Sensory ciliogenesis in Caenorhabditis elegans: Assignment of IFT components into distinct modules based on transport and phenotypic profiles

Molecular Biology of the Cell

Volumn 18, Issue 5, 2007, Pages 1554-1569

  Ou, Guangshuo ^a   Koga, Makato ^b   Blacque, Oliver E ^c,d   Murayama, Takashi ^b   Ohshima, Yasumi ^b   Schafer, Jenny C ^e   Li, Chunmei ^c   Yoder, Bradley K ^e   Leroux, Michel R ^c   Scholey, Jonathan M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c SIMON FRASER UNIVERSITY   (Canada)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TRANSPORT; WILD TYPE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL TRANSPORT, ACTIVE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CILIA; GENES, HELMINTH; GREEN FLUORESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; RECOMBINANT FUSION PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 34248214629     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-09-0805     Document Type: Article

References (72)

1. Ansley, S. J. et al. (2003). Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425, 628-633.
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. Genom. Hum. Genet. 7, 125-148.
4. Baker, S. A., Freeman, K., Luby-Phelps, K., Pazour, G. J., and Besharse, J. C. (2003). IFT20 links kinesin II with a mammalian intraflagellar transport complex that is conserved in motile flagella and sensory cilia. J. Biol. Chem. 278, 34211-34218.
5. Bargmann, C.a.M.I. (1997). Chemotaxis and thermotaxis. In: C. elegans II, ed. T.B.D.L. Riddle, B. J. Meyer, and J. R. Priess, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 717-737.
6. Bell, L.R., Stone, S., Yochem, J., Shaw, J. E., and Herman, R. K. (2006). The molecular identities of the Caenorhabditis elegans intraflagellar transport genes dyf-6, daf-10 and osm-1. Genetics 173, 1275-1286.
7. Blacque, O. E., and Leroux, M. R. (2006). Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport. Cell Mol. Life Sci. 63, 2145-2161.
8. Blacque, O. E., Li, C., Inglis, P. N., Esmail, M. A., Ou, G., Mah, A. K., Baillie, D. L., Scholey, J. M., and Leroux, M. R. (2006). The WD repeat-containing protein, IFTA-1, is required for retrograde intraflagellar transport. Mol. Biol. Cell 17, 5053-5062.
9. Blacque, O. E. et al. (2005). Functional genomics of the cilium, a sensory organelle. Curr. Biol. 15, 935-941.
10. Blacque, O. E. et al. (2004). Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport. Genes Dev. 18, 1630-1642.
11. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
12. Broadhead, R., Dawe, H. R., Farr, H., Griffiths, S., Hart, S. R., Portman, N., Shaw, M. K., Ginger, M. L., Gaskell, S. J., McKean, P. G., and Gull, K. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227.
13. Chen, N. et al. (2006). Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol. 7, R126.
14. Cole, D. G. (2003). The intraflagellar transport machinery of Chlamydomonas reinhardtii. Traffic 4, 435-442.
15. Cole, D. G., Chinn, S. W., Wedaman, K. P., Hall, K., Vuong, T., and Scholey, J. M. (1993). Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature 366, 268-270.
16. Cole, D. G., Diener, D. R., Himelblau, A. L., Beech, P. L., Fuster, J. C., 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.
17. Dwyer, N. D., Adler, C. E., Crump, J. G., L'Etoile, N. D., and Bargmann, C. I. (2001). Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31, 277-287.
18. Efimenko, E., Blacque, O. E., Ou, G., Haycraft, C. J., Yoder, B. K., Scholey, J. M., Leroux, M. R., and Swoboda, P. (2006). Caenorhabditis elegans DYF-2, an ortholog of human WDR19, is a component of the IFT machinery in sensory cilia. Mol. Biol. Cell 17, 4801-4811.
19. Efimenko, E., Bubb, K., Mak, H. Y., Holzman, T., Leroux, M. R., Ruvkun, G., Thomas, J. H., and Swoboda, P. (2005). Analysis of xbx genes in C. elegans. Development 132, 1923-1934.
20. Evans, J. E., Snow, J. J., Gunnarson, A. L., Ou, G., Stahlberg, H., McDonald, K. L., and Scholey, J. M. (2006). Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. J. Cell Biol. 172, 663-669.
21. Fan, Y. et al. (2004). Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome. Nat. Genet. 36, 989-993.
22. Fietz, M. J., McLaughlan, C. J., Campbell, M. T., and Rogers, G. E. (1993). Analysis of the sheep trichohyalin gene: potential structural and calcium-binding roles of trichohyalin in the hair follicle. J. Cell Biol. 121, 855-865.
23. Gherman, A., Davis, E. E., and Katsanis, N. (2006). The ciliary proteome database: an integrated community resource for the genetic and functional dissection of cilia. Nat. Genet. 38, 961-962.
24. Gunsalus, K. C. et al. (2005). Predictive models of molecular machines involved in Caenorhabditis elegans early embryogenesis. Nature 436, 861-865.
25. Hobert, O. (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
26. Imanishi, M., Endres, N. F., Gennerich, A., and Vale, R. D. (2006). Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. J. Cell Biol. 174, 931-937.
27. Inglis, P. N., Boroevich, K. A., and Leroux, M. R. (2006a). Piecing together a ciliome. Trends Genet. 22, 491-500.
28. Inglis, P. N., Ou, G., Leroux, M. R., and Scholey, J. M. (2006b). The sensory cilia of Caenorhabditis elegans. ed. WormBook, The C. elegans Research Community, WormBook, doi/10.1895/wormbook. 1.126.1, http://www.wormbook.org.
29. Keller, L. C., Romijn, E. P., Zamora, I., Yates, J. R., 3rd, and Marshall, W. F. (2005). Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr. Biol. 15, 1090-1098.
30. Kozminski, K. G., Johnson, K. A., Forscher, P., and Rosenbaum, J. L. (1993). A motility in the eukaryotic flagellum unrelated to flagellar beating. Proc. Natl. Acad. Sci. USA 90, 5519-5523.
31. Kunitomo, H., Uesugi, H., Kohara, Y., and Iino, Y. (2005). Identification of ciliated sensory neuron-expressed genes in Caenorhabditis elegans using targeted pull-down of poly(A) tails. Genome Biol. 6, R17.
32. Li, J. B. et al. (2004a). Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 117, 541-552.
33. Li, S. et al. (2004b). A map of the interactome network of the metazoan C. elegans. Science 303, 540-543.
34. Lucker, B. F., Behal, R. H., Qin, H., Siron, L. C., Taggart, W. D., Rosenbaum, J. L., and Cole, D. G. (2005). Characterization of the intraflagellar transport complex B core: direct interaction of the IFT81 and IFT74/72 subunits. J. Biol. Chem. 280, 27688-27696.
35. Maduro, M., and Pilgrim, D. (1995). Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141, 977-988.
36. Maduro, M. F., Gordon, M., Jacobs, R., and Pilgrim, D. B. (2000). The UNC-119 family of neural proteins is functionally conserved between humans, Drosophila and C. elegans. J. Neurogenet. 13, 191-212.
37. Mak, H. Y., Nelson, L. S., Basson, M., Johnson, C. D., and Ruvkun, G. (2006). Polygenic control of Caenorhabditis elegans fat storage. Nat. Genet. 38, 363-368.
38. Marshall, W.F., and Nonaka, S. (2006). Cilia: tuning in to the cell's antenna. Curr. Biol. 26, R604-R614.
39. Mesland, D. A., Hoffman, J. L., Caligor, E., and Goodenough, U. W. (1980). Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J. Cell Biol. 84, 599-617.
40. Murayama, T., Toh, Y., Ohshima, Y., and Koga, M. (2005). The dyf-3 gene encodes a novel protein required for sensory cilium formation in Caenorhabditis elegans. J. Mol. Biol. 346, 677-687.
41. Orozco, J. T., Wedaman, K. P., Signor, D., Brown, H., Rose, L., and Scholey, J. M. (1999). Movement of motor and cargo along cilia. Nature 398, 674.
42. Ostrowski, L. E., Blackburn, K., Radde, K. M., Moyer, M. B., Schlatzer, D. M., Moseley, A., and Boucher, R. C. (2002). A proteomic analysis of human cilia: identification of novel components. Mol. Cell Proteomics 1, 451-465.
43. Ou, G., Blacque, O. E., Snow, J. J., Leroux, M. R., and Scholey, J. M. (2005a). Functional coordination of intraflagellar transport motors. Nature 436, 583-587.
44. Ou, G., Qin, H., Rosenbaum, J. L., and Scholey, J. M. (2005b). The PKD protein qilin undergoes intraflagellar transport. Curr. Biol. 15, R410-R411.
45. Pan, J., Wang, Q., and Snell, W. J. (2005). Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85, 452-463.
46. Pan, X., Ou, G., Civelekoglu-Scholey, G., Blacque, O. E., Endres, N. F., Tao, L., Mogilner, A., Leroux, M. R., Vale, R. D., and Scholey, J. M. (2006). Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. J. Cell Biol. 174, 1035-1045.
47. Pazour, G. J., Agrin, N., Leszyk, J., and Witman, G. B. (2005). Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170, 103-113.
48. 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.
49. Peckol, E. L., Zallen, J. A., Yarrow, J. C., and Bargmann, C. I. (1999). Sensory activity affects sensory axon development in C. elegans. Development 126, 1891-1902.
50. Perens, E. A., and Shaham, S. (2005). C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev. Cell 8, 893-906.
51. Perkins, L. A., Hedgecock, E. M., Thomson, J. N., and Culotti, J. G. (1986). Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456-487.
52. Piperno, G., Siuda, E., Henderson, S., Segil, M., Vaananen, H., and Sassaroli, M. (1998). Distinct mutants of retrograde intraflagellar transport (IFT) share similar morphological and molecular defects. J. Cell Biol. 143, 1591-1601.
53. 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.
54. 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.
55. 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.
56. Qin, H., Rosenbaum, J. L., and Barr, M. M. (2001). An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr. Biol. 11, 457-461.
57. Reese, T. S. (1965). Olfactory cilia in the frog. J. Cell Biol. 25, 209-230.
58. Rosenbaum, J. L., and Witman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813-825.
59. Rothnagel, J. A., and Rogers, G. E. (1986). Trichohyalin, an intermediate filament-associated protein of the hair follicle. J. Cell Biol. 102, 1419-1429.
60. Schafer, J. C., Winkelbauer, M. E., Williams, C. L., Haycraft, C. J., Desmond, R. A., and Yoder, B. K. (2006). IFTA-2 is a conserved cilia protein involved in pathways regulating longevity and dauer formation in Caenorhabditis elegans. J. Cell Sci. 119, 4088-4100.
61. Scholey, J. M. (2003). Intraflagellar transport. Annu. Rev. Cell Dev. Biol. 19, 423-443.
62. Scholey, J. M., Ou, G., Snow, J., and Gunnarson, A. (2004). Intraflagellar transport motors in Caenorhabditis elegans neurons. Biochem. Soc. Trans. 32, 682-684.
63. Signor, D., Wedaman, K. P., Orozco, J. T., Dwyer, N. D., Bargmann, C. I., Rose, L. S., and Scholey, J. M. (1999). Role of a class DHC1b dynein in retrograde transport of IFT motors and IFT raft particles along cilia, but not dendrites, in chemosensory neurons of living Caenorhabditis elegans. J. Cell Biol. 147, 519-530.
64. Singla, V., and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
65. 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.
66. Starich, T. A., Herman, R. K., Kari, C. K., Yeh, W. H., Schackwitz, W. S., Schuyler, M. W., Collet, J., Thomas, J. H., and Riddle, D. L. (1995). Mutations affecting the chemosensory neurons of Caenorhabditis elegans. Genetics 139, 171-188.
67. Stoetzel, C. et al. (2006). BBS10 encodes a vertebrate-specific chaperonin-like protein and is a major BBS locus. Nat. Genet. 38, 521-524.
68. Stoetzel, C. et al. (2007). Identification of a novel BBS gene (BBS12) highlights the major role of a vertebrate-specific branch of chaperonin-related proteins in Bardet-Biedl syndrome. Am. J. Hum. Genet. 80, 1-11.
69. Uchida, O., Nakano, H., Koga, M., and Ohshima, Y. (2003). The C. elegans che-1 gene encodes a zinc finger transcription factor required for specification of the ASE chemosensory neurons. Development 130, 1215-1224.
70. Ward, S., Thomson, N., White, J. G., and Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160, 313-337.
71. Wicks, S. R., de Vries, C. J., van Luenen, H. G., and Plasterk, R. H. (2000). CHE-3, a cytosolic dynein heavy chain, is required for sensory cilia structure and function in Caenorhabditis elegans. Dev. Biol. 221, 295-307.
72. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H., and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.