Structure of the SAS-6 cartwheel hub from Leishmania major

eLife

Volumn 2014, Issue 3, 2014, Pages

  van Breugel, Mark ^a   Wilcken, Rainer ^a,b   McLaughlin, Stephen H ^a   Rutherford, Trevor J ^a   Johnson, Christopher M ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; SAS 6; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN;

AFRICAN TRYPANOSOMIASIS; ARTICLE; CENTRIOLE; CRYSTALLIZATION; DIMERIZATION; EUKARYOTIC FLAGELLUM; GEL PERMEATION CHROMATOGRAPHY; GENE MUTATION; HUMAN; IN VITRO STUDY; LEISHMANIA MAJOR; LEISHMANIASIS; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; POINT MUTATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TRYPANOSOMA; ULTRACENTRIFUGATION; X RAY ANALYSIS; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

CENTRIOLES; CRYSTALLOGRAPHY, X-RAY; LEISHMANIA MAJOR; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTOZOAN PROTEINS;

EID: 84898737594     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01812     Document Type: Article

References (57)

1. Afonine PV, Grosse-Kunstleve RW, Adams PD. 2005. The phenix refinement framework. CCP4 Newsletter 42.
2. Anglister J, Grzesiek S, Ren H, Klee CB, Bax A. 1993. Isotope-edited multidimensional NMR of calcineurin B in the presence of the non-deuterated detergent CHAPS. Journal of Biomolecular NMR 3:121-126. doi: 10.1007/BF00242480.
3. Avasthi P, Marshall WF. 2012. Stages of ciliogenesis and regulation of ciliary length. Differentiation Research in Biological Diversity 83:S30-S42. doi: 10.1016/j.diff.2011.11.015.
4. Azimzadeh J, Marshall WF. 2010. Building the centriole. Current Biology: CB 20:R816-R825. doi: 10.1016/j.cub.2010.08.010.
5. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Böhme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, Macleod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J, Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El-Sayed NM. 2005. The genome of the African trypanosome Trypanosoma brucei. Science (New York, NY) 309:416-422. doi: 10.1126/science.1112642.
6. Bettencourt-Dias M, Glover DM. 2007. Centrosome biogenesis and function: centrosomics brings new understanding. Nature Reviews Molecular Cell Biology 8:451-463. doi: 10.1038/nrm2180.
7. Blachon S, Cai X, Roberts KA, Yang K, Polyanovsky A, Church A, Avidor-Reiss T. 2009. A proximal centriole-like structure is present in Drosophila spermatids and can serve as a model to study centriole duplication. Genetics 182:133-144. doi: 10.1534/genetics.109.101709.
8. Brito DA, Gouveia SM, Bettencourt-Dias M. 2012. Deconstructing the centriole: structure and number control. Current Opinion in Cell Biology 24:4-13. doi: 10.1016/j.ceb.2012.01.003.
9. Carvalho-Santos Z, Machado P, Branco P, Tavares-Cadete F, Rodrigues-Martins A, Pereira-Leal JB, Bettencourt-Dias M. 2010. Stepwise evolution of the centriole-assembly pathway. Journal of Cell Science 123:1414-1426. doi: 10.1242/jcs.064931.
10. Chemes HE. 2012. Sperm centrioles and their dual role in flagellogenesis and cell cycle of the zygote. In Schatten H, editor. The centrosome cell and molecular mechanisms of functions and Dysfunctions in disease. New York, NY: Humana Press. p33-48.
11. Cowtan K. 2006. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallographica Section D Biological Crystallography 62:1002-1011. doi: 10.1107/S0907444906022116.
12. Cowtan K. 2008. Fitting molecular fragments into electron density. Acta Crystallographica Section D Biological Crystallography 64:83-89. doi: 10.1107/S0907444907033938.
13. 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. The Journal of Cell Biology 180:771-785. doi: 10.1083/jcb.200709102.
14. Dawe HR, Farr H, Gull K. 2007. Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. Journal of Cell Science 120:7-15. doi: 10.1242/jcs.03305.
15. de Vries SJ, van Dijk M, Bonvin AM. 2010. The HADDOCK web server for data-driven biomolecular docking. Nature Protocols 5:883-897. doi: 10.1038/nprot.2010.32.
16. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science (New York, NY) 309:409-415. doi: 10.1126/science.1112631.
17. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallographica Section D Biological Crystallography 60:2126-2132. doi: 10.1107/S0907444904019158.
18. Evans P. 2006. Scaling and assessment of data quality. Acta Crystallographica Section D Biological Crystallography 62:72-82. doi: 10.1107/S0907444905036693.
19. Evans PR, Murshudov GN. 2013. How good are my data and what is the resolution? Acta Crystallographica Section D Biological Crystallography 69:1204-1214. doi: 10.1107/S0907444913000061.
20. Field MC, Carrington M. 2004. Intracellular membrane transport systems in Trypanosoma brucei. Traffic (Copenhagen, Denmark) 5:905-913. doi: 10.1111/j.1600-0854.2004.00234.x.
21. Field MC, Carrington M. 2009. The trypanosome flagellar pocket. Nature Rviews Microbiology 7:775-786. doi: 10.1038/nrmicro2221.
22. Gluenz E, Ginger ML, McKean PG. 2010. Flagellum assembly and function during the Leishmania life cycle. Current Opinion in Microbiology 13:473-479. doi: 10.1016/j.mib.2010.05.008.
23. Gonczy P. 2012. Towards a molecular architecture of centriole assembly. Nature Reviews Molecular Cell Biology 13:425-435. doi: 10.1038/nrm3373.
24. 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. The Journal of Biological Chemistry 285:8759-8770. doi: 10.1074/jbc.M109.092627.
25. Guichard P, Chretien D, Marco S, Tassin AM. 2010. Procentriole assembly revealed by cryo-electron tomography. The EMBO Journal 29:1565-1572. doi: 10.1038/emboj.2010.45.
26. 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 (New York, NY) 337:553. doi: 10.1126/science.1222789.
27. Guichard P, Hachet V, Majubu N, Neves A, Demurtas D, Olieric N, Fluckiger I, Yamada A, Kihara K, Nishida Y, Moriya S, Steinmetz MO, Hongoh Y, Gönczy P. 2013. Native architecture of the centriole proximal region reveals features underlying its 9-fold radial symmetry. Current Biology: CB 23:1620-1628. doi: 10.1016/j.cub.2013.06.061.
28. Hodges ME, Scheumann N, Wickstead B, Langdale JA, Gull K. 2010. Reconstructing the evolutionary history of the centriole from protein components. Journal of Cell Science 123:1407-1413. doi: 10.1242/jcs.064873.
29. Ishikawa H, Marshall WF. 2011. Ciliogenesis: building the cell's antenna. Nature Reviews Molecular Cell Biology 12:222-234. doi: 10.1038/nrm3085.
30. Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Müller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O'neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schäfer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science (New York, NY) 309:436-442. doi: 10.1126/science.1112680.
31. Kabsch W. 2010. XDS. Acta Crystallographica Section D Biological Crystallography 66:125-132. doi: 10.1107/S0907444909047337.
32. 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. doi: 10.1016/j.cell.2011.01.008.
33. Kleylein-Sohn J, Westendorf J, Le Clech M, Habedanck R, Stierhof YD, Nigg EA. 2007. Plk4-induced centriole biogenesis in human cells. Developmental Cell 13:190-202. doi: 10.1016/j.devcel.2007.07.002.
34. Lacomble S, Vaughan S, Gadelha C, Morphew MK, Shaw MK, McIntosh JR, Gull K. 2009. Three-dimensional cellular architecture of the flagellar pocket and associated cytoskeleton in trypanosomes revealed by electron microscope tomography. Journal of Cell Science 122:1081-1090. doi: 10.1242/jcs.045740.
35. Landfear SM, Ignatushchenko M. 2001. The flagellum and flagellar pocket of trypanosomatids. Molecular and Biochemical Parasitology 115:1-17. doi: 10.1016/S0166-6851(01)00262-6.
36. Leslie AGW, Powell HR. 2007. Processing diffraction data with Mosflm. Evolving Methods for Macromolecular Crystallography 245:41-51. doi: 10.1007/978-1-4020-6316-9_4.
37. Lettman MM, Wong YL, Viscardi V, Niessen S, Chen SH, Shiau AK, Zhou H, Desai A, Oegema K. 2013. Direct binding of SAS-6 to ZYG-1 recruits SAS-6 to the mother centriole for cartwheel assembly. Developmental Cell 25:284-298. doi: 10.1016/j.devcel.2013.03.011.
38. Lin YC, Chang CW, Hsu WB, Tang CJ, Lin YN, Chou EJ, Wu CT, Tang TK. 2013. Human microcephaly protein CEP135 binds to hSAS-6 and CPAP, and is required for centriole assembly. The EMBO Journal 32:1141-1154. doi: 10.1038/emboj.2013.56.
39. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallograpy 40:658-674. doi: 10.1107/S0021889807021206.
40. Mori S, Abeygunawardana C, Johnson MO, van Zijl PC. 1995. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. Journal of Magnetic Resonance Series B 108:94-98. doi: 10.1006/jmrb.1995.1109.
41. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. 2011. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallographica Section D Biological Crystallography 67:355-367. doi: 10.1107/S0907444911001314.
42. Nakazawa Y, Hiraki M, Kamiya R, Hirono M. 2007. SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Current Biology: CB 17:2169-2174. doi: 10.1016/j.cub.2007.11.046.
43. Overath P, Engstler M. 2004. Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Molecular Microbiology 53:735-744. doi: 10.1111/j.1365-2958.2004.04224.x.
44. Overath P, Stierhof YD, Wiese M. 1997. Endocytosis and secretion in trypanosomatid parasites-Tumultuous traffic in a pocket. Trends in Cell Biology 7:27-33. doi: 10.1016/S0962-8924(97)10046-0.
45. Pape T, Schneider TR. 2004. HKL2MAP: a graphical user interface for phasing with SHELX programs. Journal of Applied Crystallogrophy 37:843-844. doi: 10.1107/S0021889804018047.
46. Ralston KS, Kabututu ZP, Melehani JH, Oberholzer M, Hill KL. 2009. The Trypanosoma brucei flagellum: moving parasites in new directions. Annual Review of Microbiology 63:335-362. doi: 10.1146/annurev.micro.091208.073353.
47. Schuck P. 2003. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Analytical Biochemistry 320:104-124. doi: 10.1016/S0003-2697(03)00289-6.
48. Sherwin T, Gull K. 1989. The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations. Philosophical transactions of the Royal Society of London Series B Biological Sciences 323:573-588. doi: 10.1098/rstb.1989.0037.
49. Simpson AG, Stevens JR, Lukes J. 2006. The evolution and diversity of kinetoplastid flagellates. Trends in Parasitology 22:168-174. doi: 10.1016/j.pt.2006.02.006.
50. Sonnen KF, Schermelleh L, Leonhardt H, Nigg EA. 2012. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biology Open 1:965-976. doi: 10.1242/bio.20122337.
51. Stevens NR, Dobbelaere J, Brunk K, Franz A, Raff JW. 2010. Drosophila Ana2 is a conserved centriole duplication factor. The Journal of Cell Biology 188:313-323. doi: 10.1083/jcb.200910016.
52. Strnad P, Leidel S, Vinogradova T, Euteneuer U, Khodjakov A, Gonczy P. 2007. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Developmental Cell 13:203-213. doi: 10.1016/j.devcel.2007.07.004.
53. 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. The EMBO Journal 30:4790-4804. doi: 10.1038/emboj.2011.378.
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 (New York, NY) 331:1196-1199. doi: 10.1126/science.1199325.
55. Vaughan S, Gull K. 2003. The trypanosome flagellum. Journal of Cell Science 116:757-759. doi: 10.1242/jcs.00287.
56. Wassenaar TA, van Dijk M, Loureiro-Ferreira N, van der Schot G, de Vries SJ, Schmitz C, van der Zwan J, Boelens R, Giachetti A, Ferella L, Rosato A, Bertini I, Herrmann T, Jonker HRA, Bagaria A, Jaravine V, Güntert P, Schwalbe H, Vranken WF, Doreleijers JF, Vriend G, Vuister GW, Franke D, Kikhney A, Svergun DI, Fogh RH, Ionides J, Laue ED, Spronk C, Jurkša S, Verlato M, Badoer S, Dal Pra S, Mazzucato M, Frizziero E, Bonvin AMJJ. 2012. WeNMR: structural biology on the grid. Journal of Grid Computing 10:743-767. doi: 10.1007/s10723-012-9246-z.
57. Wilcken R, Liu X, Zimmermann MO, Rutherford TJ, Fersht AR, Joerger AC, Boeckler FM. 2012. Halogen-enriched fragment libraries as leads for drug rescue of mutant p53. Journal of the American Chemical Society 134:6810-6818. doi: 10.1021/ja301056a.