Mapping molecules to structure: Unveiling secrets of centriole and cilia assembly with near-atomic resolution

Current Opinion in Cell Biology

Volumn 26, Issue 1, 2014, Pages 96-106

  Jana, Swadhin Chandra ^a   Marteil, Gaëlle ^a   Bettencourt Dias, Mónica ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CELL COMPONENT; CELL ELONGATION; CELL MATURATION; CELL STRUCTURE; CENTRIOLE; CILIARY MOTILITY; EUKARYOTIC FLAGELLUM; HUMAN; MOLECULE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CENTRIOLES; CILIA; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROTUBULES; NANOSTRUCTURES; ORGANELLES;

EID: 84891056698     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2013.12.001     Document Type: Review

References (89)

1. Bettencourt-Dias M., Hildebrandt F., Pellman D., Woods G., Godinho S.A. Centrosomes and cilia in human disease. Trends Genet 2011, 27:307-315.
2. Carvalho-Santos Z., Azimzadeh J., Pereira-Leal J.B., Bettencourt-Dias M. Evolution: tracing the origins of centrioles, cilia, and flagella. J Cell Biol 2011, 194:165-175.
3. Cavalier-Smith T. Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci 1974, 16:529-556.
4. Allen R.D. The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J Cell Biol 1969, 40:716-733.
5. Dippell R.V. The development of basal bodies in paramecium. Proc Natl Acad Sci U S A 1968, 61:461-468.
6. Pelletier L., O'Toole E., Schwager A., Hyman A.A., Muller-Reichert T. Centriole assembly in Caenorhabditis elegans. Nature 2006, 444:619-623.
7. Paintrand M., Moudjou M., Delacroix H., Bornens M. Centrosome organization and centriole architecture: their sensitivity to divalent cations. J Struct Biol 1992, 108:107-128.
8. Ibrahim R., Messaoudi C., Chichon F.J., Celati C., Marco S. Electron tomography study of isolated human centrioles. Microsc Res Tech 2009, 72:42-48.
9. Reiter J.F., Blacque O.E., Leroux M.R. The base of the cilium: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentalization. EMBO Rep 2012, 13:608-618.
10. Guichard P., Chretien D., Marco S., Tassin A.M. Procentriole assembly revealed by cryo-electron tomography. EMBO J 2010, 29:1565-1572.
11. Carvalho-Santos Z., Machado P., Alvarez-Martins I., Gouveia S.M., Jana S.C., Duarte P., Amado T., Branco P., Freitas M.C., Silva S.T., et al. BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. Dev Cell 2012, 23:412-424.
12. Alvey P.L. Do adult centrioles contain cartwheels and lie at right angles to each other?. Cell Biol Int Rep 1986, 10:589-598.
13. Strnad P., Leidel S., Vinogradova T., Euteneuer U., Khodjakov A., Gonczy P. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev Cell 2007, 13:203-213.
14. 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.
15. Rodrigues-Martins A., Bettencourt-Dias M., Riparbelli M., Ferreira C., Ferreira I., Callaini G., Glover D.M. DSAS-6 organizes a tube-like centriole precursor, and its absence suggests modularity in centriole assembly. Curr Biol 2007, 17:1465-1472.
16. Bayless B.A., Giddings T.H., Winey M., Pearson C.G. Bld10/Cep135 stabilizes basal bodies to resist cilia-generated forces. Mol Biol Cell 2012, 23:4820-4832.
17. Guichard P., Desfosses A., Maheshwari A., Hachet V., Dietrich C., Brune A., Ishikawa T., Sachse C., Gonczy P. Cartwheel architecture of Trichonympha basal body. Science 2012, 337:553.
18. Guichard P., Hachet V., Majubu N., Neves A., Demurtas D., Olieric N., Fluckiger I., Yamada A., Kihara K., Nishida Y., et al. Native architecture of the centriole proximal region reveals features underlying its 9-fold radial symmetry. Curr Biol 2013.
19. Gopalakrishnan J., Guichard P., Smith A.H., Schwarz H., Agard D.A., Marco S., Avidor-Reiss T. Self-assembling SAS-6 multimer is a core centriole building block. J Biol Chem 2010, 285:8759-8760.
20. Sonnen K.F., Schermelleh L., Leonhardt H., Nigg E.A. 3D-structured illumination microscopy provides novel insight into architecture of human centrosomes. Biol Open 2012, 1:965-976.
21. Jana S.C., Bazan J.F., Bettencourt-Dias M. Polo boxes come out of the crypt: a new view of PLK function and evolution. Structure 2012, 20:1801-1810.
22. 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.
23. Jerka-Dziadosz M., Gogendeau D., Klotz C., Cohen J., Beisson J., Koll F. Basal body duplication in Paramecium: the key role of Bld10 in assembly and stability of the cartwheel. Cytoskeleton (Hoboken) 2010, 67:161-171.
24. Culver B.P., Meehl J.B., Giddings T.H., Winey M. The two SAS-6 homologs in Tetrahymena thermophila have distinct functions in basal body assembly. Mol Biol Cell 2009, 20:1865-1870.
25. 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.
26. Kitagawa D., Vakonakis I., Olieric N., Hilbert M., Keller D., Olieric V., Bortfeld M., Erat M.C., Fluckiger I., Gonczy P., et al. Structural basis of the 9-fold symmetry of centrioles. Cell 2011, 144:364-375.
27. 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.
28. 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.
29. Hiraki M., Nakazawa Y., Kamiya R., Hirono M. Bld10p constitutes the cartwheel-spoke tip and stabilizes the 9-fold symmetry of the centriole. Curr Biol 2007, 17:1778-1780.
30. Fu J., Glover D.M. Structured illumination of the interface between centriole and peri-centriolar material. Open Biol 2012, 2:120104.
31. Roque H., Wainman A., Richens J., Kozyrska K., Franz A., Raff J.W. Drosophila Cep135/Bld10 maintains proper centriole structure but is dispensable for cartwheel formation. J Cell Sci 2012, 125:5881-5890.
32. Lawo S., Hasegan M., Gupta G.D., Pelletier L. Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material. Nat Cell Biol 2012, 14:1148-1150.
33. Carvalho-Santos Z., Machado P., Branco P., Tavares-Cadete F., Rodrigues-Martins A., Pereira-Leal J.B., Bettencourt-Dias M. Stepwise evolution of the centriole-assembly pathway. J Cell Sci 2010, 123:1414-1420.
34. Gonczy P. Towards a molecular architecture of centriole assembly. Nat Rev Mol Cell Biol 2012, 13:425-435.
35. Gogendeau D., Hurbain I., Raposo G., Cohen J., Koll F., Basto R. Sas-4 proteins are required during basal body duplication in Paramecium. Mol Biol Cell 2011, 22:1035-1040.
36. 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.
37. 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, 30:4790-4800.
38. Pfaff K.L., Straub C.T., Chiang K., Bear D.M., Zhou Y., Zon L.I. The zebra fish cassiopeia mutant reveals that SIL is required for mitotic spindle organization. Mol Cell Biol 2007, 27:5887-5890.
39. Castiel A., Danieli M.M., David A., Moshkovitz S., Aplan P.D., Kirsch I.R., Brandeis M., Kramer A., Izraeli S. The Stil protein regulates centrosome integrity and mitosis through suppression of Chfr. J Cell Sci 2011, 124:532-539.
40. Leidel S., Delattre M., Cerutti L., Baumer K., Gonczy P. SAS-6 defines a protein family required for centrosome duplication in C. elegans and in human cells. Nat Cell Biol 2005, 7:115-125.
41. Hilbert M., Erat M.C., Hachet V., Guichard P., Blank I.D., Fluckiger I., Slater L., Lowe E.D., Hatzopoulos G.N., Steinmetz M.O., et al. Caenorhabditis elegans centriolar protein SAS-6 forms a spiral that is consistent with imparting a ninefold symmetry. Proc Natl Acad Sci U S A 2013, 110:11373-11378.
42. Li S., Fernandez J.J., Marshall W.F., Agard D.A. Three-dimensional structure of basal body triplet revealed by electron cryo-tomography. EMBO J 2011, 31:552-562.
43. Jana S.C., Machado P., Bettencourt-Dias M. A structural road map to unveil basal body composition and assembly. EMBO J 2012, 31:519-521.
44. Comartin D., Gupta G.D., Fussner E., Coyaud E., Hasegan M., Archinti M., Cheung S.W., Pinchev D., Lawo S., Raught B., et al. CEP120 and SPICE1 cooperate with CPAP in centriole elongation. Curr Biol 2013, 23:1360-1370.
45. Lin Y.N., Wu C.T., Lin Y.C., Hsu W.B., Tang C.J., Chang C.W., Tang T.K. CEP120 interacts with CPAP and positively regulates centriole elongation. J Cell Biol 2013, 202:211-219.
46. Brito D.A., Gouveia S.M., Bettencourt-Dias M. Deconstructing the centriole: structure and number control. Curr Opin Cell Biol 2012, 24:4-13.
47. Avidor-Reiss T., Gopalakrishnan J. Building a centriole. Curr Opin Cell Biol 2013, 25:72-77.
48. Tateishi K., Yamazaki Y., Nishida T., Watanabe S., Kunimoto K., Ishikawa H., Tsukita S. Two appendages homologous between basal bodies and centrioles are formed using distinct Odf2 domains. J Cell Biol 2013, 203:417-425.
49. Sillibourne J.E., Hurbain I., Grand-Perret T., Goud B., Tran P., Bornens M. Primary ciliogenesis requires the distal appendage component Cep123. Biol Open 2013, 2:535-545.
50. Wang W.J., Tay H.G., Soni R., Perumal G.S., Goll M.G., Macaluso F.P., Asara J.M., Amack J.D., Tsou M.F. CEP162 is an axoneme-recognition protein promoting ciliary transition zone assembly at the cilia base. Nat Cell Biol 2013, 15:591-601.
51. Fisch C., Dupuis-Williams P. Ultrastructure of cilia and flagella - back to the future!. Biol Cell 2011, 103:249-270.
52. Pazour G.J., Agrin N., Leszyk J., Witman G.B. Proteomic analysis of a eukaryotic cilium. J Cell Biol 2005, 170:103-113.
53. Keller L.C., Romijn E.P., Zamora I., Yates J.R., Marshall W.F. Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr Biol 2005, 15:1090-1100.
54. Gilula N.B., Satir P. The ciliary necklace. A ciliary membrane specialization. J Cell Biol 1972, 53:494-509.
55. Craige B., Tsao C.C., Diener D.R., Hou Y., Lechtreck K.F., Rosenbaum J.L., Witman G.B. CEP290 tethers flagellar transition zone microtubules to the membrane and regulates flagellar protein content. J Cell Biol 2010, 190:927-940.
56. Williams C.L., Li C., Kida K., Inglis P.N., Mohan S., Semenec L., Bialas N.J., Stupay R.M., Chen N., Blacque O.E., et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 2011, 192:1023-1030.
57. Schmidt K.N., Kuhns S., Neuner A., Hub B., Zentgraf H., Pereira G. Cep164 mediates vesicular docking to the mother centriole during early steps of ciliogenesis. J Cell Biol 2012, 199:1083-1090.
58. Sang L., Miller J.J., Corbit K.C., Giles R.H., Brauer M.J., Otto E.A., Baye L.M., Wen X., Scales S.J., Kwong M., et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011, 145:513-528.
59. Huang L., Szymanska K., Jensen V.L., Janecke A.R., Innes A.M., Davis E.E., Frosk P., Li C., Willer J.R., Chodirker B.N., et al. TMEM237 is mutated in individuals with a Joubert syndrome related disorder and expands the role of the TMEM family at the ciliary transition zone. Am J Hum Genet 2011, 89:713-730.
60. Ounjai P., Kim K.D., Liu H., Dong M., Tauscher A.N., Witkowska H.E., Downing K.H. Architectural insights into a ciliary partition. Curr Biol 2013, 23:339-344.
61. Zhang Y., Seo S., Bhattarai S., Bugge K., Searby C.C., Zhang Q., Drack A.V., Stone E.M., Sheffield V.C. BBS mutations modify phenotypic expression of CEP290-related ciliopathies. Hum Mol Genet 2013.
62. Chang B., Khanna H., Hawes N., Jimeno D., He S., Lillo C., Parapuram S.K., Cheng H., Scott A., Hurd R.E., et al. In-frame deletion in a novel centrosomal/ciliary protein CEP290/NPHP6 perturbs its interaction with RPGR and results in early-onset retinal degeneration in the rd16 mouse. Hum Mol Genet 2006, 15:1847-1850.
63. Nicastro D., Fu X., Heuser T., Tso A., Porter M.E., Linck R.W. Cryo-electron tomography reveals conserved features of doublet microtubules in flagella. Proc Natl Acad Sci U S A 2011, 108:E845-E853.
64. Sui H., Downing K.H. Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 2006, 442:475-478.
65. Pigino G., Maheshwari A., Bui K.H., Shingyoji C., Kamimura S., Ishikawa T. Comparative structural analysis of eukaryotic flagella and cilia from Chlamydomonas, Tetrahymena, and sea urchins. J Struct Biol 2012, 178:199-206.
66. Delgehyr N., Rangone H., Fu J., Mao G., Tom B., Riparbelli M.G., Callaini G., Glover D.M. Klp10A, a microtubule-depolymerizing kinesin-13, cooperates with CP110 to control Drosophila centriole length. Curr Biol 2012, 22:502-509.
67. Dawson S.C., Sagolla M.S., Mancuso J.J., Woessner D.J., House S.A., Fritz-Laylin L., Cande W.Z. Kinesin-13 regulates flagellar, interphase, and mitotic microtubule dynamics in Giardia intestinalis. Eukaryot Cell 2007, 6:2354-2360.
68. Chan K.Y., Ersfeld K. The role of the Kinesin-13 family protein TbKif13-2 in flagellar length control of Trypanosoma brucei. Mol Biochem Parasitol 2010, 174:137-140.
69. Piao T., Luo M., Wang L., Guo Y., Li D., Li P., Snell W.J., Pan J. A microtubule depolymerizing kinesin functions during both flagellar disassembly and flagellar assembly in Chlamydomonas. Proc Natl Acad Sci U S A 2009, 106:4713-4720.
70. Wang L., Piao T., Cao M., Qin T., Huang L., Deng H., Mao T., Pan J. Flagellar regeneration requires cytoplasmic microtubule depolymerization and kinesin-13. J Cell Sci 2013, 126:1531-1540.
71. Yamamoto R., Song K., Yanagisawa H.A., Fox L., Yagi T., Wirschell M., Hirono M., Kamiya R., Nicastro D., Sale W.S. The MIA complex is a conserved and novel dynein regulator essential for normal ciliary motility. J Cell Biol 2013, 201:263-278.
72. Pigino G., Ishikawa T. Axonemal radial spokes: 3D structure, function and assembly. Bioarchitecture 2012, 2:50-58.
73. King S.M. A solid-state control system for dynein-based ciliary/flagellar motility. J Cell Biol 2013, 201:173-175.
74. Lindemann C.B., Lesich K.A. Flagellar and ciliary beating: the proven and the possible. J Cell Sci 2010, 123:519-528.
75. Bui K.H., Yagi T., Yamamoto R., Kamiya R., Ishikawa T. Polarity and asymmetry in the arrangement of dynein and related structures in the Chlamydomonas axoneme. J Cell Biol 2012, 198:913-925.
76. Pigino G., Bui K.H., Maheshwari A., Lupetti P., Diener D., Ishikawa T. Cryoelectron tomography of radial spokes in cilia and flagella. J Cell Biol 2011, 195:673-687.
77. Barber C.F., Heuser T., Carbajal-Gonzalez B.I., Botchkarev V.V., Nicastro D. Three-dimensional structure of the radial spokes reveals heterogeneity and interactions with dyneins in Chlamydomonas flagella. Mol Biol Cell 2012, 23:111-120.
78. Kohno T., Wakabayashi K., Diener D.R., Rosenbaum J.L., Kamiya R. Subunit interactions within the Chlamydomonas flagellar spokehead. Cytoskeleton (Hoboken) 2011, 68:237-246.
79. Diener D.R., Yang P., Geimer S., Cole D.G., Sale W.S., Rosenbaum J.L. Sequential assembly of flagellar radial spokes. Cytoskeleton (Hoboken) 2011, 68:389-400.
80. Qin H., Diener D.R., Geimer S., Cole D.G., Rosenbaum J.L. Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J Cell Biol 2004, 164:255-266.
81. Smith E.F., Lefebvre P.A. PF16 encodes a protein with armadillo repeats and localizes to a single microtubule of the central apparatus in Chlamydomonas flagella. J Cell Biol 1996, 132:359-370.
82. Carbajal-Gonzalez B.I., Heuser T., Fu X., Lin J., Smith B.W., Mitchell D.R., Nicastro D. Conserved structural motifs in the central pair complex of eukaryotic flagella. Cytoskeleton (Hoboken) 2013, 70:101-120.
83. Smith E.F., Yang P. The radial spokes and central apparatus: mechano-chemical transducers that regulate flagellar motility. Cell Motil Cytoskeleton 2004, 57:8-17.
84. Ishikawa H., Thompson J., Yates J.R., Marshall W.F. Proteomic analysis of mammalian primary cilia. Curr Biol 2012, 22:414-419.
85. Mesland D.A., Hoffman J.L., Caligor E., Goodenough U.W. Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J Cell Biol 1980, 84:599-617.
86. Scholey J.M. Kinesin-2: a family of heterotrimeric and homodimeric motors with diverse intracellular transport functions. Annu Rev Cell Dev Biol 2013.
87. Jana S.C., Girotra M., Ray K. Heterotrimeric kinesin-II is necessary and sufficient to promote different stepwise assembly of morphologically distinct bipartite cilia in Drosophila antenna. Mol Biol Cell 2011, 22:769-781.
88. Kim J., Krishnaswami S.R., Gleeson J.G. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet 2008, 17:3796-3800.
89. Kobayashi T., Tsang W.Y., Li J., Lane W., Dynlacht B.D. Centriolar kinesin Kif24 interacts with CP110 to remodel microtubules and regulate ciliogenesis. Cell 2011, 145:914-925.