3D-structured illumination microscopy provides novel insight into architecture of human centrosomes

Biology Open

Volumn 1, Issue 10, 2012, Pages 965-976

  Sonnen, Katharina F ^a   Schermelleh, Lothar ^b,c   Leonhardt, Heinrich ^b   Nigg, Erich A ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

3D SIM; Centriole; Centrosome; Plk4; Super resolution microscopy

Indexed keywords

EID: 84964866213     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20122337     Document Type: Article

References (78)

1. Andersen, J. S., Wilkinson, C. J., Mayor, T., Mortensen, P., Nigg, E. A. and Mann, M. (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574.
2. Arquint, C., Sonnen, K. F., Stierhof, Y. D. and Nigg, E. A. (2012). Cell-cycleregulated expression of STIL controls centriole number in human cells. J. Cell Sci. 125, 1342-1352.
3. Bahtz, R., Seidler, J., Arnold, M., Haselmann-Weiss, U., Antony, C., Lehmann, W. D. and Hoffmann, I. (2012). GCP6 is a substrate of Plk4 and required for centriole duplication. J. Cell Sci. 125, 486-496.
4. Bettencourt-Dias, M. and Glover, D. M. (2007). Centrosome biogenesis and function: centrosomics brings new understanding. Nat. Rev. Mol. Cell Biol. 8, 451-463.
5. Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L., Riparbelli, M., Lehmann, L., Gatt, M. K., Carmo, N., Balloux, F., Callaini, G. and Glover, D. M. (2005). SAK/PLK4 is required for centriole duplication and flagella development. Curr. Biol. 15, 2199-2207.
6. Bettencourt-Dias, M., Hildebrandt, F., Pellman, D., Woods, G. and Godinho, S. A. (2011). Centrosomes and cilia in human disease. Trends Genet. 27, 307-315.
7. Blagden, S. P. and Glover, D. M. (2003). Polar expeditions-provisioning the centrosome for mitosis. Nat. Cell Biol. 5, 505-511.
8. Bobinnec, Y., Moudjou, M., Fouquet, J. P., Desbruyères, E., Eddé, B. and Bornens, M. (1998). Glutamylation of centriole and cytoplasmic tubulin in proliferating nonneuronal cells. Cell Motil. Cytoskeleton 39, 223-232.
9. Bornens, M. (2002). Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25-34.
10. Bornens, M. (2012). The centrosome in cells and organisms. Science 335, 422-426.
11. Carvalho-Santos, Z., Azimzadeh, J., Pereira-Leal, J. B. and Bettencourt-Dias, M. (2011). Evolution: Tracing the origins of centrioles, cilia, and flagella. J. Cell Biol. 194, 165-175.
12. Casenghi, M., Meraldi, P., Weinhart, U., Duncan, P. I., Körner, R. and Nigg, E. A. (2003). Polo-like kinase 1 regulates Nlp, a centrosome protein involved in microtubule nucleation. Dev. Cell 5, 113-125.
13. Chrétien, D., Buendia, B., Fuller, S. D. and Karsenti, E. (1997). Reconstruction of the centrosome cycle from cryoelectron micrographs. J. Struct. Biol. 120, 117-133.
14. Cizmecioglu, O., Arnold, M., Bahtz, R., Settele, F., Ehret, L., Haselmann-Weiss, U., Antony, C. and Hoffmann, I. (2010). Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J. Cell Biol. 191, 731-739.
15. Cunha-Ferreira, I., Rodrigues-Martins, A., Bento, I., Riparbelli, M., Zhang, W., Laue, E., Callaini, G., Glover, D. M. and Bettencourt-Dias, M. (2009). The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr. Biol. 19, 43-49.
16. Cyclin F controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 466, 138-142.
17. Delgehyr, N., Sillibourne, J. and Bornens, M. (2005). Microtubule nucleation and anchoring at the centrosome are independent processes linked by ninein function. J. Cell Sci. 118, 1565-1575.
18. Dictenberg, J. B., Zimmerman, W., Sparks, C. A., Young, A., Vidair, C., Zheng, Y., Carrington, W., Fay, F. S. and Doxsey, S. J. (1998). Pericentrin and γ-tubulin form a protein complex and are organized into a novel lattice at the centrosome. J. Cell Biol. 141, 163-174.
19. Dobbelaere, J., Josué, F., Suijkerbuijk, S., Baum, B., Tapon, N. and Raff, J. (2008). A genome-wide RNAi screen to dissect centriole duplication and centrosome maturation in Drosophila. PLoS Biol. 6, e224.
20. Doxsey, S., McCollum, D. and Theurkauf, W. (2005a). Centrosomes in cellular regulation. Annu. Rev. Cell Dev. Biol. 21, 411-434.
21. Doxsey, S., Zimmerman, W. and Mikule, K. (2005b). Centrosome control of the cell cycle. Trends Cell Biol. 15, 303-311.
22. Dzhindzhev, N. S., Yu, Q. D., Weiskopf, K., Tzolovsky, G., Cunha-Ferreira, I., Riparbelli, M., Rodrigues-Martins, A., Bettencourt-Dias, M., Callaini, G. and Glover, D. M. (2010). Asterless is a scaffold for the onset of centriole assembly. Nature 467, 714-718.
23. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
24. Fry, A. M., Mayor, T., Meraldi, P., Stierhof, Y. D., Tanaka, K. and Nigg, E. A. (1998). C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 141, 1563-1574.
25. Fuller, S. D., Gowen, B. E., Reinsch, S., Sawyer, A., Buendia, B., Wepf, R. and Karsenti, E. (1995). The core of the mammalian centriole contains γ-tubulin. Curr. Biol. 5, 1384-1393.
26. Graser, S., Stierhof, Y. D., Lavoie, S. B., Gassner, O. S., Lamla, S., Le Clech, M. and Nigg, E. A. (2007a). Cep164, a novel centriole appendage protein required for primary cilium formation. J. Cell Biol. 179, 321-330.
27. Graser, S., Stierhof, Y. D. and Nigg, E. A. (2007b). Cep68 and Cep215 (Cdk5rap2) are required for centrosome cohesion. J. Cell Sci. 120, 4321-4331.
28. Guarguaglini, G., Duncan, P. I., Stierhof, Y. D., Holmström, T., Duensing, S. and Nigg, E. A. (2005). The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol. Biol. Cell 16, 1095-1107.
29. Guderian, G., Westendorf, J., Uldschmid, A. and Nigg, E. A. (2010). Plk4 transautophosphorylation regulates centriole number by controlling βTrCP-mediated degradation. J. Cell Sci. 123, 2163-2169.
30. Guichard, P., Chrétien, D., Marco, S. and Tassin, A. M. (2010). Procentriole assembly revealed by cryo-electron tomography. EMBO J. 29, 1565-1572.
31. Gustafsson, M. G., Shao, L., Carlton, P. M., Wang, C. J., Golubovskaya, I. N., Cande, W. Z., Agard, D. A. and Sedat, J. W. (2008). Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957-4970.
32. Habedanck, R., Stierhof, Y. D., Wilkinson, C. J. and Nigg, E. A. (2005). The Polo kinase Plk4 functions in centriole duplication. Nat. Cell Biol. 7, 1140-1146.
33. Haren, L., Stearns, T. and Lüders, J. (2009). Plk1-dependent recruitment of γ-tubulin complexes to mitotic centrosomes involves multiple PCM components. PLoS ONE 4, e5976.
34. Hatch, E. M., Kulukian, A., Holland, A. J., Cleveland, D. W. and Stearns, T. (2010). Cep152 interacts with Plk4 and is required for centriole duplication. J. Cell Biol. 191, 721-729.
35. Hell, S. W. (2007). Far-field optical nanoscopy. Science 316, 1153-1158.
36. Hiraki, M., Nakazawa, Y., Kamiya, R. and Hirono, M. (2007). Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr. Biol. 17, 1778-1783.
37. Holland, A. J., Lan, W., Niessen, S., Hoover, H. and Cleveland, D. W. (2010). Pololike kinase 4 kinase activity limits centrosome overduplication by autoregulating its own stability. J. Cell Biol. 188, 191-198.
38. Huang, B., Babcock, H. and Zhuang, X. (2010). Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143, 1047-1058.
39. Ishikawa, H. and Marshall, W. F. (2011). Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12, 222-234.
40. Jakobsen, L., Vanselow, K., Skogs, M., Toyoda, Y., Lundberg, E., Poser, I., Falkenby, L. G., Bennetzen, M., Westendorf, J., Nigg, E. A. et al. (2011). Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J. 30, 1520-1535.
41. Kitagawa, D., Vakonakis, I., Olieric, N., Hilbert, M., Keller, D., Olieric, V., Bortfeld, M., Erat, M. C., Flückiger, I., Gönczy, P. et al. (2011). Structural basis of the 9-fold symmetry of centrioles. Cell 144, 364-375.
42. Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Habedanck, R., Stierhof, Y.-D. and Nigg, E. A. (2007). Plk4-induced centriole biogenesis in human cells. Dev. Cell 13, 190-202.
43. Kohlmaier, G., Lončarek, J., Meng, X., McEwen, B. F., Mogensen, M. M., Spektor, A., Dynlacht, B. D., Khodjakov, A. and Gönczy, P. (2009). Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr. Biol. 19, 1012-1018.
44. Li, S., Fernandez, J. J., Marshall, W. F. and Agard, D. A. (2012). Three-dimensional structure of basal body triplet revealed by electron cryo-tomography. EMBO J. 31, 552-562.
45. Lüders, J. and Stearns, T. (2007). Microtubule-organizing centres: a re-evaluation. Nat. Rev. Mol. Cell Biol. 8, 161-167.
46. Lüders, J., Patel, U. K. and 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.
47. Matsuura, K., Lefebvre, P. A., Kamiya, R. and Hirono, M. (2004). Bld10p, a novel protein essential for basal body assembly in Chlamydomonas: localization to the cartwheel, the first ninefold symmetrical structure appearing during assembly. J. Cell Biol. 165, 663-671.
48. Meraldi, P., Lukas, J., Fry, A. M., Bartek, J. and Nigg, E. A. (1999). Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat. Cell Biol. 1, 88-93.
49. Mogensen, M. M., Malik, A., Piel, M., Bouckson-Castaing, V. and Bornens, M. (2000). Microtubule minus-end anchorage at centrosomal and non-centrosomal sites: the role of ninein. J. Cell Sci. 113, 3013-3023.
50. Nakazawa, Y., Hiraki, M., Kamiya, R. and Hirono, M. (2007). SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr. Biol. 17, 2169-2174.
51. Nigg, E. A. (2002). Centrosome aberrations: cause or consequence of cancer progression? Nat. Rev. Cancer 2, 815-825.
52. Nigg, E. A. and Raff, J. W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678.
53. Nigg, E. A. and Stearns, T. (2011). The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat. Cell Biol. 13, 1154-1160.
54. Paintrand, M., Moudjou, M., Delacroix, H. and Bornens, M. (1992). Centrosome organization and centriole architecture: their sensitivity to divalent cations. J. Struct. Biol. 108, 107-128.
55. Palazzo, R. E., Vogel, J. M., Schnackenberg, B. J., Hull, D. R. and Wu, X. (1999). Centrosome maturation. Curr. Top. Dev. Biol. 49, 449-470.
56. Paoletti, A., Moudjou, M., Paintrand, M., Salisbury, J. L. and 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.
57. Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. and Bornens, M. (2000). The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-330.
58. Rogers, G. C., Rusan, N. M., Roberts, D. M., Peifer, M. and Rogers, S. L. (2009). The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 184, 225-239.
59. Schermelleh, L., Carlton, P. M., Haase, S., Shao, L., Winoto, L., Kner, P., Burke, B., Cardoso, M. C., Agard, D. A., Gustafsson, M. G. et al. (2008). Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332-1336.
60. Schermelleh, L., Heintzmann, R. and Leonhardt, H. (2010). A guide to superresolution fluorescence microscopy. J. Cell Biol. 190, 165-175.
61. Schmidt, T. I., Kleylein-Sohn, J., Westendorf, J., Le Clech, M., Lavoie, S. B., Stierhof, Y.-D. and Nigg, E. A. (2009). Control of centriole length by CPAP and CP110. Curr. Biol. 19, 1005-1011.
62. Sillibourne, J. E., Tack, F., Vloemans, N., Boeckx, A., Thambirajah, S., Bonnet, P., Ramaekers, F. C., Bornens, M. and Grand-Perret, T. (2010). Autophosphorylation of polo-like kinase 4 and its role in centriole duplication. Mol. Biol. Cell 21, 547-561.
63. Sillibourne, J. E., Specht, C. G., Izeddin, I., Hurbain, I., Tran, P., Triller, A., Darzacq, X., Dahan, M. and Bornens, M. (2011). Assessing the localization of centrosomal proteins by PALM/STORM nanoscopy. Cytoskeleton 68, 619-627.
64. Sir, J. H., Barr, A. R., Nicholas, A. K., Carvalho, O. P., Khurshid, M., Sossick, A., Reichelt, S., D'Santos, C., Woods, C. G. and Gergely, F. (2011). A primary microcephaly protein complex forms a ring around parental centrioles. Nat. Genet. 43, 1147-1153.
65. Spektor, A., Tsang, W. Y., Khoo, D. and Dynlacht, B. D. (2007). Cep97 and CP110 suppress a cilia assembly program. Cell 130, 678-690.
66. Stevens, N. R., Dobbelaere, J., Brunk, K., Franz, A. and Raff, J. W. (2010). Drosophila Ana2 is a conserved centriole duplication factor. J. Cell Biol. 188, 313-323.
67. Strnad, P. and Gönczy, P. (2008). Mechanisms of procentriole formation. Trends Cell Biol. 18, 389-396.
68. Strnad, P., Leidel, S., Vinogradova, T., Euteneuer, U., Khodjakov, A. and Gönczy, P. (2007). Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell 13, 203-213.
69. Tang, C. J., Fu, R. H., Wu, K. S., Hsu, W. B. and Tang, T. K. (2009). CPAP is a cellcycle regulated protein that controls centriole length. Nat. Cell Biol. 11, 825-831.
70. Tang, C. J., Lin, S. Y., Hsu, W. B., Lin, Y. N., Wu, C. T., Lin, Y. C., Chang, C. W., Wu, K. S. and Tang, T. K. (2011). The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J. 30, 4790-4804.
71. Thein, K. H., Kleylein-Sohn, J., Nigg, E. A. and Gruneberg, U. (2007). Astrin is required for the maintenance of sister chromatid cohesion and centrosome integrity. J. Cell Biol. 178, 345-354.
72. Toomre, D. and Bewersdorf, J. (2010). A new wave of cellular imaging. Annu. Rev. Cell Dev. Biol. 26, 285-314.
73. van Breugel, M., Hirono, M., Andreeva, A., Yanagisawa, H. A., Yamaguchi, S., Nakazawa, Y., Morgner, N., Petrovich, M., Ebong, I. O., Robinson, C. V. et al. (2011). Structures of SAS-6 suggest its organization in centrioles. Science 331, 1196-1199.
74. Vorobjev, I. A. and Chentsov, Y. S. (1980). The ultrastructure of centriole in mammalian tissue culture cells. Cell Biol. Int. Rep. 4, 1037-1044.
75. Vulprecht, J., David, A., Tibelius, A., Castiel, A., Konotop, G., Liu, F., Bestvater, F., Raab, M. S., Zentgraf, H., Izraeli, S. et al. (2012). STIL is required for centriole duplication in human cells. J. Cell Sci. 125, 1353-1362.
76. Wang, W. J., Soni, R. K., Uryu, K. and Tsou, M. F. (2011). The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 193, 727-739.
77. Wolff, A., de Néchaud, B., Chillet, D., Mazarguil, H., Desbruyères, E., Audebert, S., Eddé, B., Gros, F. and Denoulet, P. (1992). Distribution of glutamylated α and β-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur. J. Cell Biol. 59, 425-432.
78. Yan, X., Habedanck, R. and Nigg, E. A. (2006). A complex of two centrosomal proteins, CAP350 and FOP, cooperates with EB1 in microtubule anchoring. Mol. Biol. Cell 17, 634-644.