Two classes of short intraflagellar transport train with different 3D structures are present in Chlamydomonas flagella

Journal of Cell Science

Volumn 129, Issue 10, 2016, Pages 2064-2074

  Vannuccini, Elisa ^a   Paccagnini, Eugenio ^a   Cantele, Francesca ^b   Gentile, Mariangela ^a   Dini, Daniele ^a   Fino, Federica ^a   Diener, Dennis ^c   Mencarelli, Caterina ^a   Lupetti, Pietro ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c YALE UNIVERSITY   (United States)

Author keywords

Chlamydomonas flagella; Electron tomography; Flagellar regeneration; Intraflagellar transport

Indexed keywords

ARTICLE; CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII; ELECTRON TOMOGRAPHY; FLAGELLUM; INTRAFLAGELLAR TRANSPORT; LONGITUDINAL STUDY; NONHUMAN; OBSERVATIONAL STUDY; PRIORITY JOURNAL; ULTRASTRUCTURE; AXONEME; CILIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN TRANSPORT; REGENERATION; TRANSPORT AT THE CELLULAR LEVEL;

AXONEME; BIOLOGICAL TRANSPORT; CHLAMYDOMONAS; CILIA; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; PROTEIN TRANSPORT; REGENERATION;

EID: 84971006859     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.183244     Document Type: Article

References (85)

1. Absalon, S., Blisnick, T., Kohl, L., Toutirais, G., Dore, G., Julkowska, D., Tavenet, A. and Bastin, P. (2008). Intraflagellar transport and functional analysis of genes required for flagellum formation in Trypanosomes. Mol. Biol. Cell 19, 929-944.
2. Avidor-Reiss, T., Maer, A. M., Koundakjian, E., Polyanovsky, A., Keil, T., Subramaniam, S. and Zuker, C. S. (2004). Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117, 527-539.
3. Badano, J. L., Mitsuma, N., Beales, P. L. and Katsanis, N. (2006). The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148.
4. Berbari, N. F., Lewis, J. S., Bishop, G. A., Askwith, C. C. and Mykytyn, K. (2008). Bardet-Biedl syndrome proteins are required for the localization of G proteincoupled receptors to primary cilia. Proc. Natl. Acad. Sci. USA 105, 4242-4246.
5. Bhogaraju, S., Taschner, M., Morawetz, M., Basquin, C. and Lorentzen, E. (2011). Crystal structure of the intraflagellar transport complex 25/27. EMBO J. 30, 1907-1918.
6. Bhogaraju, S., Cajanek, L., Fort, C., Blisnick, T., Weber, K., Taschner, M., Mizuno, N., Lamla, S., Bastin, P., Nigg, E. A. et al. (2013). Molecular basis of tubulin transport within the cilium by IFT74 and IFT81. Science 341, 1009-1012.
7. Buisson, J., Chenouard, N., Lagache, T., Blisnick, T., Olivo-Marin, J.-C. and Bastin, P. (2013). Intraflagellar transport proteins cycle between the flagellum and its base. J. Cell Sci. 126, 327-338.
8. Cantele, F., Paccagnini, E., Pigino, G., Lupetti, P. and Lanzavecchia, S. (2010). Simultaneous alignment of dual-axis tilt series. J. Struct. Biol. 169, 192-199.
9. Cao, M., Meng, D., Wang, L., Bei, S., Snell, W. J. and Pan, J. (2013). Activation loop phosphorylation of a protein kinase is a molecular marker of organelle size that dynamically reports flagellar length. Proc. Natl. Acad. Sci. USA 110, 12337-12342.
10. Cole, D. G. (2003). The Intraflagellar Transport machinery of Chlamydomonas reinhardtii. Traffic 4, 435-442.
11. Cole, D. G., Diener, D. R., Himelblau, A. L., Beech, P. L., Fuster, C. J. and Rosenbaum, J. L. (1998). Chlamydomonas Kinesin-II-dependent Intraflagellar Transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J. Cell Biol. 141, 993-1008.
12. Craft, J. M., Harris, J. A., Hyman, S., Kner, P. and Lechtreck, K. F. (2015). Tubulin transport by IFT is upregulated during ciliary growth by a cilium-autonomous mechanism. J. Cell Biol. 208, 223-237.
13. Deane, J. A., Cole, D. G., Seeley, E. S., Diener, D. R. and Rosenbaum, J. L. (2001). Localization of intraflagellar transport protein IFT52 identifies basal body transitional fibers as the docking site for IFT particles. Curr. Biol. 11, 1586-1590.
14. Dentler, W. (2005). Intraflagellar transport (IFT) during assembly and disassembly of Chlamydomonas flagella. J. Cell Biol. 170, 649-659.
15. Dutta-Simmons, J., Zhang, Y., Gourgun, G., Gatt, M., Mani, M., Hideshima, T., Takada, K., Carlson, N. E., Carrasco, D. E., Tai, Y.-T. et al. (2009). Aurora kinase A is a target of Wnt/beta-catenin involved in multiple myeloma disease progression. Blood 114, 2699-2708.
16. Engel, B. D., Ludington, W. B. and Marshall, W. F. (2009). Intraflagellar transport particle size scales inversely with flagellar length: revisiting the balance-point length control model. J. Cell Biol. 187, 81-89.
17. Engel, B. D., Ishikawa, H., Wemmer, K. A., Geimer, S., Wakabayashi, K.-i., Hirono, M., Craige, B., Pazour, G. J., Witman, G. B., Kamiya, R. et al. (2012). The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function. J. Cell Biol. 199, 151-167.
18. Follit, J. A., Tuft, R. A., Fogarty, K. E. and Pazour, G. J. (2006). The Intraflagellar Transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17, 3781-3792.
19. Follit, J. A., Xu, F., Keady, B. T. and Pazour, G. J. (2009). Characterization of mouse IFT complex B. Cell. Motil. Cytoskeleton 66, 457-468.
20. Fry, A. M., Leaper, M. J. and Bayliss, R. (2014). The primary cilium: guardian of organ development and homeostasis. Organogenesis 10, 62-68.
21. Geimer, S. (2009). Immunogold labeling of flagellar components in situ. Methods Cell Biol. 91, 63-80.
22. Hao, L., Efimenko, E., Swoboda, P. and Scholey, J. M. (2011). The retrograde IFT machinery of C. elegans cilia: two IFT dynein complexes? PLoS ONE 6, e20995.
23. Hilton, L. K., Gunawardane, K., Kim, J. W., Schwarz, M. C. and Quarmby, L. M. (2013). The kinases LF4 and CNK2 control ciliary length by feedback regulation of assembly and disassembly rates. Curr. Biol. 23, 2208-2214.
24. Hou, Y., Qin, H., Follit, J. A., Pazour, G. J., Rosenbaum, J. L. and Witman, G. B. (2007). Functional analysis of an individual IFT protein: IFT46 is required for transport of outer dynein arms into flagella. J. Cell Biol. 176, 653-665.
25. Huang, K., Diener, D. R., Mitchell, A., Pazour, G. J., Witman, G. B. and Rosenbaum, J. L. (2007). Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. J. Cell Biol. 179, 509-514.
26. Iomini, C., Babaev-Khaimov, V., Sassaroli, M. and Piperno, G. (2001). Protein particles in Chlamydomonas flagella undergo a transport cycle consisting of four phases. J. Cell Biol. 153, 13-24.
27. Iomini, C., Li, L., Esparza, J. M. and Dutcher, S. K. (2009). Retrograde intraflagellar transport mutants identify complex A proteins with multiple genetic interactions in Chlamydomonas reinhardtii. Genetics 183, 885-896.
28. Ishikawa, H., Ide, T., Yagi, T., Jiang, X., Hirono, M., Sasaki, H., Yanagisawa, H., Wemmer, K. A., Stainier, D. Y., Qin, H. et al. (2014). TTC26/DYF13 is an intraflagellar transport protein required for transport of motility-related proteins into flagella. eLife 1, e01566.
29. Johnson, K. A. and Rosenbaum, J. L. (1992). Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 119, 1605-1611.
30. Kozminski, K. G., Johnson, K. A., Forscher, P. and Rosenbaum, J. L. (1993). A motility in the eukaryotic flagellum unrelated to flagellar beating. Cell Biol. 90, 5519-5523.
31. Kozminski, K. G., Beech, P. L. and Rosenbaum, J. R. (1995). The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131, 1517-1527.
32. Kubo, T., Yanagisawa, H.-a., Yagi, T., Hirono, M. and Kamiya, R. (2010). Tubulin polyglutamylation regulates axonemal motility by modulating activities of innerarm dyneins. Curr. Biol. 20, 441-445.
33. Kubo, T., Yagi, T. and Kamiya, R. (2012). Tubulin polyglutamylation regulates flagellar motility by controlling a specific inner-arm dynein that interacts with the dynein regulatory complex. Cytoskeleton 69, 1059-1068.
34. Kucukelbir, A., Sigworth, F. J. and Tagare, H. D. (2014). Quantifying the local resolution of cryo-EM density maps. Nat. Methods 11, 63-65.
35. Lechtreck, K.-F., Johnson, E. C., Sakai, T., Cochran, D., Ballif, B. A., Rush, J., Pazour, G. J., Ikebe, M. and Witman, G. B. (2009). The Chlamydomonas reinhardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J. Cell Biol. 187, 1117-1132.
36. Lechtreck, K. F., Brown, J. M., Sampaio, J. L., Craft, J. M., Shevchenko, A., Evans, J. E. and Witman, G. B. (2013). Cycling of the signaling protein phospholipase D through cilia requires the BBSome only for the export phase. J. Cell Biol. 201, 249-261.
37. Lefebvre, P. A. (1995). Flagellar amputation and regeneration in Chlamydomonas. Methods Cell Biol. 47, 3-7.
38. Li, B. J., Gerdes, J. M., Haycraft, C. J., Fan, Y., Teslovich, T. M., May-Simera, H., Li, H., Blacque, O. E., Li, L., Leitch, C. C. et al. (2004). Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117, 541-552.
39. Liang, Y., Pang, Y., Wu, Q., Hu, Z., Han, X., Xu, Y., Deng, H. and Pan, J. (2014). FLA8/KIF3B phosphorylation regulates kinesin-II interaction with IFT-B to control IFT entry and turnaround. Dev. Cell 30, 585-597.
40. Loktev, A. V., Zhang, Q., Beck, J. S., Searby, C. C., Scheetz, T. E., Bazan, J. F., Slusarski, D. C., Sheffield, V. C., Jackson, P. K. and Nachury, M. V. (2008). A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev. Cell 15, 854-865.
41. Ludington,W. B.,Wemmer, K. A., Lechtreck, K. F.,Witman, G. B. and Marshall, W. F. (2013). Avalanche-like behavior in ciliary import. Proc. Natl. Acad. Sci. USA 110, 3925-3930.
42. Luo, M., Cao, M., Kan, Y., Li, G., Snell,W. and Pan, J. (2011). The phosphorylation state of an aurora-like kinase marks the length of growing flagella in Chlamydomonas. Curr. Biol. 21, 586-591.
43. Madhivanan, K. and Aguilar, R. C. (2014). Ciliopathies: the trafficking connection. Traffic 15, 1031-1056.
44. Marshall, W. F. and Rosenbaum, J. L. (2001). Intraflagellar transport balances continuous turnover of outer doublet microtubules: implications for flagellar length control. J. Cell Biol. 155, 405-414.
45. Marshall, W. F., Qin, H., Rodrigo Brenni, M. and Rosenbaum, J. L. (2005). Flagellar length control system: testing a simple model based on intraflagellar transport and turnover. Mol. Biol. Cell 16, 270-278.
46. Mencarelli, C., Mitchell, A., Leoncini, R., Rosenbaum, J. and Lupetti, P. (2013). Isolation of intraflagellar transport trains. Cytoskeleton 70, 439-452.
47. Mukhopadhyay, S., Wen, X., Chih, B., Nelson, C. D., Lane, W. S., Scales, S. J. and Jackson, P. K. (2010). TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes Dev. 24, 2180-2193
48. Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, J., Peränen, J., Merdes, A., Slusarski, D. C., Sheller, R. H., Bazan, J. F., Sheffield, V. C. et al. (2007). A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129, 1201-1213.
49. Ou, G., Blacque, O. E., Snow, J. J., Leroux, M. R. and Scholey, J. M. (2005). Functional coordination of intraflagellar transport motors. Nature 436, 583-587.
50. Pan, J.,Wang, Q. and Snell,W. J. (2004). An aurora kinase is essential for flagellar disassembly in Chlamydomonas. Dev. Cell 6, 445-451.
51. Pan, J., Seeger-Nukpezah, T. and Golemis, E. A. (2013). The role of the cilium in normal and abnormal cell cycles: emphasis on renal cystic pathologies. Cell. Mol. Life Sci. 70, 1849-1874.
52. Pazour, G. J., Wilkerson, C. G. and Witman, G. B. (1998). A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J. Cell Biol. 141, 979-992.
53. Pazour, G. J., Dickert, B. L. and Witman, G. B. (1999). The DHC1b (DHC2) isoform of cytoplasmic dynein is required for flagellar assembly. J. Cell Biol. 144, 473-481.
54. Pazour, G. J., Dickert, B. L., Vucica, Y., Seeley, E. S., Rosenbaum, J. L.,Witman, G. B. and Cole, D. G. (2000). Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene Tg737, are required for assembly of cilia and flagella. J. Cell Biol. 151, 709-718.
55. Pedersen, L. B., Geimer, S. and Rosenbaum, J. L. (2006). Dissecting the molecular mechanisms of intraflagellar transport in Chlamydomonas. Curr. Biol. 16, 450-459.
56. Pigino, G., Geimer, S., Lanzavecchia, S., Paccagnini, E., Cantele, F., Diener, D. R. Rosenbaum, J. L. and Lupetti, P. (2009). Electron-tomographic analysis of intraflagellar transport particle trains in situ. J. Cell Biol. 187, 135-148.
57. Porter, M. E., Bower, R., Knott, J. A., Byrd, P. and Dentler, W. (1999). Cytoplasmic dynein heavy chain 1b is required for flagellar assembly in Chlamydomonas. Mol. Biol. Cell 10, 693-712.
58. Qin, H., Diener, D. R., Geimer, S., Cole, D. G. and Rosenbaum, J. L. (2004). Intraflagellar transport (IFT) cargo: IFT transports flagellar precursors to the tip and turnover products to the cell body. J. Cell Biol. 164, 255-266.
59. Qin, H., Burnette, D. T., Bae, Y.-K., Forscher, P., Barr, M. M. and Rosenbaum, J. L. (2005). Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr. Biol. 15, 1695-1699.
60. Rampolas, P., Pedersen, L. B., Patel-King, R. S. and King, S. K. (2007). Chlamydomonas FAP133 is a dynein intermediate chain associated with the retrograde intraflagellar transport motor. J. Cell Sci. 120, 3653-3665.
61. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
62. Rosenbaum, J. L. and Child, F. M. (1967). Flagellar regeneration in protozoan flagellates. J. Cell Biol. 34, 345-364.
63. Rosenbaum, J. L., Moulder, J. E. and Ringo, D. L. (1969). Flagellar elongation and shortening in Chlamydomonas: the use of cycloheximide and colchicine to study the synthesis and assembly of flagellar proteins. J. Cell Biol. 41, 600-619.
64. Sager, R. and Granick, S. (1953). Nutritional studies with Chlamydomonas reinhardii. Ann. N. Y. Acad. Sci. 56, 831-838.
65. Salvi, E., Cantele, F., Zampighi, L., Fain, N., Pigino, G., Zampighi, G. and Lanzavecchia, S. (2008). JUST (Java User Segmentation Tool) for semiautomatic segmentation of tomographic maps. J. Struct. Biol. 161, 287-297.
66. Seo, S., Guo, D.-F., Bugge, K., Morgan, D. A., Rahmouni, K. and Sheffield, V. C. (2009). Requirement of Bardet-Biedl syndrome proteins for leptin receptor signaling. Hum. Mol. Genet. 18, 1323-1331.
67. Silva, D. A., Huang, X., Behal, R. H., Cole, D. G. and Qin, H. (2012). The RABL5 homolog IFT22 regulates the cellular pool size and the amount of IFT particles partitioned to the flagellar compartment in Chlamydomonas reinhardtii. Cytoskeleton 69, 33-48.
68. Snow, J. J., Ou, G., Gunnarson, A. L., Walker, M. R., Zhou, H. M., Brust- Mascher, I. and Scholey, J. M. (2004). Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat. Cell Biol. 6, 1109-1113.
69. Su, X., Driscoll, K., Yao, G., Raed, A., Wu, M., Beales, P. L. and Zhou, J. (2014). Bardet-Biedl syndrome proteins 1 and 3 regulate the ciliary trafficking of polycystic kidney disease 1 protein. Hum. Mol. Genet. 23, 5441-5451.
70. Suryavanshi, S., Eddé, B., Fox, L. A., Guerrero, S., Hard, R., Hennessey, T., Kabi, A., Malison, D., Pennock, D., Sale, W. S. et al. (2010). Tubulin glutamylation regulates ciliary motility by altering inner dynein arm activity. Curr. Biol. 20, 435-440.
71. Taschner, M., Bhogaraju, S., Vetter, M., Morawetz, M. and Lorentzen, E. (2011). Biochemical mapping of interactions within the intraflagellar transport (IFT) B core complex: IFT52 binds directly to four other IFT-B subunits. J. Biol. Chem. 286, 26344-26352.
72. Taschner, M., Kotsis, F., Brauer, P., Kuehn, E.W. and Lorentzen, E. (2014). Crystal structures of IFT70/52 and IFT52/46 provide insight into intraflagellar transport B core complex asembly. J. Cell Biol. 207, 269-282.
73. Taschner, M., Bhogaraju, S. and Lorentzen, E. (2012). Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 83, S12-S22.
74. Thoma, C. R., Frew, I. J., Hoerner, C. R., Montani, M., Moch, H. and Krek, W. (2007). pVHL and GSK3beta are components of a primary cilium-maintenance signalling network. Nat. Cell Biol. 9, 588-595.
75. Torisawa, T., Ichikawa, M., Furuta, A., Saito, K., Oiwa, K., Kojima, H., Toyoshima, Y. Y. and Furuta, K. (2014). Autoinhibition and cooperative activation mechanisms of cytoplasmic dynein. Nat. Cell Biol. 16, 1118-1124.
76. Tsao, C.-C. and Gorovsky, M. A. (2008). Different effects of Tetrahymena IFT172 domains on anterograde and retrograde intraflagellar transport. Mol. Cell. Biol. 19, 1450-1461.
77. van Heel, M. and Schatz, M. (2005). Fourier shell correlation threshold criteria. J. Struct. Biol. 151, 250-262.
78. Vashishtha, M., Walther, Z. and Hall, J. L. (1996). The kinesin-homologous protein encoded by the Chlamydomonas FLA10 gene is associated with basal bodies and centrioles. J. Cell Sci. 109, 541-549.
79. Viswanadha, R., Hunter, E. L., Yamamoto, R., Wirschell, M., Alford, L. M., Dutcher, S. K. and Sale, W. S. (2014). The ciliary inner dynein arm, I1 dynein, is assembled in the cytoplasm and transported by IFT before axonemal docking. Cytoskeleton 71, 573-586.
80. Walther, Z., Vashishtha, M. and Hall, J. L. (1994). The Chlamydomonas FLA10 gene encodes a novel kinesin-homologous protein. J. Cell Biol. 126, 175-188.
81. Wei, Q., Zhang, Y., Li, Y., Zhang, Q., Ling, K. and Hu, J. (2012). The BBSome controls IFT assembly and turnaround in cilia. Nat. Cell Biol. 14, 950-957.
82. Wei, Q., Xu, Q., Zhang, Y., Li, Y., Zhang, Q., Hu, Z., Harris, P. C., Torres, V. E., Ling, K. and Hu, J. (2013). Transition fibre protein FBF1 is required for the ciliary entry of assembled intraflagellar transport complexes. Nat. Commun. 4, 2750.
83. Wilson, N. F. and Lefebvre, P. A. (2004). Regulation of flagellar assembly by glycogen synthase kinase 3 in Chlamydomonas reinhardtii. Eukaryot. Cell 3, 1307-1319.
84. Wood, C. R. and Rosenbaum, J. L. (2014). Proteins of the ciliary axoneme are found on cytoplasmic membrane vesicles during growth of cilia. Curr. Biol. 24, 1114-1120.
85. Wren, K. N., Craft, J. M., Tritschler, D., Schauer, A., Patel, D. K., Smith, E. F., Porter, M., Kner, P. and Lechtreck, K. F. (2013). A differential cargo-loading model of ciliary length regulation by IFT. Curr. Biol. 23, 2463-2471.