Crystal structures of the CPAP/STIL complex reveal its role in centriole assembly and human microcephaly

eLife

Volumn 2013, Issue 2, 2013, Pages

  Cottee, Matthew A ^a   Muschalik, Nadine ^a   Wong, Yao Liang ^b   Johnson, Christopher M ^c   Johnson, Steven ^a   Andreeva, Antonina ^c   Oegema, Karen ^b   Lea, Susan M ^a   Raff, Jordan W ^a   van Breugel, Mark ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CPAP PROTEIN; MEMBRANE PROTEIN; STIL PROTEIN; UNCLASSIFIED DRUG; CENPJ PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; PROLINE; SIGNAL PEPTIDE; STIL PROTEIN, HUMAN;

AMINO ACID ANALYSIS; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CENTRIOLE; CIRCULAR DICHROISM; CONTROLLED STUDY; CRYSTALLIZATION; DROSOPHILA MELANOGASTER; EMBRYO; GEL PERMEATION CHROMATOGRAPHY; GENE MUTATION; IMMUNOHISTOCHEMISTRY; ISOTHERMAL TITRATION CALORIMETRY; MICROCEPHALY; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; TIME LAPSE IMAGING; WESTERN BLOTTING; ZEBRA FISH; BINDING SITE; CHEMISTRY; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; POINT MUTATION; PROTEIN CONFORMATION;

BINDING SITES; CENTRIOLES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROCEPHALY; MICROTUBULE-ASSOCIATED PROTEINS; POINT MUTATION; PROLINE; PROTEIN CONFORMATION;

EID: 84884683290     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01071     Document Type: Article

References (84)

1. Abrahams JP, Leslie AG. 1996. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr D Biol Crystallogr 52:30-42. doi: 10.1107/S0907444995008754.
2. Afonine PV, Grosse-Kunstleve RW, Adams PD. 2005. The Phenix refinement framework. CCP4 Newsletter 42. http://www.ccp4.ac.uk/newsletters/newsletter42/content.html.
3. Al-Dosari MS, Shaheen R, Colak D, Alkuraya FS. 2010. Novel CENPJ mutation causes Seckel syndrome. J Med Genet 47:411-4. doi: 10.1136/jmg.2009.076646.
4. Arquint C, Sonnen KF, Stierhof YD, Nigg EA. 2012. Cell-cycle-regulated expression of STIL controls centriole number in human cells. J Cell Sci 125:1342-52. doi: 10.1242/jcs.099887.
5. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, et al. 2006. Flies without centrioles. Cell 125:1375-86. doi: 10.1016/j.cell.2006.05.025.
6. Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA. 2011. Centrosomes and cilia in human disease. Trends Genet 27:307-15. doi: 10.1016/j.tig.2011.05.004.
7. Blachon S, Cai X, Roberts KA, Yang K, Polyanovsky A, Church A, et al. 2009. A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 182:133-44. doi: 10.1534/genetics.109.101709.
8. Bond J, Roberts E, Springell K, Lizarraga SB, Scott S, Higgins J, et al. 2005. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat Genet 37:353-5. doi: 10.1038/ng1539.
9. Bricogne GBE, Brandl M, Flensburg C, Keller P, Paciorek W, Roversi PSA, et al. 2011. BUSTER version 2.11.4.
10. Brito DA, Gouveia SM, Bettencourt-Dias M. 2012. Deconstructing the centriole: structure and number control. Curr Opin Cell Biol 24:4-13. doi: 10.1016/j.ceb.2012.01.003.
11. Chothia C. 1973. Conformation of twisted β-pleated sheets in proteins. J Mol Biol 75:295-302. doi: 10.1016/0022-2836(73)90022-3.
12. Cizmecioglu O, Arnold M, Bahtz R, Settele F, Ehret L, Haselmann-Weiss U, et al. 2010. Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome. J Cell Biol 191:731-9. doi: 10.1083/jcb.201007107.
13. Conduit PT, Brunk K, Dobbelaere J, Dix CI, Lucas EP, Raff JW. 2010. Centrioles regulate centrosome size by controlling the rate of Cnn incorporation into the PCM. Curr Biol 20:2178-86. doi: 10.1016/j.cub.2010.11.011.
14. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62:1002-11. doi: 10.1107/S0907444906022116.
15. 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 180:771-85. doi: 10.1083/jcb.200709102.
16. Darvish H, Esmaeeli-Nieh S, Monajemi GB, Mohseni M, Ghasemi-Firouzabadi S, Abedini SS, et al. 2010. A clinical and molecular genetic study of 112 Iranian families with primary microcephaly. J Med Genet 47:823-8. doi: 10.1136/jmg.2009.076398.
17. 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. doi: 10.1371/journal.pbio.0060224.
18. Dzhindzhev NS, Yu QD, Weiskopf K, Tzolovsky G, Cunha-Ferreira I, Riparbelli M, et al. 2010. Asterless is a scaffold for the onset of centriole assembly. Nature 467:714-8. doi: 10.1038/nature09445.
19. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126-32. doi: 10.1107/S0907444904019158.
20. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62:72-82. doi: 10.1107/S0907444905036693.
21. Frøkjær-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, Olesen SP, et al. 2008. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40:1375-83. doi: 10.1038/ng.248.
22. Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, Martz E, et al. 2003. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19:163-4. doi: 10.1093/bioinformatics/19.1.163.
23. Gonczy P. 2012. Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 13:425-35. doi: 10.1038/nrm3373.
24. Gul A, Hassan MJ, Hussain S, Raza SI, Chishti MS, Ahmad W. 2006. A novel deletion mutation in CENPJ gene in a Pakistani family with autosomal recessive primary microcephaly. J Hum Genet 51:760-4. doi: 10.1007/s10038-006-0017-1.
25. Han YG, Alvarez-Buylla A. 2010. Role of primary cilia in brain development and cancer. Curr Opin Neurobiol 20:58-67. doi: 10.1016/j.conb.2009.12.002.
26. Hatch EM, Kulukian A, Holland AJ, Cleveland DW, Stearns T. 2010. Cep152 interacts with Plk4 and is required for centriole duplication. J Cell Biol 191:721-9. doi: 10.1083/jcb.201006049.
27. 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 17:1778-83. doi: 10.1016/j.cub.2007.09.021.
28. 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 314:2591-602. doi: 10.1016/j.yexcr.2008.05.012.
29. 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 20:7813-25. doi: 10.1128/MCB.20.20.7813-7825.2000.
30. Hussain MS, Baig SM, Neumann S, Nurnberg G, Farooq M, Ahmad I, et al. 2012. A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am J Hum Genet 90:871-8. doi: 10.1016/j.ajhg.2012.03.016.
31. Islam SD, Pilder SH, Decker CL, Cebra-Thomas JA, Silver LM. 1993. The human homolog of a candidate mouse t complex responder gene: conserved motifs and evolution with punctuated equilibria. Hum Mol Genet 2:2075-9. doi: 10.1093/hmg/2.12.2075.
32. Kalay E, Yigit G, Aslan Y, Brown KE, Pohl E, Bicknell LS, et al. 2011. CEP152 is a genome maintenance protein disrupted in Seckel syndrome. Nat Genet 43:23-6. doi: 10.1038/ng.725.
33. Kay BK, Williamson MP, Sudol M. 2000. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14:231-41.
34. Kernan M, Cowan D, Zuker C. 1994. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195-206. doi: 10.1016/0896-6273(94)90437-5.
35. Kim MK, Dudognon C, Smith S. 2012. Tankyrase 1 regulates centrosome function by controlling CPAP stability. EMBO Rep 13:724-32. doi: 10.1038/embor.2012.86.
36. 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 112:575-87. doi: 10.1016/S0092-8674(03)00117-X.
37. Kitagawa D, Kohlmaier G, Keller D, Strnad P, Balestra FR, Fluckiger I, et al. 2011a. Spindle positioning in human cells relies on proper centriole formation and on the microcephaly proteins CPAP and STIL. J Cell Sci 124:3884-93. doi: 10.1242/jcs.089888.
38. Kitagawa D, Vakonakis I, Olieric N, Hilbert M, Keller D, Olieric V, et al. 2011b. Structural basis of the 9-fold symmetry of centrioles. Cell 144:364-75. doi: 10.1016/j.cell.2011.01.008.
39. 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. doi: 10.1016/j.devcel.2007.07.002.
40. Kohlmaier G, Loncarek J, Meng X, McEwen BF, Mogensen MM, Spektor A, et al. 2009. Overly long centrioles and defective cell division upon excess of the SAS-4-related protein CPAP. Curr Biol 19:1012-8. doi: 10.1016/j.cub.2009.05.018.
41. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: a windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36:1277-82. doi: 10.1107/S0021889803012779.
42. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3:1171-9. doi: 10.1038/nprot.2008.91.
43. Leal GF, Roberts E, Silva EO, Costa SM, Hampshire DJ, Woods CG. 2003. A novel locus for autosomal recessive primary microcephaly (MCPH6) maps to 13q12.2. J Med Genet 40:540-2. doi: 10.1136/jmg.40.7.540.
44. Lee HS, Simon JA, Lis JT. 1988. Structure and expression of ubiquitin genes of Drosophila melanogaster. Mol Cell Biol 8:4727-35.
45. 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 4:431-9. doi: 10.1016/S1534-5807(03)00062-5.
46. Leslie AGW, Powell HR. 2007. Processing diffraction data with Mosflm. Evolving methods for macromolecular crystallography. 245:41-51.
47. Leung GC, Hudson JW, Kozarova A, Davidson A, Dennis JW, Sicheri F. 2002. The Sak polo-box comprises a structural domain sufficient for mitotic subcellular localization. Nat Struct Biol 9:719-24. doi: 10.1038/nsb848.
48. Lin YC, Chang CW, Hsu WB, Tang CJ, Lin YN, Chou EJ, et al. 2013. Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. EMBO J 32:1141-54. doi: 10.1038/emboj.2013.56.
49. Lucas EP, Raff JW. 2007. Maintaining the proper connection between the centrioles and the pericentriolar matrix requires Drosophila centrosomin. J Cell Biol 178:725-32. doi: 10.1083/jcb.200704081.
50. Lukinavičius G, Lavogina D, Orpinell M, Umezawa K, Reymond L, Garin N, et al. 2013. Selective chemical crosslinking reveals a Cep57-Cep63-Cep152 centrosomal complex. Curr Biol 23:265-70. doi: 10.1016/j.cub.2012.12.030.
51. Makabe K, McElheny D, Tereshko V, Hilyard A, Gawlak G, Yan S, et al. 2006. Atomic structures of peptide self-assembly mimics. Proc Natl Acad Sci USA 103:17753-8. doi: 10.1073/pnas.0606690103.
52. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr 40:658-74. doi: 10.1107/S0021889807021206.
53. McIntyre RE, Lakshminarasimhan Chavali P, Ismail O, Carragher DM, Sanchez-Andrade G, Forment JV, et al. 2012. Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLOS Genet 8:e1003022. doi: 10.1371/journal.pgen.1003022.
54. Megraw TL, Sharkey JT, Nowakowski RS. 2011. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol 21:470-80. doi: 10.1016/j.tcb.2011.04.007.
55. Mennella V, Keszthelyi B, McDonald KL, Chhun B, Kan F, Rogers GC, et al. 2012. Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization. Nat Cell Biol 14:1159-68. doi: 10.1038/ncb2597.
56. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, et al. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 67:355-67. doi: 10.1107/S0907444911001314.
57. Murzin AG. 1992. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 14:191-201. doi: 10.1002/prot.340140206.
58. 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 17:2169-74. doi: 10.1016/j.cub.2007.11.046.
59. Ness SR, de Graaff RA, Abrahams JP, Pannu NS. 2004. CRANK: new methods for automated macromolecular crystal structure solution. Structure 12:1753-61. doi: 10.1016/j.str.2004.07.018.
60. Nigg EA, Raff JW. 2009. Centrioles, centrosomes, and cilia in health and disease. Cell 139:663-78. doi: 10.1016/j.cell.2009.10.036.
61. O'Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, Li Y, et al. 2001. The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105:547-58. doi: 10.1016/S0092-8674(01)00338-5.
62. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA. 2001. Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153:1209-26. doi: 10.1083/jcb.153.6.1209.
63. Pelletier L, O'Toole E, Schwager A, Hyman AA, Müller-Reichert T. 2006. Centriole assembly in Caenorhabditis elegans. Nature 444:619-23. doi: 10.1038/nature05318.
64. Qiao R, Cabral G, Lettman MM, Dammermann A, Dong G. 2012. SAS-6 coiled-coil structure and interaction with SAS-5 suggest a regulatory mechanism in C. elegans centriole assembly. EMBO J 31:4334-47. doi: 10.1038/emboj.2012.280.
65. Roque H, Wainman A, Richens J, Kozyrska K, Franz A, Raff JW. 2012. Drosophila Cep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation. J Cell Sci 125:5881-6. doi: 10.1242/jcs.113506.
66. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676-82. doi: 10.1038/nmeth.2019.
67. Schmidt TI, Kleylein-Sohn J, Westendorf J, Le Clech M, Lavoie SB, Stierhof YD, et al. 2009. Control of centriole length by CPAP and CP110. Curr Biol 19:1005-11. doi: 10.1016/j.cub.2009.05.016.
68. Sheldrick GM. 2008. A short history of SHELX. Acta Crystallogr A 64:112-22. doi: 10.1107/S0108767307043930.
69. Siller KH, Doe CQ. 2009. Spindle orientation during asymmetric cell division. Nat Cell Biol 11:365-74. doi: 10.1038/ncb0409-365.
70. Slevin LK, Nye J, Pinkerton DC, Buster DW, Rogers GC, Slep KC. 2012. The structure of the plk4 cryptic polo box reveals two tandem polo boxes required for centriole duplication. Structure 20:1905-17. doi: 10.1016/j.str.2012.08.025.
71. Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA. 2012. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 1:965-76. doi: 10.1242/bio.20122337.
72. Stein N. 2008. CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J Appl Cryst 41:641-3. doi: 10.1107/S0021889808006985.
73. Stevens NR, Dobbelaere J, Brunk K, Franz A, Raff JW. 2010a. Drosophila Ana2 is a conserved centriole duplication factor. J Cell Biol 188:313-23. doi: 10.1083/jcb.200910016.
74. Stevens NR, Dobbelaere J, Wainman A, Gergely F, Raff JW. 2009. Ana3 is a conserved protein required for the structural integrity of centrioles and basal bodies. J Cell Biol 187:355-63. doi: 10.1083/jcb.200905031.
75. Stevens NR, Roque H, Raff JW. 2010b. DSas-6 and Ana2 coassemble into tubules to promote centriole duplication and engagement. Dev Cell 19:913-9. doi: 10.1016/j.devcel.2010.11.010.
76. Svergun DI, Barberato C, Koch MHJ. 1995. CRYSOL-a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Cryst 28:768-73. doi: 10.1107/S0021889895007047.
77. 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 11:825-31. doi: 10.1038/ncb1889.
78. Tang CJ, Lin SY, Hsu WB, Lin YN, Wu CT, Lin YC, et al. 2011. The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J 30:4790-804. doi: 10.1038/emboj.2011.378.
79. Thornton GK, Woods CG. 2009. Primary microcephaly: do all roads lead to Rome? Trends Genet 25:501-10. doi: 10.1016/j.tig.2009.09.011.
80. van Breugel M, Hirono M, Andreeva A, Yanagisawa HA, Yamaguchi S, Nakazawa Y, et al. 2011. Structures of SAS-6 suggest its organization in centrioles. Science 331:1196-9. doi: 10.1126/science.1199325.
81. Vonrhein C, Blanc E, Roversi P, Bricogne G. 2007. Automated structure solution with autoSHARP. Methods Mol Biol 364:215-30. doi: 10.1385/1-59745-266-1:215.
82. Vulprecht J, David A, Tibelius A, Castiel A, Konotop G, Liu F, et al. 2012. STIL is required for centriole duplication in human cells. J Cell Sci 125:1353-62. doi: 10.1242/jcs.104109.
83. Wang C, Li S, Januschke J, Rossi F, Izumi Y, Garcia-Alvarez G, et al. 2011. An ana2/ctp/mud complex regulates spindle orientation in Drosophila neuroblasts. Dev Cell 21:520-33. doi: 10.1016/j.devcel.2011.08.002.
84. Winter G. 2010. xia2: an expert system for macromolecular crystallography data reduction. J Appl Cryst 43:186-90. doi: 10.1107/S0021889809045701.