SAS-6 coiled-coil structure and interaction with SAS-5 suggest a regulatory mechanism in C. elegans centriole assembly

EMBO Journal

Volumn 31, Issue 22, 2012, Pages 4334-4347

  Qiao, Renping ^a   Cabral, Gabriela ^b   Lettman, Molly M ^c   Dammermann, Alexander ^b   Dong, Gang ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Centriole; crystallography; SAS 5; SAS 6; structure

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; SAS 5 PROTEIN; SAS 6 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CARBOXY TERMINAL SEQUENCE; CENTRIOLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; HYDROPHOBICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CENTRIOLES; CRYSTALLOGRAPHY, X-RAY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

CAENORHABDITIS ELEGANS;

EID: 84869236675     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.280     Document Type: Article

References (55)

1. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426:570-574 (Pubitemid 37522644)
2. Arquint C, Sonnen KF, Stierhof YD, Nigg EA (2012) Cell-cycle-regulated expression of STIL controls centriole number in human cells. J Cell Sci 125:1342-1352
3. Azimzadeh J, Marshall WF (2010) Building the centriole. Curr Biol 20: R816-R825
4. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW (2006) Flies without centrioles. Cell 125:1375-1386 (Pubitemid 43929089)
5. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67:271-281
6. Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA (2011) Centrosomes and cilia in human disease. Trends Genet 27:307-315
7. 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 15:2199-2207 (Pubitemid 41790613)
8. Boxem M, Maliga Z, Klitgord N, Li N, Lemmens I, Mana M, de Lichtervelde L, Mul JD, van de Peut D, Devos M, Simonis N, Yildirim MA, Cokol M, Kao HL, de Smet AS, Wang H, Schlaitz AL, Hao T, Milstein S, Fan C et al (2008) A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134:534-545
9. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905-921
10. Castiel A, Danieli MM, David A, Moshkovitz S, Aplan PD, Kirsch IR, Brandeis M, Kramer A, Izraeli S (2011) The Stil protein regulates centrosome integrity and mitosis through suppression of Chfr. J Cell Sci 124:532-539
11. Cottee MA, Raff JW, Lea SM, Roque H (2011) SAS-6 oligomerization: the key to the centriole? Nat Chem Biol 7:650-653
12. Dammermann A, Maddox PS, Desai A, Oegema K (2008) SAS-4 is recruited to a dynamic structure in newly forming centrioles that is stabilized by the gamma-tubulin-mediated addition of centriolar microtubules. J Cell Biol 180:771-785 (Pubitemid 351397777)
13. Dammermann A, Muller-Reichert T, Pelletier L, Habermann B, Desai A, Oegema K (2004) Centriole assembly requires both centriolar and pericentriolar material proteins. Dev Cell 7:815-829 (Pubitemid 39654727)
14. Delattre M, Canard C, Gonczy P (2006) Sequential protein recruitment in C. elegans centriole formation. Curr Biol 16:1844-1849 (Pubitemid 44354142)
15. Delattre M, Gonczy P (2004) The arithmetic of centrosome biogenesis. J Cell Sci 117:1619-1630
16. Delattre M, Leidel S, Wani K, Baumer K, Bamat J, Schnabel H, Feichtinger R, Schnabel R, Gonczy P (2004) Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat Cell Biol 6:656-664 (Pubitemid 38960924)
17. Doublie S (1997) Preparation of selenomethionyl proteins for phase determination. Methods Enzymol 276:523-530 (Pubitemid 27085620)
18. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-2132 (Pubitemid 41742764)
19. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62:72-82
20. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, Grunnet M, Jorgensen EM (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40:1375-1383
21. Gopalakrishnan J, Guichard P, Smith AH, Schwarz H, Agard DA, Marco S, Avidor-Reiss T (2010) Self-assembling SAS-6 multimer is a core centriole building block. J Biol Chem 285:8759-8770
22. Gopalakrishnan J, Mennella V, Blachon S, Zhai B, Smith AH, Megraw TL, Nicastro D, Gygi SP, Agard DA, Avidor-Reiss T (2011) Sas-4 provides a scaffold for cytoplasmic complexes and tethers them in a centrosome. Nat Commun 2:359
23. Guichard P, Desfosses A, Maheshwari A, Hachet V, Dietrich C, Brune A, Ishikawa T, Sachse C, Gonczy P (2012) Cartwheel architecture of Trichonympha basal body. Science 337:553
24. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7:1140-1146
25. 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 17:1778-1783 (Pubitemid 47576667)
26. 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 20:7813-7825
27. Kemp CA, Kopish KR, Zipperlen P, Ahringer J, O'Connell KF (2004) Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev Cell 6:511-523 (Pubitemid 38456180)
28. Kirkham M, Muller-Reichert T, Oegema K, Grill S, Hyman AA (2003) SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112:575-587 (Pubitemid 36263088)
29. Kitagawa D, Busso C, Fluckiger I, Gonczy P (2009) Phosphorylation of SAS-6 by ZYG-1 is critical for centriole formation in C. elegans embryos. Dev Cell 17:900-907
30. Kitagawa D, Fluckiger I, Polanowska J, Keller D, Reboul J, Gonczy P (2011a) PP2A phosphatase acts upon SAS-5 to ensure centriole formation in C. elegans embryos. Dev Cell 20:550-562
31. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Fluckiger I, Gonczy P, Steinmetz MO (2011b) Structural basis of the 9-fold symmetry of centrioles. Cell 144:364-375
32. Kohlmaier G, Loncarek J, Meng X, McEwen BF, Mogensen MM, Spektor A, Dynlacht BD, Khodjakov A, Gonczy P (2009) Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr Biol 19:1012-1018
33. Kozakov D, Hall DR, Beglov D, Brenke R, Comeau SR, Shen Y, Li K, Zheng J, Vakili P, Paschalidis ICh., Vajda S (2010) Achieving reliability and high accuracy in automated protein docking: ClusPro, PIPER, SDU, and stability analysis in CAPRI rounds 13-19. Proteins 78:3124-3130
34. Leidel S, Delattre M, Cerutti L, Baumer K, Gonczy P (2005) SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat Cell Biol 7:115-125 (Pubitemid 40268126)
35. Leidel S, Gonczy P (2003) SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle. Dev Cell 4:431-439 (Pubitemid 36342367)
36. Leidel S, Gonczy P (2005) Centrosome duplication and nematodes: recent insights from an old relationship. Dev Cell 9:317-325 (Pubitemid 41235802)
37. Lovatt M, Cooper A, Camilleri P (1996) Energetics of cyclodextrin-induced dissociation of insulin. Eur Biophys J 24:354-357 (Pubitemid 26290951)
38. Marshall WF (2001) Centrioles take center stage. Curr Biol 11: R487-R496
39. Mottier-Pavie V, Megraw TL (2009) Drosophila bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol Biol Cell 20:2605-2614
40. Nakazawa Y, Hiraki M, Kamiya R, Hirono M (2007) SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr Biol 17:2169-2174 (Pubitemid 50014863)
41. Nigg EA, Raff JW (2009) Centrioles, centrosomes, and cilia in health and disease. Cell 139:663-678
42. O'Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, Li Y, White JG (2001) The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105:547-558 (Pubitemid 32520859)
43. Peel N, Stevens NR, Basto R, Raff JW (2007) Overexpressing centriole-replication proteins in vivo induces centriole overdupli-cation and de novo formation. Curr Biol 17:834-843 (Pubitemid 46702671)
44. Pelletier L, O'Toole E, Schwager A, Hyman AA, Muller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444:619-623 (Pubitemid 44864439)
45. Pelletier L, Ozlu N, Hannak E, Cowan C, Habermann B, Ruer M, Muller-Reichert T, Hyman AA (2004) The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr Biol 14:863-873 (Pubitemid 38800907)
46. Preble AM, Giddings Jr TM, Dutcher SK (2000) Basal bodies and centrioles: their function and structure. Curr Top Dev Biol 49:207-233
47. Sibanda BL, Critchlow SE, Begun J, Pei XY, Jackson SP, Blundell TL, Pellegrini L (2001) Crystal structure of an Xrcc4-DNA ligase IV complex. Nat Struct Biol 8:1015-1019 (Pubitemid 33101619)
48. Song MH, Liu Y, Anderson DE, Jahng WJ, O'Connell KF (2011) Protein phosphatase 2A-SUR-6/B55 regulates centriole duplication in C. elegans by controlling the levels of centriole assembly factors. Dev Cell 20:563-571
49. Stevens NR, Dobbelaere J, Brunk K, Franz A, Raff JW (2010a) Drosophila Ana2 is a conserved centriole duplication factor. J Cell Biol 188:313-323
50. Stevens NR, Roque H, Raff JW (2010b) DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev Cell 19:913-919
51. Tang CJ, Fu RH, Wu KS, Hsu WB, Tang TK (2009) CPAP is a cell-cycle regulated protein that controls centriole length. Nat Cell Biol 11:825-831
52. Tang CJ, Lin SY, Hsu WB, Lin YN, Wu CT, Lin YC, Chang CW, Wu KS, Tang TK (2011) The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J 30:4790-4804
53. Terwilliger TC, Adams PD, Read RJ, McCoy AJ, Moriarty NW, Grosse-Kunstleve RW, Afonine PV, Zwart PH, Hung LW (2009) Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard. Acta Crystallogr D Biol Crystallogr 65:582-601
54. van Breugel M, Hirono M, Andreeva A, Yanagisawa HA, Yamaguchi S, Nakazawa Y, Morgner N, Petrovich M, Ebong IO, Robinson CV, Johnson CM, Veprintsev D, Zuber B (2011) Structures of SAS-6 suggest its organization in centrioles. Science 331:1196-1199
55. Vulprecht J, David A, Tibelius A, Castiel A, Konotop G, Liu F, Bestvater F, Raab MS, Zentgraf H, Izraeli S, Krämer A (2012) STIL is required for centriole duplication in human cells. J Cell Sci 125(Part 5):1353-1362