Switching on cilia: Transcriptional networks regulating ciliogenesis

Development (Cambridge)

Volumn 141, Issue 7, 2014, Pages 1427-1441

  Choksi, Semil P ^a   Lauter, Gilbert ^b   Swoboda, Peter ^b   Roy, Sudipto ^a,c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b KAROLINSKA INSTITUTE   (Sweden)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cilia; Ciliogenesis; FOXJ1; Motile cilia; RFX; Transcriptional regulation

Indexed keywords

FIBROCYSTIN; FORKHEAD TRANSCRIPTION FACTOR; HEPATOCYTE NUCLEAR FACTOR 1BETA; HORMONE RECEPTOR; KINESIN 2; PROTEIN MYB; REGULATORY FACTOR 1; REGULATORY FACTOR 2; REGULATORY FACTOR 3; REGULATORY FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXJ1; TRANSCRIPTION FACTOR SOX5; UNCLASSIFIED DRUG;

BIOGENESIS; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CILIARY MOTILITY; CILIATED EPITHELIUM; CILIOGENESIS; DNA BINDING; DNA LIBRARY; DROSOPHILA MELANOGASTER; EPENDYMA CELL; EUKARYOTIC FLAGELLUM; FLUID TRANSPORT; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC CONSERVATION; HUMAN; MECHANORECEPTOR; MICROTUBULE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

CILIA; CILIOGENESIS; FOXJ1; MOTILE CILIA; RFX; TRANSCRIPTIONAL REGULATION;

ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; CILIA; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HUMANS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84896257145     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074666     Document Type: Review

References (167)

1. Acton, A. B. (1966). An unusual ciliumlike process. J. Cell Biol. 29, 366-369.
2. Aftab, S., Semenec, L., Chu, J. S. and Chen, N. (2008). Identification and characterization of novel human tissue-specific RFX transcription factors. BMC Evol. Biol. 8, 226.
3. Afzelius, B. A. (1976). A human syndrome caused by immotile cilia. Science 193, 317-319.
4. Ait-Lounis, A., Baas, D., Barras, E., Benadiba, C., Charollais, A., Nlend Nlend, R., Liègeois, D., Meda, P., Durand, B. and Reith, W. (2007). Novel function of the ciliogenic transcription factor RFX3 in development of the endocrine pancreas. Diabetes 56, 950-959.
5. Alten, L., Schuster-Gossler, K., Beckers, A., Groos, S., Ulmer, B., Hegermann, J., Ochs, M. and Gossler, A. (2012). Differential regulation of node formation, nodal ciliogenesis and cilia positioning by Noto and Foxj1. Development 139, 1276-1284.
6. Anderson, R. G. and Brenner, R. M. (1971). The formation of basal bodies (centrioles) in the Rhesus monkey oviduct. J. Cell Biol. 50, 10-34.
7. Ansley, S. J., Badano, J. L., Blacque, O. E., Hill, J., Hoskins, B. E., Leitch, C. C., Kim, J. C., Ross, A. J., Eichers, E. R., Teslovich, T. M. et al. (2003). Basal body dysfunction is a likely cause of pleiotropic Bardet-Biedl syndrome. Nature 425, 628-633.
8. Arnaiz, O., Malinowska, A., Klotz, C., Sperling, L., Dadlez, M., Koll, F. and Cohen, J. (2009). Cildb: a knowledgebase for centrosomes and cilia. Database (Oxford) 2009, bap022.
9. Ashique, A. M., Choe, Y., Karlen, M., May, S. R., Phamluong, K., Solloway, M. J., Ericson, J. and Peterson, A. S. (2009). The Rfx4 transcription factor modulates Shh signaling by regional control of ciliogenesis. Sci. Signal. 2, ra70.
10. Baas, D., Meiniel, A., Benadiba, C., Bonnafe, E., Meiniel, O., Reith, W. and Durand, B. (2006). A deficiency in RFX3 causes hydrocephalus associated with abnormal differentiation of ependymal cells. Eur. J. Neurosci. 24, 1020-1030.
11. Babu, D. and Roy, S. (2013). Left-right asymmetry: cilia stir up new surprises in the node. Open Biol 3, 130052.
12. Beckers, A., Alten, L., Viebahn, C., Andre, P. and Gossler, A. (2007). The mouse homeobox gene Noto regulates node morphogenesis, notochordal ciliogenesis, and left right patterning. Proc. Natl. Acad. Sci. USA 104, 15765-15770.
13. Benadiba, C., Magnani, D., Niquille, M., Morlé, L., Valloton, D., Nawabi, H., Ait-Lounis, A., Otsmane, B., Reith, W., Theil, T. et al. (2012). The ciliogenic transcription factor RFX3 regulates early midline distribution of guidepost neurons required for corpus callosum development. PLoS Genet. 8, e1002606.
14. Bisgrove, B. W., Makova, S., Yost, H. J. and Brueckner, M. (2012). RFX2 is essential in the ciliated organ of asymmetry and an RFX2 transgene identifies a population of ciliated cells sufficient for fluid flow. Dev. Biol. 363, 166-178.
15. Blackshear, P. J., Graves, J. P., Stumpo, D. J., Cobos, I., Rubenstein, J. L. and Zeldin, D. C. (2003). Graded phenotypic response to partial and complete deficiency of a brain-specific transcript variant of the winged helix transcription factor RFX4. Development 130, 4539-4552.
16. Blacque, O. E., Perens, E. A., Boroevich, K. A., Inglis, P. N., Li, C., Warner, A., Khattra, J., Holt, R. A., Ou, G., Mah, A. K. et al. (2005). Functional genomics of the cilium, a sensory organelle. Curr. Biol. 15, 935-941.
17. Blatt, E. N., Yan, X. H., Wuerffel, M. K., Hamilos, D. L. and Brody, S. L. (1999). Forkhead transcription factor HFH-4 expression is temporally related to ciliogenesis. Am. J. Respir. Cell Mol. Biol. 21, 168-176.
18. Bloodgood, R. A. (2010). Sensory reception is an attribute of both primary cilia and motile cilia. J. Cell Sci. 123, 505-509.
19. Bonnafe, E., Touka, M., AitLounis, A., Baas, D., Barras, E., Ucla, C., Moreau, A., Flamant, F., Dubruille, R., Couble, P. et al. (2004). The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Cell. Biol. 24, 4417-4427.
20. Boon, M., Jorissen, M., Proesmans, M. and De Boeck, K. (2013). Primary ciliary dyskinesia, an orphan disease. Eur. J. Pediatr. 172, 151-162.
21. Boskovski, M. T., Yuan, S., Pedersen, N. B., Goth, C. K., Makova, S., Clausen, H., Brueckner, M. and Khokha, M. K. (2013). The heterotaxy gene GALNT11 glycosylates Notch to orchestrate cilia type and laterality. Nature 504, 456-459.
22. Brightman, M. W. and Palay, S. L. (1963). The fine structure of ependyma in the brain of the rat. J. Cell Biol. 19, 415-439.
23. Brody, S. L., Yan, X. H., Wuerffel, M. K., Song, S. K. and Shapiro, S. D. (2000). Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 23, 45-51.
24. Burghoorn, J., Piasecki, B. P., Crona, F., Phirke, P., Jeppsson, K. E. and Swoboda, P. (2012). The in vivo dissection of direct RFX-target gene promoters in C. elegans reveals a novel cis-regulatory element, the C-box. Dev. Biol. 368, 415-426.
25. Cachero, S., Simpson, T. I., Zur Lage, P. I., Ma, L., Newton, F. G., Holohan, E. E., Armstrong, J. D. and Jarman, A. P. (2011). The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons. PLoS Biol. 9, e1000568.
26. Caron, A., Xu, X. and Lin, X. (2012). Wnt/β-catenin signaling directly regulates Foxj1 expression and ciliogenesis in zebrafish Kupffer's vesicle. Development 139, 514-524.
27. 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. (2012). BLD10/CEP135 is a microtubule-associated protein that controls the formation of the flagellum central microtubule pair. Dev. Cell 23, 412-424.
28. Caspary, T., Larkins, C. E. and Anderson, K. V. (2007). The graded response to Sonic Hedgehog depends on cilia architecture. Dev. Cell 12, 767-778.
29. Chen, J., Knowles, H. J., Hebert, J. L. and Hackett, B. P. (1998). Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J. Clin. Invest. 102, 1077-1082.
30. Chen, N., Mah, A., Blacque, O. E., Chu, J., Phgora, K., Bakhoum, M. W., Newbury, C. R., Khattra, J., Chan, S., Go, A. et al. (2006). Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol. 7, R126.
31. Chu, J. S., Baillie, D. L. and Chen, N. (2010). Convergent evolution of RFX transcription factors and ciliary genes predated the origin of metazoans. BMC Evol. Biol. 10, 130.
32. Chung, M. I., Peyrot, S. M., LeBoeuf, S., Park, T. J., McGary, K. L., Marcotte, E. M. and Wallingford, J. B. (2012). RFX2 is broadly required for ciliogenesis during vertebrate development. Dev. Biol. 363, 155-165.
33. Clark, K. L., Halay, E. D., Lai, E. and Burley, S. K. (1993). Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412-420.
34. Clevidence, D. E., Overdier, D. G., Tao, W., Qian, X., Pani, L., Lai, E. and Costa, R. H. (1993). Identification of nine tissue-specific transcription factors of the hepatocyte nuclear factor 3/forkhead DNA-binding-domain family. Proc. Natl. Acad. Sci. USA 90, 3948-3952.
35. Clevidence, D. E., Overdier, D. G., Peterson, R. S., Porcella, A., Ye, H., Paulson, K. E. and Costa, R. H. (1994). Members of the HNF-3/forkhead family of transcription factors exhibit distinct cellular expression patterns in lung and regulate the surfactant protein B promoter. Dev. Biol. 166, 195-209.
36. Cruz, C., Ribes, V., Kutejova, E., Cayuso, J., Lawson, V., Norris, D., Stevens, J., Davey, M., Blight, K., Bangs, F. et al. (2010). Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 137, 4271-4282.
37. De Robertis, E. (1956). Morphogenesis of the retinal rods; an electron microscope study. J. Biophys. Biochem. Cytol. 2 Suppl., 209-218.
38. De Waele, G. and Dierickx, K. (1979). Scanning electron microscopy of the wall of the third ventricle in the brain of Rana temporaria. Part IV. Cell Tissue Res. 203, 53-64.
39. Del Bigio, M. R. (2010). Ependymal cells: biology and pathology. Acta Neuropathol. 119, 55-73.
40. Didon, L., Zwick, R. K., Chao, I. W., Walters, M. S., Wang, R., Hackett, N. R. and Crystal, R. G. (2013). RFX3 modulation of FOXJ1 regulation of cilia genes in the human airway epithelium. Respir. Res. 14, 70.
41. Dubruille, R., Laurençon, A., Vandaele, C., Shishido, E., Coulon-Bublex, M., Swoboda, P., Couble, P., Kernan, M. and Durand, B. (2002). Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129, 5487-5498.
42. Durand, B., Vandaele, C., Spencer, D., Pantalacci, S. and Couble, P. (2000). Cloning and characterization of dRFX, the Drosophila member of the RFX family of transcription factors. Gene 246, 285-293.
43. Dwyer, N. D., Troemel, E. R., Sengupta, P. and Bargmann, C. I. (1998). Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membraneassociated protein. Cell 93, 455-466.
44. 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.
45. El Zein, L., Ait-Lounis, A., Morlé, L., Thomas, J., Chhin, B., Spassky, N., Reith, W. and Durand, B. (2009). RFX3 governs growth and beating efficiency of motile cilia in mouse and controls the expression of genes involved in human ciliopathies. J. Cell Sci. 122, 3180-3189.
46. Emery, P., Durand, B., Mach, B. and Reith, W. (1996). RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res. 24, 803-807.
47. Fawcett, D. W. (1954). The study of epithelial cilia and sperm flagella with the electron microscope. Laryngoscope 64, 557-567.
48. Fawcett, D. W. and Porter, K. R. (1954). A study of the fine structure of ciliated epithelia. J. Morphol. 94, 221-281.
49. Feistel, K. and Blum, M. (2006). Three types of cilia including a novel 9+4 axoneme on the notochordal plate of the rabbit embryo. Dev. Dyn. 235, 3348-3358.
50. Feng, C., Xu, W. and Zuo, Z. (2009). Knockout of the regulatory factor X1 gene leads to early embryonic lethality. Biochem. Biophys. Res. Commun. 386, 715-717.
51. Feng, C., Li, J. and Zuo, Z. (2011). Expression of the transcription factor regulatory factor X1 in the mouse brain. Folia Histochem. Cytobiol. 49, 344-351.
52. Flock, A. and Wersall, J. (1962). A study of the orientation of the sensory hairs of the receptor cells in the lateral line organ of fish, with special reference to the function of the receptors. J. Cell Biol. 15, 19-27.
53. Fox, H. and Hamilton, L. (1971). Ultrastructure of diploid and haploid cells of Xenopus laevis larvae. J. Embryol. Exp. Morphol. 26, 81-98.
54. Gajiwala, K. S., Chen, H., Cornille, F., Roques, B. P., Reith, W., Mach, B. and Burley, S. K. (2000). Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 403, 916-921.
55. Garcia-Gonzalo, F. R. and Reiter, J. F. (2012). Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697-709.
56. 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.
57. Goetz, S. C. and Anderson, K. V. (2010). The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11, 331-344.
58. Gomperts, B. N., Gong-Cooper, X. and Hackett, B. P. (2004). Foxj1 regulates basal body anchoring to the cytoskeleton of ciliated pulmonary epithelial cells. J. Cell Sci. 117, 1329-1337.
59. Gresh, L., Fischer, E., Reimann, A., Tanguy, M., Garbay, S., Shao, X., Hiesberger, T., Fiette, L., Igarashi, P., Yaniv, M. et al. (2004). A transcriptional network in polycystic kidney disease. EMBO J. 23, 1657-1668.
60. Hackett, B. P., Brody, S. L., Liang, M., Zeitz, I. D., Bruns, L. A. and Gitlin, J. D. (1995). Primary structure of hepatocyte nuclear factor/forkhead homologue 4 and characterization of gene expression in the developing respiratory and reproductive epithelium. Proc. Natl. Acad. Sci. USA 92, 4249-4253.
61. Hagenlocher, C., Walentek, P., Muller, C., Thumberger, T. and Feistel, K. (2013). Ciliogenesis and cerebrospinal fluid flow in the developing Xenopus brain are regulated by foxj1. Cilia 2, 12.
62. Hannenhalli, S. and Kaestner, K. H. (2009). The evolution of Fox genes and their role in development and disease. Nat. Rev. Genet. 10, 233-240.
63. Hansen, A. and Zeiske, E. (1998). The peripheral olfactory organ of the zebrafish, Danio rerio: an ultrastructural study. Chem. Senses 23, 39-48.
64. Hansen, I. A., Sieglaff, D. H., Munro, J. B., Shiao, S. H., Cruz, J., Lee, I. W., Heraty, J. M. and Raikhel, A. S. (2007). Forkhead transcription factors regulate mosquito reproduction. Insect Biochem. Mol. Biol. 37, 985-997.
65. Hashimoto, M., Shinohara, K., Wang, J., Ikeuchi, S., Yoshiba, S., Meno, C., Nonaka, S., Takada, S., Hatta, K., Wynshaw-Boris, A. et al. (2010). Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 12, 170-176.
66. Haycraft, C. J., Swoboda, P., Taulman, P. D., Thomas, J. H. and Yoder, B. K. (2001). The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128, 1493-1505.
67. Hellman, N. E., Liu, Y., Merkel, E., Austin, C., Le Corre, S., Beier, D. R., Sun, Z., Sharma, N., Yoder, B. K. and Drummond, I. A. (2010). The zebrafish foxj1a transcription factor regulates cilia function in response to injury and epithelial stretch. Proc. Natl. Acad. Sci. USA 107, 18499-18504.
68. Hildebrandt, F., Benzing, T. and Katsanis, N. (2011). Ciliopathies. N. Engl. J. Med. 364, 1533-1543.
69. Horvath, G. C., Kistler, W. S. and Kistler, M. K. (2004). RFX2 is a potential transcriptional regulatory factor for histone H1t and other genes expressed during the meiotic phase of spermatogenesis. Biol. Reprod. 71, 1551-1559.
70. Huang, M., Zhou, Z. and Elledge, S. J. (1998). The DNA replication and damage checkpoint pathways induce transcription by inhibition of the Crt1 repressor. Cell 94, 595-605.
71. Inaba, K. (2011). Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol. Hum. Reprod. 17, 524-538.
72. Inglis, P. N., Boroevich, K. A. and Leroux, M. R. (2006). Piecing together a ciliome. Trends Genet. 22, 491-500.
73. Insinna, C. and Besharse, J. C. (2008). Intraflagellar transport and the sensory outer segment of vertebrate photoreceptors. Dev. Dyn. 237, 1982-1992.
74. Ishikawa, H. and Marshall, W. F. (2011). Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 12, 222-234.
75. Iwama, A., Pan, J., Zhang, P., Reith, W., Mach, B., Tenen, D. G. and Sun, Z. (1999). Dimeric RFX proteins contribute to the activity and lineage specificity of the interleukin-5 receptor alpha promoter through activation and repression domains. Mol. Cell. Biol. 19, 3940-3950.
76. Jackson, B. C., Carpenter, C., Nebert, D. W. and Vasiliou, V. (2010). Update of human and mouse forkhead box (FOX) gene families. Hum. Genomics 4, 345-352.
77. Jacquet, B. V., Salinas-Mondragon, R., Liang, H., Therit, B., Buie, J. D., Dykstra, M., Campbell, K., Ostrowski, L. E., Brody, S. L. and Ghashghaei, H. T. (2009). FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136, 4021-4031.
78. Jenkins, P. M., McEwen, D. P. and Martens, J. R. (2009). Olfactory cilia: linking sensory cilia function and human disease. Chem. Senses 34, 451-464.
79. Jurand, A. (1974). Some aspects of the development of the notochord in mouse embryos. J. Embryol. Exp. Morphol. 32, 1-33.
80. Kaestner, K. H., Knochel, W. and Martinez, D. E. (2000). Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14, 142-146.
81. Kiselak, E. A., Shen, X., Song, J., Gude, D. R., Wang, J., Brody, S. L., Strauss, J. F., III and Zhang, Z. (2010). Transcriptional regulation of an axonemal central apparatus gene, sperm-associated antigen 6, by a SRY-related high mobility group transcription factor, S-SOX5. J. Biol. Chem. 285, 30496-30505.
82. Klos Dehring, D. A., Vladar, E. K., Werner, M. E., Mitchell, J. W., Hwang, P. and Mitchell, B. J. (2013). Deuterosome-mediated centriole biogenesis. Dev. Cell 27, 103-112.
83. Konno, A., Setou, M. and Ikegami, K. (2012). Ciliary and flagellar structure and function-their regulations by posttranslational modifications of axonemal tubulin. Int Rev Cell Mol Biol 294, 133-170.
84. Kramer-Zucker, A. G., Olale, F., Haycraft, C. J., Yoder, B. K., Schier, A. F. and Drummond, I. A. (2005). Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921.
85. Lai, E., Prezioso, V. R., Smith, E., Litvin, O., Costa, R. H. and Darnell, J. E., Jr (1990). HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev. 4, 1427-1436.
86. Latta, H., Maunsbach, A. B. and Madden, S. C. (1961). Cilia in different segments of the rat nephron. J. Biophys. Biochem. Cytol. 11, 248-252.
87. Laurençon, A., Dubruille, R., Efimenko, E., Grenier, G., Bissett, R., Cortier, E., Rolland, V., Swoboda, P. and Durand, B. (2007). Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species. Genome Biol. 8, R195.
88. Lee, J. H., Silhavy, J. L., Lee, J. E., Al-Gazali, L., Thomas, S., Davis, E. E., Bielas, S. L., Hill, K. J., Iannicelli, M., Brancati, F. et al. (2012). Evolutionarily assembled cis-regulatory module at a human ciliopathy locus. Science 335, 966-969.
89. Lidow, M. S. and Menco, B. P. (1984). Observations on axonemes and membranes of olfactory and respiratory cilia in frogs and rats using tannic acid-supplemented fixation and photographic rotation. J. Ultrastruct. Res. 86, 18-30.
90. Lim, L., Zhou, H. and Costa, R. H. (1997). The winged helix transcription factor HFH-4 is expressed during choroid plexus epithelial development in the mouse embryo. Proc. Natl. Acad. Sci. USA 94, 3094-3099.
91. Lindemann, C. B. and Lesich, K. A. (2010). Flagellar and ciliary beating: the proven and the possible. J. Cell Sci. 123, 519-528.
92. Liu, Y., Pathak, N., Kramer-Zucker, A. and Drummond, I. A. (2007). Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros. Development 134, 1111-1122.
93. Lopes, S. S., Lourenço, R., Pacheco, L., Moreno, N., Kreiling, J. and Saúde, L. (2010). Notch signalling regulates left-right asymmetry through ciliary length control. Development 137, 3625-3632.
94. Luse, S. A. (1956). Electron microscopic observations of the central nervous system. J. Biophys. Biochem. Cytol. 2, 531-542.
95. Ma, L. and Jarman, A. P. (2011). Dilatory is a Drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation. J. Cell Sci. 124, 2622-2630.
96. Ma, M. and Jiang, Y. J. (2007). Jagged2a-notch signaling mediates cell fate choice in the zebrafish pronephric duct. PLoS Genet. 3, e18.
97. Ma, K., Zheng, S. and Zuo, Z. (2006). The transcription factor regulatory factor X1 increases the expression of neuronal glutamate transporter type 3. J. Biol. Chem. 281, 21250-21255.
98. Marcet, B., Chevalier, B., Luxardi, G., Coraux, C., Zaragosi, L. E., Cibois, M., Robbe-Sermesant, K., Jolly, T., Cardinaud, B., Moreilhon, C. et al. (2011). Control of vertebrate multiciliogenesis by miR-449 through direct repression of the Delta/Notch pathway. Nat. Cell Biol. 13, 693-699.
99. Morotomi-Yano, K., Yano, K., Saito, H., Sun, Z., Iwama, A. and Miki, Y. (2002). Human regulatory factor X 4 (RFX4) is a testis-specific dimeric DNA-binding protein that cooperates with other human RFX members. J. Biol. Chem. 277, 836-842.
100. Mukhopadhyay, S., Lu, Y., Qin, H., Lanjuin, A., Shaham, S. and Sengupta, P. (2007). Distinct IFT mechanisms contribute to the generation of ciliary structural diversity in C. elegans. EMBO J. 26, 2966-2980.
101. Murphy, D. B., Seemann, S., Wiese, S., Kirschner, R., Grzeschik, K. H. and Thies, U. (1997). The human hepatocyte nuclear factor 3/fork head gene FKHL13: genomic structure and pattern of expression. Genomics 40, 462-469.
102. Nakagawa, S., Gisselbrecht, S. S., Rogers, J. M., Hartl, D. L. and Bulyk, M. L. (2013). DNA-binding specificity changes in the evolution of forkhead transcription factors. Proc. Natl. Acad. Sci. USA 110, 12349-12354.
103. Narita, K., Kawate, T., Kakinuma, N. and Takeda, S. (2010). Multiple primary cilia modulate the fluid transcytosis in choroid plexus epithelium. Traffic 11, 287-301.
104. Neugebauer, J. M., Amack, J. D., Peterson, A. G., Bisgrove, B. W. and Yost, H. J. (2009). FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 458, 651-654.
105. Newton, F. G., zur Lage, P. I., Karak, S., Moore, D. J., Göpfert, M. C. and Jarman, A. P. (2012). Forkhead transcription factor Fd3F cooperates with Rfx to regulate a gene expression program for mechanosensory cilia specialization. Dev. Cell 22, 1221-1233.
106. Olivier-Mason, A., Wojtyniak, M., Bowie, R. V., Nechipurenko, I. V., Blacque, O. E. and Sengupta, P. (2013). Transmembrane protein OSTA-1 shapes sensory cilia morphology via regulation of intracellular membrane trafficking in C. elegans. Development 140, 1560-1572.
107. Otsuki, K., Hayashi, Y., Kato, M., Yoshida, H. and Yamaguchi, M. (2004). Characterization of dRFX2, a novel RFX family protein in Drosophila. Nucleic Acids Res. 32, 5636-5648.
108. 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.
109. Peters, K. R., Palade, G. E., Schneider, B. G. and Papermaster, D. S. (1983). Fine structure of a periciliary ridge complex of frog retinal rod cells revealed by ultrahigh resolution scanning electron microscopy. J. Cell Biol. 96, 265-276.
110. Phirke, P., Efimenko, E., Mohan, S., Burghoorn, J., Crona, F., Bakhoum, M. W., Trieb, M., Schuske, K., Jorgensen, E. M., Piasecki, B. P. et al. (2011). Transcriptional profiling of C. elegans DAF-19 uncovers a ciliary base-associated protein and a CDK/CCRK/LF2p-related kinase required for intraflagellar transport. Dev. Biol. 357, 235-247.
111. Piasecki, B. P., Burghoorn, J. and Swoboda, P. (2010). Regulatory Factor X (RFX)-mediated transcriptional rewiring of ciliary genes in animals. Proc. Natl. Acad. Sci. USA 107, 12969-12974.
112. Poirier, G. R. and Spink, G. C. (1971). The ultrastructure of testicular spermatozoa in two species of Rana. J. Ultrastruct. Res. 36, 455-465.
113. Praetorius, H. A. and Leipziger, J. (2013). Primary cilium-dependent sensing of urinary flow and paracrine purinergic signaling. Semin. Cell Dev. Biol. 24, 3-10.
114. Purvis, T. L., Hearn, T., Spalluto, C., Knorz, V. J., Hanley, K. P., Sanchez-Elsner, T., Hanley, N. A. and Wilson, D. I. (2010). Transcriptional regulation of the Alström syndrome gene ALMS1 by members of the RFX family and Sp1. Gene 460, 20-29.
115. Ravasi, T., Suzuki, H., Cannistraci, C. V., Katayama, S., Bajic, V. B., Tan, K., Akalin, A., Schmeier, S., Kanamori-Katayama, M., Bertin, N. et al. (2010). An atlas of combinatorial transcriptional regulation in mouse and man. Cell 140, 744-752.
116. Reith, W. and Mach, B. (2001). The bare lymphocyte syndrome and the regulation of MHC expression. Annu. Rev. Immunol. 19, 331-373.
117. Reith, W., Herrero-Sanchez, C., Kobr, M., Silacci, P., Berte, C., Barras, E., Fey, S. and Mach, B. (1990). MHC class II regulatory factor RFX has a novel DNA-binding domain and a functionally independent dimerization domain. Genes Dev. 4, 1528-1540.
118. Reith, W., Kobr, M., Emery, P., Durand, B., Siegrist, C. A. and Mach, B. (1994a). Cooperative binding between factors RFX and X2bp to the X and X2 boxes of MHC class II promoters. J. Biol. Chem. 269, 20020-20025.
119. Reith, W., Ucla, C., Barras, E., Gaud, A., Durand, B., Herrero-Sanchez, C., Kobr, M. and Mach, B. (1994b). RFX1, a transactivator of hepatitis B virus enhancer I, belongs to a novel family of homodimeric and heterodimeric DNA-binding proteins. Mol. Cell. Biol. 14, 1230-1244.
120. Rhodin, J. and Dalhamn, T. (1956). Electron microscopy of the tracheal ciliated mucosa in rat. Z. Zellforsch. Mikrosk. Anat. 44, 345-412.
121. Riparbelli, M. G., Callaini, G. and Megraw, T. L. (2012). Assembly and persistence of primary cilia in dividing Drosophila spermatocytes. Dev. Cell 23, 425-432.
122. Sarmah, B., Winfrey, V. P., Olson, G. E., Appel, B. and Wente, S. R. (2007). A role for the inositol kinase Ipk1 in ciliary beating and length maintenance. Proc. Natl. Acad. Sci. USA 104, 19843-19848.
123. Satir, P. (1995). Landmarks in cilia research from Leeuwenhoek to us. Cell Motil. Cytoskeleton 32, 90-94.
124. Satir, P. and Sleigh, M. A. (1990). The physiology of cilia and mucociliary interactions. Annu. Rev. Physiol. 52, 137-155.
125. Schafer, J. C., Haycraft, C. J., Thomas, J. H., Yoder, B. K. and Swoboda, P. (2003). XBX-1 encodes a dynein light intermediate chain required for retrograde intraflagellar transport and cilia assembly in Caenorhabditis elegans. Mol. Biol. Cell 14, 2057-2070.
126. Schwander, M., Kachar, B. and Müller, U. (2010). Review series: The cell biology of hearing. J. Cell Biol. 190, 9-20.
127. Senti, G. and Swoboda, P. (2008). Distinct isoforms of the RFX transcription factor DAF-19 regulate ciliogenesis and maintenance of synaptic activity. Mol. Biol. Cell 19, 5517-5528.
128. Senti, G., Ezcurra, M., Lobner, J., Schafer, W. R. and Swoboda, P. (2009). Worms with a single functional sensory cilium generate proper neuron-specific behavioral output. Genetics 183, 595-605.
129. 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.
130. Silverman, M. A. and Leroux, M. R. (2009). Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol. 19, 306-316.
131. Sobkowicz, H. M., Slapnick, S. M. and August, B. K. (1995). The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates. J. Neurocytol. 24, 633-653.
132. Song, H., Hu, J., Chen, W., Elliott, G., Andre, P., Gao, B. and Yang, Y. (2010). Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466, 378-382.
133. Sorokin, S. (1962). Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363-377.
134. Sorokin, S. P. (1968). Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3, 207-230.
135. Steimle, V., Durand, B., Barras, E., Zufferey, M., Hadam, M. R., Mach, B. and Reith, W. (1995). A novel DNA-binding regulatory factor is mutated in primary MHC class II deficiency (bare lymphocyte syndrome). Genes Dev. 9, 1021-1032.
136. Steinman, R. M. (1968). An electron microscopic study of ciliogenesis in developing epidermis and trachea in the embryo of Xenopus laevis. Am. J. Anat. 122, 19-55.
137. Stolc, V., Samanta, M. P., Tongprasit, W. and Marshall, W. F. (2005). Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes. Proc. Natl. Acad. Sci. USA 102, 3703-3707.
138. Stubbs, J. L., Oishi, I., Izpisúa Belmonte, J. C. and Kintner, C. (2008). The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat. Genet. 40, 1454-1460.
139. Stubbs, J. L., Vladar, E. K., Axelrod, J. D. and Kintner, C. (2012). Multicilin promotes centriole assembly and ciliogenesis during multiciliate cell differentiation. Nat. Cell Biol. 14, 140-147.
140. Sulik, K., Dehart, D. B., Iangaki, T., Carson, J. L., Vrablic, T., Gesteland, K. and Schoenwolf, G. C. (1994). Morphogenesis of the murine node and notochordal plate. Dev. Dyn. 201, 260-278.
141. Swoboda, P., Adler, H. T. and Thomas, J. H. (2000). The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol. Cell 5, 411-421.
142. Takeda, S. and Narita, K. (2012). Structure and function of vertebrate cilia, towards a new taxonomy. Differentiation 83, S4-S11.
143. Tan, F. E., Vladar, E. K., Ma, L., Fuentealba, L. C., Hoh, R., Espinoza, F. H., Axelrod, J. D., Alvarez-Buylla, A., Stearns, T., Kintner, C. et al. (2013). Myb promotes centriole amplification and later steps of the multiciliogenesis program. Development 140, 4277-4286.
144. Thisse, B., Heyer, V., Lux, A., Alunni, V., Degrave, A., Seiliez, I., Kirchner, J., Parkhill, J. P. and Thisse, C. (2004). Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol. 77, 505-519.
145. Thomas, J., Morlé, L., Soulavie, F., Laurençon, A., Sagnol, S. and Durand, B. (2010). Transcriptional control of genes involved in ciliogenesis: a first step in making cilia. Biol. Cell 102, 499-513.
146. Tichelaar, J. W., Lim, L., Costa, R. H. and Whitsett, J. A. (1999a). HNF-3/forkhead homologue-4 influences lung morphogenesis and respiratory epithelial cell differentiation in vivo. Dev. Biol. 213, 405-417.
147. Tichelaar, J. W., Wert, S. E., Costa, R. H., Kimura, S. and Whitsett, J. A. (1999b). HNF-3/forkhead homologue-4 (HFH-4) is expressed in ciliated epithelial cells in the developing mouse lung. J. Histochem. Cytochem. 47, 823-831.
148. Toyoshima, K. and Shimamura, A. (1982). Comparative study of ultrastructures of the lateral-line organs and the palatal taste organs in the African clawed toad, Xenopus laevis. Anat. Rec. 204, 371-381.
149. Vij, S., Rink, J. C., Ho, H. K., Babu, D., Eitel, M., Narasimhan, V., Tiku, V., Westbrook, J., Schierwater, B. and Roy, S. (2012). Evolutionarily ancient association of the FoxJ1 transcription factor with the motile ciliogenic program. PLoS Genet. 8, e1003019.
150. Walentek, P., Beyer, T., Thumberger, T., Schweickert, A. and Blum, M. (2012). ATP4a is required for Wnt-dependent Foxj1 expression and leftward flow in Xenopus left-right development. Cell Rep 1, 516-527.
151. Wang, J., Schwartz, H. T. and Barr, M. M. (2010). Functional specialization of sensory cilia by an RFX transcription factor isoform. Genetics 186, 1295-1307.
152. Wang, L., Fu, C., Fan, H., Du, T., Dong, M., Chen, Y., Jin, Y., Zhou, Y., Deng, M., Gu, A. et al. (2013). miR-34b regulates multiciliogenesis during organ formation in zebrafish. Development 140, 2755-2764.
153. Ward, S., Thomson, N., White, J. G. and Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans.?2UU. J. Comp. Neurol. 160, 313-337.
154. Waters, A. M. and Beales, P. L. (2011). Ciliopathies: an expanding disease spectrum. Pediatr. Nephrol. 26, 1039-1056.
155. Weigel, D. and Jäckle, H. (1990). The fork head domain: a novel DNA binding motif of eukaryotic transcription factors? Cell 63, 455-456.
156. Weigel, D., Jürgens, G., Küttner, F., Seifert, E. and Jäckle, H. (1989). The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658.
157. Williams, C. L., Winkelbauer, M. E., Schafer, J. C., Michaud, E. J. and Yoder, B. K. (2008). Functional redundancy of the B9 proteins and nephrocystins in Caenorhabditis elegans ciliogenesis. Mol. Biol. Cell 19, 2154-2168.
158. Winkelbauer, M. E., Schafer, J. C., Haycraft, C. J., Swoboda, P. and Yoder, B. K. (2005). The C. elegans homologs of nephrocystin-1 and nephrocystin-4 are cilia transition zone proteins involved in chemosensory perception. J. Cell Sci. 118, 5575-5587.
159. Wolenski, J. S. and Hart, N. H. (1987). Scanning electron microscope studies of sperm incorporation into the zebrafish (Brachydanio) egg. J. Exp. Zool. 243, 259-273.
160. Wolfe, S. A., Wilkerson, D. C., Prado, S. and Grimes, S. R. (2004). Regulatory factor X2 (RFX2) binds to the H1t/TE1 promoter element and activates transcription of the testis-specific histone H1t gene. J. Cell. Biochem. 91, 375-383.
161. Wu, S. Y. and McLeod, M. (1995). The sak1+ gene of Schizosaccharomyces pombe encodes an RFX family DNA-binding protein that positively regulates cyclic AMPdependent protein kinase-mediated exit from the mitotic cell cycle. Mol. Cell. Biol. 15, 1479-1488.
162. You, Y., Huang, T., Richer, E. J., Schmidt, J. E., Zabner, J., Borok, Z. and Brody, S. L. (2004). Role of f-box factor foxj1 in differentiation of ciliated airway epithelial cells. Am. J. Physiol. 286, L650-L657.
163. Yu, H., Pretot, R. F., Burglin, T. R. and Sternberg, P. W. (2003). Distinct roles of transcription factors EGL-46 and DAF-19 in specifying the functionality of a polycystin-expressing sensory neuron necessary for C. elegans male vulva location behavior. Development 130, 5217-5227.
164. Yu, X., Ng, C. P., Habacher, H. and Roy, S. (2008). Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat. Genet. 40, 1445-1453.
165. Yu, X., Lau, D., Ng, C. P. and Roy, S. (2011). Cilia-driven fluid flow as an epigenetic cue for otolith biomineralization on sensory hair cells of the inner ear. Development 138, 487-494.
166. Zhang, D., Stumpo, D. J., Graves, J. P., DeGraff, L. M., Grissom, S. F., Collins, J. B., Li, L., Zeldin, D. C. and Blackshear, P. J. (2006). Identification of potential target genes for RFX4_v3, a transcription factor critical for brain development. J. Neurochem. 98, 860-875.
167. Zhao, H., Zhu, L., Zhu, Y., Cao, J., Li, S., Huang, Q., Xu, T., Huang, X., Yan, X. and Zhu, X. (2013). The Cep63 paralogue Deup1 enables massive de novo centriole biogenesis for vertebrate multiciliogenesis. Nat. Cell Biol. 15, 1434-1444.