Molecular mechanisms of protein and lipid targeting to ciliary membranes

Journal of Cell Science

Volumn 123, Issue 4, 2010, Pages 529-536

  Emmer, Brian T ^a   Maric, Danijela ^a   Engman, David M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cilia; Intraflagellar transport; Lipid rafts; Palmitoylation; Targeting

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE; KARYOPHERIN BETA; KINESIN 2; RAB11 PROTEIN; SNARE PROTEIN;

AXONEME; CELL BUDDING; CELL MEMBRANE; CELL MOTILITY; CELL MOTION; CELL SELECTION; CELL SPECIFICITY; CELL TRANSPORT; CELL VACUOLE; EUKARYOTIC FLAGELLUM; GOLGI COMPLEX; LIPID COMPOSITION; LIPID RAFT; LIPID TRANSPORT; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; NOTE; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT;

ANIMALS; AXONEME; CILIA; GOLGI APPARATUS; HUMANS; MEMBRANE FUSION; MEMBRANE LIPIDS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOVEMENT; PROTEIN TRANSPORT;

EUKARYOTA;

EID: 76649133765     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.062968     Document Type: Note

References (94)

1. Adhiambo, C., Blisnick, T., Toutirais, G., Delannoy, E. and Bastin, P. (2009). A novel function for the atypical small G protein Rab-like 5 in the assembly of the trypanosome flagellum. J. Cell Sci. 122, 834-841.
2. Baldari, C. T. and Rosenbaum, J. (2009). Intraflagellar transport: it's not just for cilia anymore. Curr. Opin. Cell Biol. [Epub ahead of print] doi:10.1016/j.ceb.2009.10.010.
3. Bethani, I., Lang, T., Geumann, U., Sieber, J. J., Jahn, R. and Rizzoli, S. O. (2007). The specificity of SNARE pairing in biological membranes is mediated by both proof-reading and spatial segregation. EMBO J. 26, 3981-3992.
4. Bhowmick, R., Li, M., Sun, J., Baker, S. A., Insinna, C. and Besharse, J. C. (2009). Photoreceptor IFT complexes containing chaperones, guanylyl cyclase 1 and rhodopsin. Traffic 10, 648-663.
5. Blacque, O. E. and Leroux, M. R. (2006). Bardet-Biedl syndrome: an emerging pathomechanism of intracellular transport. Cell. Mol. Life Sci. 63, 2145-2161.
6. Bloodgood, R. A., Woodward, M. P. and Young, W. W. (1995). Unusual distribution of a glycolipid antigen in the flagella of Chamydomonas. Protoplasma 185, 123-130.
7. Bouck, G. B. (1971). The structure, origin, isolation, and composition of the tubular mastigonemes of the Ochromas flagellum. J. Cell Biol. 50, 362-384.
8. Brandhorst, D., Zwilling, D., Rizzoli, S. O., Lippert, U., Lang, T. and Jahn, R. (2006). Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity. Proc. Natl. Acad. Sci. USA 103, 2701-2706.
9. Chailley, B. and Boisvieux-Ulrich, E. (1985). Detection of plasma membrane cholesterol by filipin during microvillogenesis and ciliogenesis in quail oviduct. J. Histochem. Cytochem. 33, 1-10.
10. 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.
11. Deretic, D., Traverso, V., Parkins, N., Jackson, F., Rodriguez de Turco, E. B. and Ransom, N. (2004). Phosphoinositides, ezrin/moesin, and rac1 regulate fusion of rhodopsin transport carriers in retinal photoreceptors. Mol. Biol. Cell 15, 359-370.
12. Drin, G., Morello, V., Casella, J. F., Gounon, P. and Antonny, B. (2008). Asymmetric tethering of flat and curved lipid membranes by a golgin. Science 320, 670-673.
13. Ejsing, C. S., Sampaio, J. L., Surendranath, V., Duchoslav, E., Ekroos, K., Klemm, R. W., Simons, K. and Shevchenko, A. (2009). Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc. Natl. Acad. Sci. USA 106, 2136-2141.
14. Emmer, B. T., Souther, C., Toriello, K. M., Olson, C. L., Epting, C. L. and Engman, D. M. (2009). Identification of a palmitoyl acyltransferase required for protein sorting to the flagellar membrane. J. Cell Sci. 122, 867-874.
15. European Polycystic Kidney Disease Consortium (1994). The polycystic kidney disease 1 gene encodes a 14 kb transcript and lies within a duplicated region on chromosome 16. Cell 77, 881-894.
16. Fan, S., Fogg, V., Wang, Q., Chen, X. W., Liu, C. J. and Margolis, B. (2007). A novel Crumbs3 isoform regulates cell division and ciliogenesis via importin beta interactions. J. Cell Biol. 178, 387-398.
17. Fan, Y., Esmail, M. A., Ansley, S. J., Blacque, O. E., Boroevich, K., Ross, A. J., Moore, S. J., Badano, J. L., May-Simera, H., Compton, D. S. 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.
18. Fielding, A. B., Schonteich, E., Matheson, J., Wilson, G., Yu, X., Hickson, G. R., Srivaslava, S., Baldwin, S. A., Prekeris, R. and Gould, G. W. (2005). Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 24, 3389-3399.
19. 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.
20. Follit, J. A., San Agustin, J. T., Xu, F., Jonassen, J. A., Samtani, R., Lo, C. W. and Pazour, G. J. (2008). The golgin GMAP210/TRIP11 anchors IFT20 to the Golgi complex. PLoS Genet. 4, e1000315.
21. 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.
22. Gaus, K., Gratton, E., Kable, E. P., Jones, A. S., Gelissen, I., Kritharides, L. and Jessup, W. (2003). Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. USA 100, 15554-15559.
23. Geng, L., Okuhara, D., Yu, Z., Tian, X., Cai, Y., Shibazaki, S. and Somlo, S. (2006). Polycystin-2 traffics to cillia independently of polycystin-1 by using an N-terminal RVxP motif. J. Cell Sci. 119, 1383-1395.
24. Gilula, N. B. and Satir, P. (1972). The ciliary necklace. A ciliary membrane specialization.. J. Cell Biol. 53, 494-509.
25. Godsel, L. M. and Engman, D. M. (1999). Flagellar protein localization mediated by a calcium-myristoyl/palmitoyl switch mechanism. EMBO J. 18, 2057-2065.
26. Guo, W., Roth, D., Walch-Solimena, C. and Novick, P. (1999). The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18, 1071-1080.
27. Guo, W., Sacher, M., Barrowman, J., Ferro-Novick, S. and Novick, P. (2000). Protein complexes in transport vesicle targeting.. Trends Cell Biol. 10, 251-255.
28. Hao, L. and Scholey, J. M. (2009). Intraflagellar transport at a glance. J. Cell Sci. 122, 889-892.
29. 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, 501-514.
30. Inoue, H., Ha, V. L., Prekeris, R. and Randazzo, P. A. (2008). Arf GTPase-activating protein ASAP1 interacts with Rab11 effector FIP3 and regulates pericentrosomal localization of transferring receptor-positive recycling endosome. Mol. Biol. Cell 19, 4224-4237.
31. Iomini, C., Li, L., Mo, W., Dutcher, S. K. and Piperno, G. (2006). Two flagellar genes, AGG2 and AGG3, mediate orientation to light in Chlamydomonas. Curr. Biol. 16, 1147-1153.
32. Jenkins, P. M., Hurd, T. W., Zhang, L., McEwen, D. P., Brown, R. L., Margolis, B., Verhey, K. J. and Martens, J. R. (2006). Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr. Biol. 16, 1211-1216.
33. Jin, H. and Nachury, M. V. (2009). The BBSome. Curr. Biol. 19, R472-R473.
34. Johnson, K. A. and Rosenbaum, J. L. (1992). Polarity of flagellar assembly in Chlamydomonas. J. Cell Biol. 119, 1605-1611.
35. Kaneshiro, E. S. (1990). Lipids of ciliary and flagellar membranes. In Ciliary and Flagellar Membranes (ed. R. A. Bloodgood), pp. 241-265. New York: Plenum Press.
36. Kaneshiro, E. S., Matesic, D. F. and Jayasimhulu, K. (1984). Characterizations of six ethanolamine sphingophospholipids from Paramecium cells and cilia. J. Lipid Res. 25, 369-377.
37. Kaupp, U. B., Solzin, J., Hildebrand, E., Brown, J. E., Helbig, A., Hagen, V., Beyermann, M., Pampaloni, F. and Weyand, I. (2003). The signal flow and motor response controlling chemotaxis of sea urchin sperm. Nat. Cell Biol. 5, 109-117.
38. Kaya, K., Ramesha, C. S. and Thompson, G. A., Jr (1984). On the formation of alpha-hydroxy fatty acids. Evidence for a direct hydroxylation of nonhydroxy fatty acid-containing sphingolipids. J. Biol. Chem. 259, 3548-3553.
39. Kizhatil, K., Baker, S. A., Arshavsky, V. Y. and Bennett, V. (2009). Ankyrin-G promotes cyclic nucleotide-gated channel transport to rod photoreceptor sensory cilia. Science 323, 1614-1617.
40. Klemm, R. W., Ejsing, C. S., Surma, M. A., Kaiser, H. J., Gerl, M. J., Sampaio, J. L., de Robillard, Q., Ferguson, C., Proszynski, T. J., Shevchenko, A. et al. (2009). Segregation of sphingolipids and sterols during formation of secretory vesicles at the trans-Golgi network. J. Cell Biol. 185, 601-612.
41. 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.
42. Kozminski, K. G., Beech, P. L. and Rosenbaum, J. L. (1995). The Chlamydomonas kinesin-like protein FLA10 is involved in motility associated with the flagellar membrane. J. Cell Biol. 131, 1517-1527.
43. Krauss, M., Jia, J. Y., Roux, A., Beck, R., Wieland, F. T., De Camilli, P. and Haucke, V. (2008). Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J. Biol. Chem. 283, 27717-27723.
44. Kunitomo, H. and Iino, Y. (2008). Caenorhabditis elegans DYF-11, an orthologue of mammalian Traf3ip1/MIP-T3, is required for sensory cilia formation. Genes Cells 13, 13-25.
45. Liu, J., Zuo, X., Yue, P. and Guo, W. (2007). Phosphatidylinositol 4,5-bisphosphate mediates the targeting of the exocyst to the plasma membrane for exocytosis in mammalian cells. Mol. Biol. Cell 18, 4483-4492.
46. Liu, X., Udovichenko, I. P., Brown, S. D., Steel, K. P. and Williams, D. S. (1999). Myosin VIIa participates in opsin transport through the photoreceptor cilium. J. Neurosci. 19, 6267-6274.
47. Low, S. H., Vasanji, A., Nanduri, J., He, M., Sharma, N., Koo, M., Drazba, J. and Weimbs, T. (2006). Syntaxins 3 and 4 are concentrated in separate clusters on the plasma membrane before the establishment of cell polarity. Mol. Biol. Cell 17, 977-989.
48. Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B. M., Schonteich, E., Prekeris, R., Moritz, O. L., Randazzo, P. A. and Deretic, D. (2009a). Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28, 183-192.
49. Mazelova, J., Ransom, N., Astuto-Gribble, L., Wilson, M. C. and Deretic, D. (2009b). Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J. Cell Sci. 122, 2003-2013.
50. Mitchell, D. R. (2007). The evolution of eukaryotic cilia and flagella as motile and sensory organelles. Adv. Exp. Med. Biol. 607, 130-140.
51. Mochizuki, T., Wu, G., Hayashi, T., Xenophontos, S. L., Veldhuisen, B., Saris, J. J., Reynolds, D. M., Cai, Y., Gabow, P. A., Pierides, A. et al. (1996). PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein. Science 272, 1339-1342.
52. Moritz, O. L., Tam, B. M., Hurd, L. L., Peranen, J., Deretic, D. and Papermaster, D. S. (2001). Mutant rab8 impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell 12, 2341-2351.
53. Nachury, M. V., Loktev, A. V., Zhang, Q., Westlake, C. J., Peranen, J., Merdes, A., Slusarski, D. C., Scheller, 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.
54. Nie, Z., Hirsch, D. S., Luo, R., Jian, X., Stauffer, S., Cremesti, A., Andrade, J., Lebowitz, J., Marino, M., Ahvazi, B. et al. (2006). A BAR domain in the N terminus of the Arf GAP ASAP1 affects membrane structure and trafficking of epidermal growth factor receptor. Curr. Biol. 16, 130-139.
55. Novick, P., Field, C. and Schekman, R. (1980). Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205-215.
56. Omori, Y., Zhao, C., Saras, A., Mukhopadhyay, S., Kim, W., Furukawa, T., Sengupta, P., Veraksa, A. and Malicki, J. (2008). Elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat. Cell Biol. 10, 437-444.
57. 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.
58. Ouaissi, A., Aguirre, T., Plumas-Marty, B., Piras, M., Schoneck, R., Gras-Masse, H., Taibi, A., Loyens, M., Tartar, A., Capron, A. et al. (1992). Cloning and sequencing of a 24-kDa Trypanosoma cruzi specific antigen released in association with membrane vesicles and defined by a monoclonal antibody. Biol. Cell 75, 11-17.
59. Pan, J. and Snell, W. J. (2000). Signal transduction during fertilization in the unicellular green alga, Chlamydomonas. Curr. Opin. Microbiol. 3, 596-602.
60. Pan, J. and Snell, W. J. (2003). Kinesin II and regulated intraflagellar transport of Chlamydomonas aurora protein kinase. J. Cell Sci. 116, 2179-2186.
61. Papermaster, D. S., Schneider, B. G. and Besharse, J. C. (1985). Vesicular transport of newly synthesized opsin from the Golgi apparatus toward the rod outer segment. Ultrastructural immunocytochemical and autoradiographic evidence in Xenopus retinas. Invest. Ophthalmol. Vis. Sci. 26, 1386-1404.
62. Pazour, G. J. and Bloodgood, R. A. (2008). Targeting proteins to the ciliary membrane. Curr. Top. Dev. Biol. 85, 111-145.
63. 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.
64. 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.
65. Pazour, G. J., San Agustin, J. T., Follit, J. A., Rosenbaum, J. L. and Witman, G. B. (2002). Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr. Biol. 12, R378-R380.
66. Pedersen, L. B., Geimer, S., Sloboda, R. D. and Rosenbaum, J. L. (2003). The microtubule plus end-tracking protein EB1 is localized to the flagellar tip and basal bodies in Chlamydomonas reinhardtii. Curr. Biol. 13, 1969-1974.
67. Pedersen, L. B., Miller, M. S., Geimer, S., Leitch, J. M., Rosenbaum, J. L. and Cole, D. G. (2005). Chlamydomonas IFT172 is encoded by FLA11, interacts with CrEB1, and regulates IFT at the flagellar tip. Curr. Biol. 15, 262-266.
68. 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.
69. 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.
70. 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.
71. Qin, H., Wang, Z., Diener, D. and Rosenbaum, J. (2007). Intraflagellar transport protein 27 is a small G protein involved in cell-cycle control. Curr. Biol. 17, 193-202.
72. Reiter, J. F. and Mostov, K. (2006). Vesicle transport, cilium formation, and membrane specialization: the origins of a sensory organelle. Proc. Natl. Acad. Sci. USA 103, 18383-18384.
73. Rogers, K. K., Wilson, P. D., Snyder, R. W., Zhang, X., Guo, W., Burrow, C. R. and Lipschutz, J. H. (2004). The exocyst localizes to the primary cilium in MDCK cells. Biochem. Biophys. Res. Commun. 319, 138-143.
74. Schuck, S. and Simons, K. (2004). Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117, 5955-5964.
75. Senin, I. I., Hoppner-Heitmann, D., Polkovnikova, O. O., Churumova, V. A., Tikhomirova, N. K., Philippov, P. P. and Koch, K. W. (2004). Recoverin and rhodopsin kinase activity in detergent-resistant membrane rafts from rod outer segments. J. Biol. Chem. 279, 48647-48653.
76. Shah, A. S., Ben-Shahar, Y., Moninger, T. O., Kline, J. N. and Weish, M. J. (2009). Motile cilia of human airway epithelia are chemosensory. Science 325, 1131-1134.
77. Shogomori, H. and Brown, D. A. (2003). Use of detergents to study membrane rafts: the good, the bad, and the ugly. Biol. Chem. 384, 1259-1263.
78. Short, B., Haas, A. and Barr, F. A. (2005). Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim. Biophys. Acta 1744, 383-395.
79. 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.
80. Sloboda, R. D. and Rosenbaum, J. L. (2007). Making sense of cilia and flagella. J. Cell Biol. 179, 575-582.
81. Song, L. and Dentler, W. L. (2001). Flagellar protein dynamics in Chlamydomonas. J. Biol. Chem. 276, 29754-29763.
82. Souto-Padron, T. and de Souza, W. (1983). Freeze-fracture localization of filipin-cholesterol complexes in the plasma membrane of Trypanosoma cruzi. J. Parasitol. 69, 129-137.
83. Stephens, R. E. (2000). Preferential incorporation of tubulin into the junctional region of ciliary outer doublet microtubules: a model for treadmilling by lattice dislocation. Cell Motil. Cytoskeleton 47, 130-140.
84. ter Beest, M. B., Chapin, S. J., Avrahami, D. and Mostov, K. E. (2005). The role of syntaxins in the specificity of vesicle targeting in polarized epithelial cells. Mol. Biol. Cell 16, 5784-5792.
85. TerBush, D. R., Maurice, T., Roth, D. and Novick, P. (1996). The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15, 6483-6494.
86. Tetley, L. (1986). Freeze-fracture studies on the surface membranes of pleomorphic bloodstream and in vitro transformed procyclic Trypanosoma brucei. Acta Trop. 43, 307-317.
87. Tobin, J. L. and Beales, P. L. (2009). The nonmotile ciliopathies. Genet. Med. 11, 386-402.
88. Torres, V. E. and Harris, P. C. (2006). Mechanisms of disease: autosomal dominant and recessive polycystic kidney diseases. Nat. Clin. Pract. Nephrol. 2, 40-55; quiz 55.
89. Travis, A. J., Merdiushev, T., Vargas, L. A., Jones, B. H., Purdon, M. A., Nipper, R. W., Galatioto, J., Moss, S. B., Hunnicutt, G. R. and Kopf, G. S. (2001). Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa. Dev. Biol. 240, 599-610.
90. Tull, D., Vince, J. E., Callaghan, J. M., Naderer, T., Spurck, T., McFadden, G. I., Currie, G., Ferguson, K., Bacic, A. and McConville, M. J. (2004). SMP-1, a member of a new family of small myristoylated proteins in kinetoplastid parasites, is targeted to the flagellum membrane in Leishmania. Mol. Biol. Cell 15, 4775-4786.
91. Tyler, K. M., Fridberg, A., Toriello, K. M., Olson, C. L., Cieslak, J. A., Hazlett, T. L. and Engman, D. M. (2009). Flagellar membrane localization via association with lipid rafts. J. Cell Sci. 122, 859-866.
92. Yoshimura, S., Egerer, J., Fuchs, E., Haas, A. K. and Barr, F. A. (2007). Functional dissection of Rab GTPases involved in primary cilium formation. J. Cell Biol. 178, 363-369.
93. Zimmermann, K. W. (1898). Beiträge zur Kenntnis einiger Drüsen und Epithelien. Arch. Mikrosk. Entwickl. Mech. 52, 552-706.
94. Zuo, X., Guo, W. and Lipschutz, J. H. (2009). The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 20, 2522-2529.