New insights into subcomplex assembly and modifications of centrosomal proteins

Cell Division

Volumn 7, Issue , 2012, Pages

  Habermann, Karin ^a   Lange, Bodo M H ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

TuRC; Augmin HAUS complex; Centrosome

Indexed keywords

EID: 84867772494     PISSN: None     EISSN: 17471028     Source Type: Journal    
DOI: 10.1186/1747-1028-7-17     Document Type: Review

References (91)

1. Dobbelaere J, Josue F, Suijkerbuijk S, Baum B, Tapon N, Raff J. A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol 2008, 6:e224. 10.1371/journal.pbio.0060224, 2535660, 18798690.
2. Fuchs F, Pau G, Kranz D, Sklyar O, Budjan C, Steinbrink S, Horn T, Pedal A, Huber W, Boutros M. Clustering phenotype populations by genome-wide RNAi and multiparametric imaging. Mol Syst Biol 2010, 6:370. 2913390, 20531400.
3. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316:417-421. 10.1126/science.1141314, 2837481, 17412918.
4. Neumann B, Walter T, Heriche JK, Bulkescher J, Erfle H, Conrad C, Rogers P, Poser I, Held M, Liebel U, et al. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 2010, 464:721-727. 10.1038/nature08869, 3108885, 20360735.
5. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 2003, 426:570-574. 10.1038/nature02166, 14654843.
6. Müller H, Schmidt D, Steinbrink S, Mirgorodskaya E, Lehmann V, Habermann K, Dreher F, Gustavsson N, Kessler T, Lehrach H, et al. Proteomic and functional analysis of the mitotic Drosophila centrosome. EMBO J 2010, 29:3344-3357. 10.1038/emboj.2010.210, 2957212, 20818332.
7. Jakobsen L, Vanselow K, Skogs M, Toyoda Y, Lundberg E, Poser I, Falkenby LG, Bennetzen M, Westendorf J, Nigg EA, et al. Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J 2011, 30:1520-1535. 10.1038/emboj.2011.63, 3102290, 21399614.
8. Wigge PA, Jensen ON, Holmes S, Soues S, Mann M, Kilmartin JV. Analysis of the Saccharomyces spindle pole by matrix-assisted laser desorption/ionization (MALDI) mass spectrometry. J Cell Biol 1998, 141:967-977. 10.1083/jcb.141.4.967, 2132767, 9585415.
9. Sauer G, Korner R, Hanisch A, Ries A, Nigg EA, Sillje HH. Proteome analysis of the human mitotic spindle. Mol Cell Proteomics 2005, 4:35-43.
10. Liska AJ, Popov AV, Sunyaev S, Coughlin P, Habermann B, Shevchenko A, Bork P, Karsenti E. Homology-based functional proteomics by mass spectrometry: application to the Xenopus microtubule-associated proteome. Proteomics 2004, 4:2707-2721. 10.1002/pmic.200300813, 15352245.
11. Reinders Y, Schulz I, Graf R, Sickmann A. Identification of novel centrosomal proteins in Dictyostelium discoideum by comparative proteomic approaches. J Proteome Res 2006, 5:589-598. 10.1021/pr050350q, 16512674.
12. Ostrowski LE, Blackburn K, Radde KM, Moyer MB, Schlatzer DM, Moseley A, Boucher RC. A proteomic analysis of human cilia: identification of novel components. Mol Cell Proteomics 2002, 1:451-465. 10.1074/mcp.M200037-MCP200, 12169685.
13. Liu Q, Tan G, Levenkova N, Li T, Pugh EN, Rux JJ, Speicher DW, Pierce EA. The proteome of the mouse photoreceptor sensory cilium complex. Mol Cell Proteomics 2007, 6:1299-1317. 10.1074/mcp.M700054-MCP200, 2128741, 17494944.
14. Keller LC, Romijn EP, Zamora I, Yates JR, Marshall WF. Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr Biol 2005, 15:1090-1098. 10.1016/j.cub.2005.05.024, 15964273.
15. Pazour GJ, Agrin N, Leszyk J, Witman GB. Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005, 170:103-113. 10.1083/jcb.200504008, 2171396, 15998802.
16. Broadhead R, Dawe HR, Farr H, Griffiths S, Hart SR, Portman N, Shaw MK, Ginger ML, Gaskell SJ, McKean PG, Gull K. Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 2006, 440:224-227. 10.1038/nature04541, 16525475.
17. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, Li H, Blacque OE, Li L, Leitch CC, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 2004, 117:541-552. 10.1016/S0092-8674(04)00450-7, 15137946.
18. Baron DM, Ralston KS, Kabututu ZP, Hill KL. Functional genomics in Trypanosoma brucei identifies evolutionarily conserved components of motile flagella. J Cell Sci 2007, 120:478-491. 10.1242/jcs.03352, 17227795.
19. Chen N, Mah A, Blacque OE, Chu J, Phgora K, Bakhoum MW, Newbury CR, Khattra J, Chan S, Go A, et al. Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol 2006, 7:R126. 10.1186/gb-2006-7-12-r126, 1794439, 17187676.
20. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, et al. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 2007, 318:245-250. 10.1126/science.1143609, 2875087, 17932292.
21. Nogales-Cadenas R, Abascal F, Diez-Perez J, Carazo JM, Pascual-Montano A. CentrosomeDB: a human centrosomal proteins database. Nucleic Acids Res 2009, 37:D175-180. 10.1093/nar/gkn815, 2686521, 18971254.
22. Ren J, Liu Z, Gao X, Jin C, Ye M, Zou H, Wen L, Zhang Z, Xue Y, Yao X. MiCroKit 3.0: an integrated database of midbody, centrosome and kinetochore. Nucleic Acids Res 2010, 38:D155-160. 10.1093/nar/gkp784, 2808993, 19783819.
23. Bettencourt-Dias M, Glover DM. Centrosome biogenesis and function: centrosomics brings new understanding. Nat Rev Mol Cell Biol 2007, 8:451-463. 10.1038/nrm2180, 17505520.
24. Doxsey S. Re-evaluating centrosome function. Nat Rev Mol Cell Biol 2001, 2:688-698. 10.1038/35089575, 11533726.
25. Schatten H. The mammalian centrosome and its functional significance. Histochem Cell Biol 2008, 129:667-686. 10.1007/s00418-008-0427-6, 2386528, 18437411.
26. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW. Flies without centrioles. Cell 2006, 125:1375-1386. 10.1016/j.cell.2006.05.025, 16814722.
27. Schmit AC. Acentrosomal microtubule nucleation in higher plants. Int Rev Cytol 2002, 220:257-289.
28. Singla V, Reiter JF. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 2006, 313:629-633. 10.1126/science.1124534, 16888132.
29. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 1998, 95:829-837. 10.1016/S0092-8674(00)81705-5, 9865700.
30. Badano JL, Mitsuma N, Beales PL, Katsanis N. The ciliopathies: an emerging class of human genetic disorders. Annu Rev Genomics Hum Genet 2006, 7:125-148. 10.1146/annurev.genom.7.080505.115610, 16722803.
31. Sluder G. Two-way traffic: centrosomes and the cell cycle. Nat Rev Mol Cell Biol 2005, 6:743-748.
32. Debec A, Marcaillou C. Structural alterations of the mitotic apparatus induced by the heat shock response in Drosophila cells. Biol Cell 1997, 89:67-78. 10.1016/S0248-4900(99)80082-3, 9297784.
33. Sibon OC, Kelkar A, Lemstra W, Theurkauf WE. DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat Cell Biol 2000, 2:90-95. 10.1038/35000041, 10655588.
34. Takada S, Kelkar A, Theurkauf WE. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 2003, 113:87-99. 10.1016/S0092-8674(03)00202-2, 12679037.
35. Hut HM, Lemstra W, Blaauw EH, Van Cappellen GW, Kampinga HH, Sibon OC. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol Biol Cell 2003, 14:1993-2004. 10.1091/mbc.E02-08-0510, 165092, 12802070.
36. Castedo M, Perfettini JL, Roumier T, Yakushijin K, Horne D, Medema R, Kroemer G. The cell cycle checkpoint kinase Chk2 is a negative regulator of mitotic catastrophe. Oncogene 2004, 23:4353-4361. 10.1038/sj.onc.1207573, 15048074.
37. Lange BM, Bachi A, Wilm M, Gonzalez C. Hsp90 is a core centrosomal component and is required at different stages of the centrosome cycle in Drosophila and vertebrates. EMBO J 2000, 19:1252-1262. 10.1093/emboj/19.6.1252, 305666, 10716925.
38. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 2004, 6:884-891. 10.1038/ncb1165, 15311285.
39. Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A, Raff JW. Centrosome amplification can initiate tumorigenesis in flies. Cell 2008, 133:1032-1042. 10.1016/j.cell.2008.05.039, 2653712, 18555779.
40. Castellanos E, Dominguez P, Gonzalez C. Centrosome dysfunction in Drosophila neural stem cells causes tumors that are not due to genome instability. Curr Biol 2008, 18:1209-1214. 10.1016/j.cub.2008.07.029, 18656356.
41. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009, 460:278-282. 10.1038/nature08136, 2743290, 19506557.
42. Kwon M, Godinho SA, Chandhok NS, Ganem NJ, Azioune A, Thery M, Pellman D. Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev 2008, 22:2189-2203. 10.1101/gad.1700908, 2518815, 18662975.
43. Silkworth WT, Nardi IK, Scholl LM, Cimini D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS One 2009, 4:e6564. 10.1371/journal.pone.0006564, 2719800, 19668340.
44. Yang Z, Loncarek J, Khodjakov A, Rieder CL. Extra centrosomes and/or chromosomes prolong mitosis in human cells. Nat Cell Biol 2008, 10:748-751. 10.1038/ncb1738, 2430725, 18469805.
45. Quintyne NJ, Reing JE, Hoffelder DR, Gollin SM, Saunders WS. Spindle multipolarity is prevented by centrosomal clustering. Science 2005, 307:127-129. 10.1126/science.1104905, 15637283.
46. Nigg EA, Raff JW. Centrioles, centrosomes, and cilia in health and disease. Cell 2009, 139:663-678. 10.1016/j.cell.2009.10.036, 19914163.
47. Doxsey S, McCollum D, Theurkauf W. Centrosomes in cellular regulation. Annu Rev Cell Dev Biol 2005, 21:411-434. 10.1146/annurev.cellbio.21.122303.120418, 16212501.
48. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
49. Mahoney NM, Goshima G, Douglass AD, Vale RD. Making microtubules and mitotic spindles in cells without functional centrosomes. Curr Biol 2006, 16:564-569. 10.1016/j.cub.2006.01.053, 16546079.
50. Fava F, Raynaud-Messina B, Leung-Tack J, Mazzolini L, Li M, Guillemot JC, Cachot D, Tollon Y, Ferrara P, Wright M. Human 76p: A new member of the gamma-tubulin-associated protein family. J Cell Biol 1999, 147:857-868. 10.1083/jcb.147.4.857, 2156165, 10562286.
51. Murphy SM, Preble AM, Patel UK, O'Connell KL, Dias DP, Moritz M, Agard D, Stults JT, Stearns T. GCP5 and GCP6: two new members of the human gamma-tubulin complex. Mol Biol Cell 2001, 12:3340-3352. 60259, 11694571.
52. Murphy SM, Urbani L, Stearns T. The mammalian gamma-tubulin complex contains homologues of the yeast spindle pole body components spc97p and spc98p. J Cell Biol 1998, 141:663-674. 10.1083/jcb.141.3.663, 2132743, 9566967.
53. Haren L, Remy MH, Bazin I, Callebaut I, Wright M, Merdes A. NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 2006, 172:505-515. 10.1083/jcb.200510028, 2063671, 16461362.
54. Lüders J, Patel UK, Stearns T. GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat Cell Biol 2006, 8:137-147. 10.1038/ncb1349, 16378099.
55. Oegema K, Wiese C, Martin OC, Milligan RA, Iwamatsu A, Mitchison TJ, 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. 10.1083/jcb.144.4.721, 2132928, 10037793.
56. Kollman JM, Polka JK, Zelter A, Davis TN, Agard DA. Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 2010, 466:879-882. 10.1038/nature09207, 2921000, 20631709.
57. Moritz M, Braunfeld MB, Guenebaut V, Heuser J, Agard DA. Structure of the gamma-tubulin ring complex: a template for microtubule nucleation. Nat Cell Biol 2000, 2:365-370. 10.1038/35014058, 10854328.
58. Fong KW, Choi YK, Rattner JB, Qi RZ. CDK5RAP2 is a pericentriolar protein that functions in centrosomal attachment of the gamma-tubulin ring complex. Mol Biol Cell 2008, 19:115-125. 10.1091/mbc.E07-04-0371, 2174194, 17959831.
59. Choi YK, Liu P, Sze SK, Dai C, Qi RZ. CDK5RAP2 stimulates microtubule nucleation by the gamma-tubulin ring complex. J Cell Biol 2010, 191:1089-1095. 10.1083/jcb.201007030, 3002024, 21135143.
60. Hutchins JR, Toyoda Y, Hegemann B, Poser I, Heriche JK, Sykora MM, Augsburg M, Hudecz O, Buschhorn BA, Bulkescher J, et al. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328:593-599. 10.1126/science.1181348, 2989461, 20360068.
61. Teixido-Travesa N, Villen J, Lacasa C, Bertran MT, Archinti M, Gygi SP, 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. 10.1091/mbc.E10-05-0408, 2982109, 20861304.
62. Goshima G, Mayer M, Zhang N, Stuurman N, Vale RD. Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J Cell Biol 2008, 181:421-429. 10.1083/jcb.200711053, 2364697, 18443220.
63. Uehara R, Nozawa RS, Tomioka A, Petry S, Vale RD, Obuse C, Goshima G. 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 2009, 106:6998-7003. 10.1073/pnas.0901587106, 2668966, 19369198.
64. Meireles AM, Fisher KH, Colombie N, Wakefield JG, Ohkura H. Wac: a new Augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J Cell Biol 2009, 184:777-784. 10.1083/jcb.200811102, 2699157, 19289792.
65. Zhu H, Coppinger JA, Jang CY, Yates JR, Fang G. FAM29A promotes microtubule amplification via recruitment of the NEDD1-gamma-tubulin complex to the mitotic spindle. J Cell Biol 2008, 183:835-848. 10.1083/jcb.200807046, 2592839, 19029337.
66. Lawo S, Bashkurov M, Mullin M, Ferreria MG, Kittler R, Habermann B, Tagliaferro A, Poser I, Hutchins JR, Hegemann B, et al. HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity. Curr Biol 2009, 19:816-826. 10.1016/j.cub.2009.04.033, 19427217.
67. Conduit PT, Raff JW. Cnn dynamics drive centrosome size asymmetry to ensure daughter centriole retention in Drosophila neuroblasts. Curr Biol 2010, 20:2187-2192. 10.1016/j.cub.2010.11.055, 21145745.
68. Rebollo E, Sampaio P, Januschke J, Llamazares S, Varmark H, Gonzalez C. Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell 2007, 12:467-474. 10.1016/j.devcel.2007.01.021, 17336911.
69. Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M. The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 2010, 12:164-169. 10.1038/ncb2016, 2859955, 20081840.
70. Resendes KK, Rasala BA, Forbes DJ. Centrin 2 localizes to the vertebrate nuclear pore and plays a role in mRNA and protein export. Mol Cell Biol 2008, 28:1755-1769. 10.1128/MCB.01697-07, 2258798, 18172010.
71. Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH, O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI. beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 2008, 22:91-105. 10.1101/gad.1596308, 2151018, 18086858.
72. Fumoto K, Kadono M, Izumi N, Kikuchi A. Axin localizes to the centrosome and is involved in microtubule nucleation. EMBO Rep 2009, 10:606-613. 10.1038/embor.2009.45, 2711835, 19390532.
73. Barr AR, Kilmartin JV, Gergely F. CDK5RAP2 functions in centrosome to spindle pole attachment and DNA damage response. J Cell Biol 2010, 189:23-39. 10.1083/jcb.200912163, 2854379, 20368616.
74. Ferguson RL, Pascreau G, Maller JL. The cyclin A centrosomal localization sequence recruits MCM5 and Orc1 to regulate centrosome reduplication. J Cell Sci 2010, 123:2743-2749. 10.1242/jcs.073098, 2915877, 20663915.
75. Nayak T, Edgerton-Morgan H, Horio T, Xiong Y, De Souza CP, Osmani SA, Oakley BR. Gamma-tubulin regulates the anaphase-promoting complex/cyclosome during interphase. J Cell Biol 2010, 190:317-330. 10.1083/jcb.201002105, 2922653, 20679430.
76. Keck JM, Jones MH, Wong CC, Binkley J, Chen D, Jaspersen SL, Holinger EP, Xu T, Niepel M, Rout MP, et al. A cell cycle phosphoproteome of the yeast centrosome. Science 2011, 332:1557-1561. 10.1126/science.1205193, 21700874.
77. Lowery DM, Clauser KR, Hjerrild M, Lim D, Alexander J, Kishi K, Ong SE, Gammeltoft S, Carr SA, Yaffe MB. Proteomic screen defines the Polo-box domain interactome and identifies Rock2 as a Plk1 substrate. EMBO J 2007, 26:2262-2273. 10.1038/sj.emboj.7601683, 1864981, 17446864.
78. Vaz Meirelles G, Ferreira Lanza DC, da Silva JC, Santana Bernachi J, Paes Leme AF, Kobarg J. Characterization of hNek6 interactome reveals an important role for its short N-terminal domain and colocalization with proteins at the centrosome. J Proteome Res 2010, 9:6298-6316. 10.1021/pr100562w, 20873783.
79. Sardon T, Pache RA, Stein A, Molina H, Vernos I, Aloy P. Uncovering new substrates for Aurora A kinase. EMBO Rep 2010, 11:977-984. 10.1038/embor.2010.171, 2999863, 21072059.
80. Chang J, Cizmecioglu O, Hoffmann I, Rhee K. PLK2 phosphorylation is critical for CPAP function in procentriole formation during the centrosome cycle. EMBO J 2010, 29:2395-2406. 10.1038/emboj.2010.118, 2910268, 20531387.
81. D'Angiolella V, Donato V, Vijayakumar S, Saraf A, Florens L, Washburn MP, Dynlacht B, Pagano M. SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 2010, 466:138-142. 10.1038/nature09140, 2946399, 20596027.
82. Korzeniewski N, Cuevas R, Duensing A, Duensing S. Daughter centriole elongation is controlled by proteolysis. Mol Biol Cell 2010, 21:3942-3951. 10.1091/mbc.E09-12-1049, 2982099, 20861314.
83. Strnad P, Leidel S, Vinogradova T, Euteneuer U, Khodjakov A, Gonczy P. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev Cell 2007, 13:203-213. 10.1016/j.devcel.2007.07.004, 2628752, 17681132.
84. Puklowski A, Homsi Y, Keller D, May M, Chauhan S, Kossatz U, Grunwald V, Kubicka S, Pich A, Manns MP, et al. The SCF-FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nature Cell Biol 2011, 13:1004-1009. 10.1038/ncb2282, 21725316.
85. Klein UR, Nigg EA. SUMO-dependent regulation of centrin-2. J Cell Sci 2009, 122:3312-3321. 10.1242/jcs.050245, 19706679.
86. Gonzalez C, Tavosanis G, Mollinari C. Centrosomes and microtubule organisation during Drosophila development. J Cell Sci 1998, 111(Pt 18):2697-2706.
87. Huang B, Babcock H, Zhuang X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2011, 143:1047-1058.
88. Guichard P, Chretien D, Marco S, Tassin AM. Procentriole assembly revealed by cryo-electron tomography. EMBO J 2010, 29:1565-1572. 10.1038/emboj.2010.45, 2876950, 20339347.
89. Müller-Reichert T, Mancuso J, Lich B, McDonald K. Three-dimensional reconstruction methods for Caenorhabditis elegans ultrastructure. Methods Cell Biol 2010, 96:331-361.
90. van Breugel M, Hirono M, Andreeva A, Yanagisawa HA, Yamaguchi S, Nakazawa Y, Morgner N, Petrovich M, Ebong IO, Robinson CV, et al. Structures of SAS-6 suggest its organization in centrioles. Science 2011, 331:1196-1199. 10.1126/science.1199325, 21273447.
91. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Fluckiger I, Gonczy P, Steinmetz MO. Structural basis of the 9-fold symmetry of centrioles. Cell 2011, 144:364-375. 10.1016/j.cell.2011.01.008, 3089914, 21277013.