Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly

EMBO Journal

Volumn 32, Issue 8, 2013, Pages 1141-1154

  Lin, Yu Chih ^a   Chang, Ching Wen ^a   Hsu, Wen Bin ^a   Tang, Chieh Ju C ^a   Lin, Yi Nan ^a   Chou, En Ju ^a,b   Wu, Chien Ting ^a   Tang, Tang K ^a  

^a INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

cartwheel; CENPJ; centriole duplication; centrosome; microcephaly

Indexed keywords

CEP135 PROTEIN; CPAP PROTEIN; MUTANT PROTEIN; PROTEIN; SAS 6 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRIOLE; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL LINE; CENTRIOLES; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING;

EID: 84876416327     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.56     Document Type: Article

References (49)

1. 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
2. Azimzadeh J, Hergert P, Delouvee A, Euteneuer U, Formstecher E, Khodjakov A, Bornens M (2009) hPOC5 is a centrin-binding protein required for assembly of full-length centrioles. J Cell Biol 185: 101-114
3. Azimzadeh J, Marshall WF (2010) Building the centriole. Curr Biol 20: 816-825
4. Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA (2011) Centrosomes and cilia in human disease. Trends Genet 27: 307-315
5. 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
6. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J, Hampshire DJ, Morrison EE, Leal GF, Silva EO, Costa SM, Baralle D, Raponi M, Karbani G, Rashid Y, Jafri H, Bennett C, Corry P, Walsh CA, Woods CG (2005) A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37: 353-355
7. Brito DA, Gouveia SM, Bettencourt-Dias M (2012) Deconstructing the centriole: structure and number control. Curr Opin Cell Biol 24: 4-13
8. Carvalho-Santos Z, Machado P, Alvarez-Martins I, Gouveia SM, Jana SC, Duarte P, Amado T, Branco P, Freitas MC, Silva ST, Antony C, Bandeiras TM, Bettencourt-Dias M (2012) BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. Dev Cell 23: 412-424
9. Cizmecioglu O, Arnold M, Bahtz R, Settele F, Ehret L, Haselmann-Weiss U, Antony C, Hoffmann I (2010) Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J Cell Biol 191: 731-739
10. Delattre M, Canard C, Gonczy P (2006) Sequential protein recruitment in C. elegans centriole formation. Curr Biol 16: 1844-1849
11. Dobbelaere J, Josue 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 6: e224
12. Dzhindzhev NS, Yu QD, Weiskopf K, Tzolovsky G, Cunha-Ferreira I, Riparbelli M, Rodrigues-Martins A, Bettencourt-Dias M, Callaini G, Glover DM (2010) Asterless is a scaffold for the onset of centriole assembly. Nature 467: 714-718
13. Gonczy P (2012) Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13: 425-435
14. Guernsey DL, Jiang H, Hussin J, Arnold M, Bouyakdan K, Perry S, Babineau-Sturk T, Beis J, Dumas N, Evans SC, Ferguson M, Matsuoka M, Macgillivray C, Nightingale M, Patry L, Rideout AL, Thomas A, Orr A, Hoffmann I, Michaud JL et al (2010) Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am J Hum Genet 87: 40-51
15. Guichard P, Chretien D, Marco S, Tassin AM (2010) Procentriole assembly revealed by cryo-electron tomography. EMBO J 29: 1565-1572
16. Habedanck R, Stierhof YD, Wilkinson CJ, Nigg EA (2005) The Polo kinase Plk4 functions in centriole duplication. Nat Cell Biol 7: 1140-1146
17. 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
18. Hsu WB, Hung LY, Tang CJ, Su CL, Chang Y, Tang TK (2008) Functional characterization of the microtubule-binding and-destabilizing domains of CPAP and d-SAS-4. Exp Cell Res 314: 2591-2602
19. Hung LY, Chen HL, Chang CW, Li BR, 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: 2697-2706
20. 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
21. Hussain MS, Baig SM, Neumann S, Nurnberg G, Farooq M, Ahmad I, Alef T, Hennies HC, Technau M, Altmuller J, Frommolt P, Thiele H, Noegel AA, Nurnberg P (2012) A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am J Hum Genet 90: 871-878
22. 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 67: 161-171
23. Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, Bicknell LS, Kayserili H, Li Y, Tuysuz B, Nurnberg G, Kiess W, Koegl M, Baessmann I, Buruk K, Toraman B, Kayipmaz S, Kul S, Ikbal M, Turner DJ, Taylor MS et al (2011) CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat Genet 43: 23-26
24. 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
25. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, Bortfeld M, Erat MC, Fluckiger I, Gonczy P, Steinmetz MO (2011) Structural basis of the 9-fold symmetry of centrioles. Cell 144: 364-375
26. Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA (2007) Plk4-induced centriole biogenesis in human cells. Dev Cell 13: 190-202
27. 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
28. Kumar A, Girimaji SC, Duvvari MR, Blanton SH (2009) Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly. Am J Hum Genet 84: 286-290
29. Kuriyama R, Borisy GG (1981) Centriole cycle in Chinese hamster ovary cells as determined by whole-mount electron microscopy. J Cell Biol 91 : 814-821
30. 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
31. 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
32. Matsuura K, Lefebvre PA, Kamiya R, 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
33. 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
34. 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
35. Nigg EA, Stearns T (2011) The centrosome cycle: centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol 13: 1154-1160
36. 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
37. Ohta T, Essner R, Ryu JH, 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: 87-99
38. 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
39. Pelletier L, O'Toole E, Schwager A, Hyman AA, Muller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444: 619-623
40. Rodrigues-Martins A, Bettencourt-Dias M, Riparbelli M, Ferreira C, Ferreira I, Callaini G, Glover DM (2007) DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 17: 1465-1472
41. Roque H, Wainman A, Richens J, Kozyrska K, Franz A, Raff JW (2013) Drosophila Cep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation. J Cell Sci 125(Pt 23): 5881-5886
42. Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB, Stierhof YD, Nigg EA (2009) Control of centriole length by CPAP and CP110. Curr Biol 19: 1005-1011
43. Singla V, Romaguera-Ros M, Garcia-Verdugo JM, Reiter JF (2010) Ofd1, a human disease gene, regulates the length and distal structure of centrioles. Dev Cell 18: 410-424
44. Sir JH, Barr AR, Nicholas AK, Carvalho OP, Khurshid M, Sossick A, Reichelt S, D'Santos C, Woods CG, Gergely F (2011) A primary microcephaly protein complex forms a ring around parental centrioles. Nat Genet 43: 1147-1153
45. 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
46. 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
47. Thornton GK, Woods CG (2009) Primary microcephaly: do all roads lead to Rome? Trends Genet 25: 501-510
48. 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
49. Vulprecht J, David A, Tibelius A, Castiel A, Konotop G, Liu F, Bestvater F, Raab MS, Zentgraf H, Izraeli S, Kramer A (2012) STIL is required for centriole duplication in human cells. J Cell Sci 125: 1353-1362