 55(4):578–591. https://doi.org/10.1016/j.molcel.2014.06.016
Kalt A, Schliwa M (1993) Molecular components of the centrosome. Trends Cell Biol 3(4):118–128. https://doi.org/10.1016/0962-8924(93)90174-y
Keryer G, Witczak O, Delouvée A, Kemmner WA, Rouillard D, Taskén K, Bornens M (2003) Dissociating the centrosomal matrix protein AKAP450 from centrioles impairs centriole duplication and cell cycle progression. Mol Biol Cell 14(6):2436–2446. https://doi.org/10.1091/mbc.e02-09-0614
Kirkham M, Müller-Reichert T, Oegema K, Grill S, Hyman AA (2003) SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112(4):575–587. https://doi.org/https://doi.org/10.1016/s0092-8674(03)00117-x
Kobayashi T, Dynlacht BD (2011) Regulating the transition from centriole to basal body. J Cell Biol 193(3):435–444. https://doi.org/10.1083/jcb.201101005
Kollman JM, Greenberg CH, Li S, Moritz M, Zelter A, Fong KK, Fernandez J-J, Sali A, Kilmartin J, Davis TN, Agard DA (2015) Ring closure activates yeast γTuRC for species-specific microtubule nucleation. Nat Struct Mol Biol 22(2):132–137. https://doi.org/10.1038/nsmb.2953
Kollman JM, Merdes A, Mourey L, Agard DA (2011) Microtubule nucleation by γ-tubulin complexes. Nat Rev Mol Cell Biol 12(11):709–721. https://doi.org/10.1038/nrm3209
Kollman JM, Polka JK, Zelter A, Davis TN, Agard DA (2010) Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466(7308):879–882. https://doi.org/10.1038/nature09207
Kollman JM, Zelter A, Muller EGD, Fox B, Rice LM, Davis TN, Agard DA (2008) The structure of the gamma-tubulin small complex: implications of its architecture and flexibility for microtubule nucleation. Mol Biol Cell 19(1):207–215. https://doi.org/10.1091/mbc.e07-09-0879
Kufer TA, Silljé HHW, Körner R, Gruss OJ, Meraldi P, Nigg EA (2002) Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 158(4):617–623. https://doi.org/10.1083/jcb.200204155
Laos T, Cabral G, Dammermann A (2015) Isotropic incorporation of SPD-5 underlies centrosome assembly in C. elegans. Curr Biol CB 25(15):R648– R649. https://doi.org/https://doi.org/10.1016/j.cub.2015.05.060
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(11):1148–1158. https://doi.org/10.1038/ncb2591
Lecland N, Hsu C-Y, Chemin C, Merdes A, Bierkamp C (2019) Epidermal development requires ninein for spindle orientation and cortical microtubule organization. Life Sci Alliance 2(2). https://doi.org/https://doi.org/10.26508/lsa.201900373
Lee K, Rhee K (2011) PLK1 phosphorylation of pericentrin initiates centrosome maturation at the onset of mitosis. J Cell Biol 195(7):1093–1101. https://doi.org/10.1083/jcb.201106093
Leidel S, Gönczy P (2003) SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle. Dev Cell 4(3):431–439. https://doi.org/10.1016/s1534-5807(03)00062-5
Li Z, Dai K, Wang C, Song Y, Gu F, Liu F, Fu L (2016) Expression of polo-like kinase 4(PLK4) in breast cancer and its response to taxane-based neoadjuvant chemotherapy. J Cancer 7(9):1125–1132. https://doi.org/10.7150/jca.14307
Lin T, Neuner A, Schiebel E (2015) Targeting of γ-tubulin complexes to microtubule organizing centers: conservation and divergence. Trends Cell Biol 25(5):296–307. https://doi.org/10.1016/j.tcb.2014.12.002
Lin Y-C, Chang C-W, Hsu W-B, Tang C-JC, Lin Y-N, Chou E-J, Wu C-T, Tang TK (2013) Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J 32(8):1141–1154. https://doi.org/10.1038/emboj.2013.56
Liu P, Zupa E, Neuner A, Böhler A, Loerke J, Flemming D, Ruppert T, Rudack T, Peter C, Spahn C, Gruss OJ, Pfeffer S, Schiebel E (2020) Insights into the assembly and activation of the microtubule nucleator γ-TuRC. Nature 578(7795):467–471. https://doi.org/10.1038/s41586-019-1896-6
Liu P, Choi Y-K, Qi RZ (2014) NME7 is a functional component of the γ-tubulin ring complex. Mol Biol Cell 25(13):2017–2025. https://doi.org/10.1091/mbc.E13-06-0339
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(22):2708–2713. https://doi.org/10.1016/j.cub.2014.09.053
Meng L, Park J-E, Kim T-S, Lee EH, Park S-Y, Zhou M, Bang JK, Lee KS (2015) Bimodal interaction of mammalian Polo-Like Kinase 1 and a centrosomal scaffold, Cep192, in the regulation of bipolar spindle formation. Mol Cell Biol 35(15):2626–2640. https://doi.org/10.1128/MCB.00068-15
Mennella V, Keszthelyi B, McDonald KL, Chhun B, Kan F, Rogers GC, Huang B, Agard DA (2012) Sub-diffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 14(11):1159–1168. https://doi.org/10.1038/ncb2597
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
Moritz M, Braunfeld MB, Guénebaut V, Heuser J, Agard DA (2000) Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2(6):365–370. https://doi.org/10.1038/35014058
Moritz M, Braunfeld MB, Sedat JW, Alberts B, Agard DA (1995) Microtubule nucleation by gamma-tubulin-containing rings in the centrosome. Nature 378(6557):638–640. https://doi.org/10.1038/378638a0
Mottier-Pavie V, Megraw TL (2009) Drosophila Bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol Biol Cell 20(10):2605–2614. https://doi.org/https://doi.org/10.1091/mbc.E08-11-1115
Murphy SM, Preble AM, Patel UK, O’Connell KL, Dias DP, Moritz M, Agard D, Stults JT, Stearns T (2001) GCP5 and GCP6: two new members of the human gamma-tubulin complex. Mol Biol Cell 12(11):3340–3352. https://doi.org/10.1091/mbc.12.11.3340
Novak ZA, Wainman A, Gartenmann L, Raff JW (2016) Cdk1 phosphorylates Drosophila Sas-4 to recruit polo to daughter centrioles and convert them to centrosomes. Dev Cell 37(6):545–557. https://doi.org/10.1016/j.devcel.2016.05.022
Oakley BR, Oakley CE, Yoon Y, Jung MK (1990) γ-tubulin is a component of the spindle pole body that is essential for microtubule function in Aspergillus nidulans. Cell 61(7):1289–1301. https://doi.org/10.1016/0092-8674(90)90693-9
Oakley BR, Paolillo V, Zheng Y (2015) γ-Tubulin complexes in microtubule nucleation and beyond. Mol Biol Cell 26(17):2957–2962. https://doi.org/10.1091/mbc.E14-11-1514
Ohta T, Essner R, Ryu J-H, Palazzo RE, Uetake Y, Kuriyama R (2002) Characterization of Cep135, a novel coiled-coil centrosomal protein involved in microtubule organization in mammalian cells. J Cell Biol 156(1):87–100. https://doi.org/10.1083/jcb.200108088
Paoletti A, Moudjou M, Paintrand M, Salisbury JL, Bornens M (1996) Most of centrin in animal cells is not centrosome-associated and centrosomal centrin is confined to the distal lumen of centrioles. J Cell Sci 109:3089–3102
Pelletier L, O’Toole E, Schwager A, Hyman AA, Müller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444(7119):619–623. https://doi.org/10.1038/nature05318
Pelletier L, Ozlü N, Hannak E, Cowan C, Habermann B, Ruer M, Müller-Reichert T, Hyman AA (2004) The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr Biol CB 14(10):863–873. https://doi.org/10.1016/j.cub.2004.04.012
Pickett-Heaps J (1974) The evolution of mitosis and the eukaryotic condition. Biosystems 6(1):37–48. https://doi.org/10.1016/0303-2647(74)90009-4
Piedra F-A, Kim T, Garza ES, Geyer EA, Burns A, Ye X, Rice LM (2016) GDP-to-GTP exchange on the microtubule end can contribute to the frequency of catastrophe. Mol Biol Cell 27(22):3515–3525. https://doi.org/10.1091/mbc.E16-03-0199
Rajeev R, Singh P, Asmita A, Anand U, Manna TK (2019) Aurora A site specific TACC3 phosphorylation regulates astral microtubule assembly by stabilizing γ-tubulin ring complex. BMC Mol Cell Biol. https://doi.org/10.1186/s12860-019-0242-z
Ramani A, Mariappan A, Gottardo M, Mandad S, Urlaub H, Avidor-Reiss T, Riparbelli M, Callaini G, Debec A, Feederle R, Gopalakrishnan J (2018) Plk1/Polo phosphorylates Sas-4 at the onset of mitosis for an efficient recruitment of pericentriolar material to centrosomes. Cell Rep 25(13):3618-3630.e6. https://doi.org/10.1016/j.celrep.2018.11.102
Reschen RF, Colombie N, Wheatley L, Dobbelaere J, St Johnston D, Ohkura H, Raff JW (2012) Dgp71WD is required for the assembly of the acentrosomal Meiosis I spindle, and is not a general targeting factor for the γ-TuRC. Biol Open 1(5):422–429. https://doi.org/10.1242/bio.2012596
Richens JH, Barros TP, Lucas EP, Peel N, Pinto DMS, Wainman A, Raff JW (2015) The Drosophila Pericentrin-like-protein (PLP) cooperates with Cnn to maintain the integrity of the outer PCM. Biol Open 4(8):1052–1061. https://doi.org/10.1242/bio.012914
Sampaio P, Rebollo E, Varmark H, Sunkel CE, González C (2001) Organized microtubule arrays in γ-tubulin-depleted Drosophila spermatocytes. Curr Biol 11(22):1788–1793. https://doi.org/10.1016/S0960-9822(01)00561-9
Sanchez AD, Feldman JL (2017) Microtubule-organizing centers: from the centrosome to non-centrosomal sites. Curr Opin Cell Biol 44:93–101. https://doi.org/10.1016/j.ceb.2016.09.003
Schnackenberg BJ, Khodjakov A, Rieder CL, Palazzo RE (1998) The disassembly and reassembly of functional centrosomes in vitro. Proc Natl Acad Sci 95(16):9295–9300. https://doi.org/10.1073/pnas.95.16.9295
Seetapun D, Castle BT, McIntyre AJ, Tran PT, Odde DJ (2012) Estimating the microtubule GTP cap size in vivo. Curr Biol 22(18):1681–1687. https://doi.org/10.1016/j.cub.2012.06.068
Shahid U, Singh P (2018) Emerging picture of deuterosome-dependent centriole amplification in MCCs. Cells. https://doi.org/https://doi.org/10.3390/cells7100152
Shinmura K, Kato H, Kawanishi Y, Nagura K, Kamo T, Okubo Y, Inoue Y, Kurabe N, Du C, Iwaizumi M, Kurachi K, Nakamura T, Sugimura H (2015) SASS6 overexpression is associated with mitotic chromosomal abnormalities and a poor prognosis in patients with colorectal cancer. Oncol Rep 34(2):727–738. https://doi.org/10.3892/or.2015.4014
Singh P, Ramdas Nair A, Cabernard C (2014) The centriolar protein Bld10/Cep135 is required to establish centrosome asymmetry in Drosophila neuroblasts. Curr Biol CB 24(13):1548–1555. https://doi.org/10.1016/j.cub.2014.05.050
Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA (2012) 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 1(10):965–976. https://doi.org/10.1242/bio.20122337
Stearns T, Evans L, Kirschner M (1991) γ-Tubulin is a highly conserved component of the centrosome. Cell 65(5):825–836. https://doi.org/10.1016/0092-8674(91)90390-K
Stillwell EE, Zhou J, Joshi HC (2004) Human Ninein is a centrosomal autoantigen recognized by CREST patient sera and plays a regulatory role in microtubule nucleation. Cell Cycle 3(7):921–928. https://doi.org/10.4161/cc.3.7.947
Strome S, Powers J, Dunn M, Reese K, Malone CJ, White J, Seydoux G, Saxton W (2001) Spindle dynamics and the role of γ-tubulin in early Caenorhabditis elegans embryos. Mol Biol Cell 12(6):1751–1764. https://doi.org/10.1091/mbc.12.6.1751
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(9):4099–4111. https://doi.org/10.4049/jimmunol.1402459
Takahashi M, Yamagiwa A, Nishimura T, Mukai H, Ono Y (2002) Centrosomal proteins CG-NAP and kendrin provide microtubule nucleation sites by anchoring gamma-tubulin ring complex. Mol Biol Cell 13(9):3235–3245. https://doi.org/10.1091/mbc.e02-02-0112
Teixidó-Travesa N, Villén J, Lacasa C, Bertran MT, Archinti M, Gygi SP, Caelles C, Roig J, Lüders J (2010) The γTuRC revisited: a comparative analysis of interphase and mitotic human γTuRC redefines the set of core components and identifies the novel subunit GCP8. Mol Biol Cell 21(22):3963–3972. https://doi.org/10.1091/mbc.e10-05-0408
Ueda M, Gräf R, MacWilliams HK, Schliwa M, Euteneuer U (1997) Centrosome positioning and directionality of cell movements. Proc Natl Acad Sci 94(18):9674–9678. https://doi.org/10.1073/pnas.94.18.9674
Vérollet C, Colombié N, Daubon T, Bourbon H-M, Wright M, Raynaud-Messina B (2006) Drosophila melanogaster γ-TuRC is dispensable for targeting γ-tubulin to the centrosome and microtubule nucleation. J Cell Biol 172(4):517–528. https://doi.org/10.1083/jcb.200511071
Wakida NM, Botvinick EL, Lin J, Berns MW (2010) An intact centrosome is required for the maintenance of polarization during directional cell migration. PLoS ONE 5(12):e15462. https://doi.org/10.1371/journal.pone.0015462
Wieczorek M, Urnavicius L, Ti S-C, Molloy KR, Chait BT, Kapoor TM (2020) Asymmetric molecular architecture of the human γ-tubulin ring complex. Cell 180(1):165-175.e16. https://doi.org/10.1016/j.cell.2019.12.007
Wilson EB (1901) Ueber die Natur der Centrosomen. Science 13(320):264–267. https://doi.org/10.1126/science.13.320.264
Winey M, O’Toole E (2014) Centriole structure. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2013.0457
Woodruff JB, Gomes BF, Widlund PO, Mahamid J, Honigmann A, Hyman AA (2017) The centrosome is a selective condensate that nucleates microtubules by concentrating Tubulin. Cell 169(6):1066-1077.e10. https://doi.org/10.1016/j.cell.2017.05.028
Wu J, Akhmanova A (2017) Microtubule-organizing centers. Annu Rev Cell Dev Biol 33(1):51–75. https://doi.org/10.1146/annurev-cellbio-100616-060615
Wueseke O, Zwicker D, Schwager A, Wong YL, Oegema K, Jülicher F, Hyman AA, Woodruff JB (2016) Polo-like kinase phosphorylation determines Caenorhabditis elegans centrosome size and density by biasing SPD-5 toward an assembly-competent conformation. Biol Open 5(10):1431–1440. https://doi.org/10.1242/bio.020990
Zhang J, Wang Y (2017) Centrosome defines the rear of cells during mesenchymal migration. Mol Biol Cell 28(23):3240–3251. https://doi.org/10.1091/mbc.e17-06-0366
Zhang J, Megraw TL (2007) Proper recruitment of γ-tubulin and D-TACC/Msps to embryonic Drosophila centrosomes requires Centrosomin Motif 1. Mol Biol Cell 18(10):4037–4049. https://doi.org/10.1091/mbc.e07-05-0474
Zhang T, Braun U, Leitges M (2016) PKD3 deficiency causes alterations in microtubule dynamics during the cell cycle. Cell Cycle 15(14):1844–1854. https://doi.org/10.1080/15384101.2016.1188237
Zheng Y, Wong ML, Alberts B, Mitchison T (1995) Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378(6557):578–583. https://doi.org/10.1038/378578a0
Zimmerman WC, Sillibourne J, Rosa J, Doxsey SJ (2004) Mitosis-specific anchoring of gamma tubulin complexes by pericentrin controls spindle organization and mitotic entry. Mol Biol Cell 15(8):3642–3657. https://doi.org/10.1091/mbc.e03-11-0796
Acknowledgements
PS is thankful to Indian Institute of Technology Jodhpur for seed fund and infrastructure support. PS would like to thank Science and Engineering Research Board (Grant ECR/2017/001410), Department of Science and Technology, India and Department of Biotechnology (BT/12/IYBA/2019/02) for the funding support. SJ, HK and SJ are supported by the fellowship from the Ministry of Education, India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jaiswal, S., Kasera, H., Jain, S. et al. Centrosome: A Microtubule Nucleating Cellular Machinery. J Indian Inst Sci 101, 5–18 (2021). https://doi.org/10.1007/s41745-020-00213-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s41745-020-00213-1