SAS-6 Assembly Templated by the Lumen of Cartwheel-less Centrioles Precedes Centriole Duplication

Developmental Cell

Volumn 30, Issue 2, 2014, Pages 238-245

  Fong, Chii Shyang ^a   Kim, Minhee ^a,b   Yang, T Tony ^c   Liao, Jung Chi ^c   Tsou, Meng Fu Bryan ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c INSTITUTE OF ATOMIC AND MOLECULAR SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CYCLE S PHASE; CENTRIOLE; MOLECULAR RECOGNITION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN SECRETION;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; CENTRIOLES; HUMANS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84904873297     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.05.008     Document Type: Article

References (41)

1. Anderson R.G., Brenner R.M. The formation of basal bodies (centrioles) in the Rhesus monkey oviduct. J. Cell Biol. 1971, 50:10-34.
2. Arquint C., Nigg E.A. STIL microcephaly mutations interfere with APC/C-mediated degradation and cause centriole amplification. Curr. Biol. 2014, 24:351-360.
3. Arquint C., Sonnen K.F., Stierhof Y.D., Nigg E.A. Cell-cycle-regulated expression of STIL controls centriole number in human cells. J. Cell Sci. 2012, 125:1342-1352.
4. Azimzadeh J., Wong M.L., Downhour D.M., Sánchez Alvarado A., Marshall W.F. Centrosome loss in the evolution of planarians. Science 2012, 335:461-463.
5. Cottee M.A., Raff J.W., Lea S.M., Roque H. SAS-6 oligomerization: the key to the centriole?. Nat. Chem. Biol. 2011, 7:650-653.
6. Cottee M.A., Muschalik N., Wong Y.L., Johnson C.M., Johnson S., Andreeva A., Oegema K., Lea S.M., Raff J.W., van Breugel M. Crystal structures of the CPAP/STIL complex reveal its role in centriole assembly and human microcephaly. eLife 2013, 2:e01071.
7. Donnert G., Keller J., Wurm C.A., Rizzoli S.O., Westphal V., Schönle A., Jahn R., Jakobs S., Eggeling C., Hell S.W. Two-color far-field fluorescence nanoscopy. Biophys. J. 2007, 92:L67-L69.
8. Firat-Karalar E.N., Rauniyar N., Yates J.R., Stearns T. Proximity interactions among centrosome components identify regulators of centriole duplication. Curr. Biol. 2014, 24:664-670.
9. Fry A.M., Mayor T., Meraldi P., Stierhof Y.D., Tanaka K., Nigg E.A. C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 1998, 141:1563-1574.
10. Ganem N.J., Godinho S.A., Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009, 460:278-282.
11. Guichard P., Desfosses A., Maheshwari A., Hachet V., Dietrich C., Brune A., Ishikawa T., Sachse C., Gönczy P. Cartwheel architecture of Trichonympha basal body. Science 2012, 337:553.
12. Hell S.W., Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 1994, 19:780-782.
13. Keller D., Orpinell M., Olivier N., Wachsmuth M., Mahen R., Wyss R., Hachet V., Ellenberg J., Manley S., Gönczy P. Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells. J. Cell Biol. 2014, 204:697-712.
14. Khodjakov A., Rieder C.L., Sluder G., Cassels G., Sibon O., Wang C.L. De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 2002, 158:1171-1181.
15. Kitagawa D., Vakonakis I., Olieric N., Hilbert M., Keller D., Olieric V., Bortfeld M., Erat M.C., Flückiger I., Gönczy P., Steinmetz M.O. Structural basis of the 9-fold symmetry of centrioles. Cell 2011, 144:364-375.
16. Klar T.A., Jakobs S., Dyba M., Egner A., Hell S.W. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl. Acad. Sci. USA 2000, 97:8206-8210.
17. Kleylein-Sohn J., Westendorf J., Le Clech M., Habedanck R., Stierhof Y.D., Nigg E.A. Plk4-induced centriole biogenesis in human cells. Dev. Cell 2007, 13:190-202.
18. La Terra S., English C.N., Hergert P., McEwen B.F., Sluder G., Khodjakov A. The de novo centriole assembly pathway in HeLa cells: cell cycle progression and centriole assembly/maturation. J. Cell Biol. 2005, 168:713-722.
19. Lettman M.M., Wong Y.L., Viscardi V., Niessen S., Chen S.H., Shiau A.K., Zhou H., Desai A., Oegema K. Direct binding of SAS-6 to ZYG-1 recruits SAS-6 to the mother centriole for cartwheel assembly. Dev. Cell 2013, 25:284-298.
20. Lin Y.C., Chang C.W., Hsu W.B., Tang C.J., Lin Y.N., Chou E.J., Wu C.T., Tang T.K. Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J. 2013, 32:1141-1154.
21. Mahjoub M.R., Stearns T. Supernumerary centrosomes nucleate extra cilia and compromise primary cilium signaling. Curr. Biol. 2012, 22:1628-1634.
22. Mayor T., Stierhof Y.D., Tanaka K., Fry A.M., Nigg E.A. The centrosomal protein C-Nap1 is required for cell cycle-regulated centrosome cohesion. J. Cell Biol. 2000, 151:837-846.
23. Mignot J.P. [New hypothesis on the replication of centrioles and basal bodies]. C. R. Acad. Sci. III 1996, 319:1093-1099.
24. Nakazawa Y., Hiraki M., Kamiya R., Hirono M. SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr. Biol. 2007, 17:2169-2174.
25. Puklowski A., Homsi Y., Keller D., May M., Chauhan S., Kossatz U., Grünwald V., Kubicka S., Pich A., Manns M.P., et al. The SCF-FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat. Cell Biol. 2011, 13:1004-1009.
26. Qiao R., Cabral G., Lettman M.M., Dammermann A., Dong G. SAS-6 coiled-coil structure and interaction with SAS-5 suggest a regulatory mechanism in C. elegans centriole assembly. EMBO J. 2012, 31:4334-4347.
27. Stevens N.R., Roque H., Raff J.W. DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev. Cell 2010, 19:913-919.
28. Strnad P., Leidel S., Vinogradova T., Euteneuer U., Khodjakov A., Gönczy P. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev. Cell 2007, 13:203-213.
29. Szollosi D., Calarco P., Donahue R.P. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J. Cell Sci. 1972, 11:521-541.
30. Tang C.J., Lin S.Y., Hsu W.B., Lin Y.N., Wu C.T., Lin Y.C., Chang C.W., Wu K.S., Tang T.K. The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J. 2011, 30:4790-4804.
31. Tikhonov A., Arsenin V. Solutions of Ill-Posed Problems 1977, Winston & Sons, Great Falls, MT.
32. Tsou M.F., Stearns T. Controlling centrosome number: licenses and blocks. Curr. Opin. Cell Biol. 2006, 18:74-78.
33. Tsou M.F., Stearns T. Mechanism limiting centrosome duplication to once per cell cycle. Nature 2006, 442:947-951.
34. Tsou M.F., Wang W.J., George K.A., Uryu K., Stearns T., Jallepalli P.V. Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev. Cell 2009, 17:344-354.
35. 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. Structures of SAS-6 suggest its organization in centrioles. Science 2011, 331:1196-1199.
36. Vladar E.K., Stearns T. Molecular characterization of centriole assembly in ciliated epithelial cells. J. Cell Biol. 2007, 178:31-42.
37. Vorobjev I.A., Chentsov Y.S. The ultrastructure of centriole in mammalian tissue culture cells. Cell Biol. Int. Rep. 1980, 4:1037-1044.
38. Vorobjev I.A., Chentsov YuS. Centrioles in the cell cycle. I. Epithelial cells. J. Cell Biol. 1982, 93:938-949.
39. Vulprecht J., David A., Tibelius A., Castiel A., Konotop G., Liu F., Bestvater F., Raab M.S., Zentgraf H., Izraeli S., Krämer A. STIL is required for centriole duplication in human cells. J. Cell Sci. 2012, 125:1353-1362.
40. Wang W.J., Soni R.K., Uryu K., Tsou M.F. The conversion of centrioles to centrosomes: essential coupling of duplication with segregation. J. Cell Biol. 2011, 193:727-739.
41. Yang T.T., Hampilos P.J., Nathwani B., Miller C.H., Sutaria N.D., Liao J.C. Superresolution STED microscopy reveals differential localization in primary cilia. Cytoskeleton (Hoboken) 2013, 70:54-65.