RFX3 governs growth and beating efficiency of motile cilia in mouse and controls the expression of genes involved in human ciliopathies

Journal of Cell Science

Volumn 122, Issue 17, 2009, Pages 3180-3189

  El Zein, Loubna ^a,d   Ait Lounis, Aouatef ^b   Morlé, Laurette ^a,d   Thomas, Joëlle ^a,d   Chhin, Brigitte ^a,d   Spassky, Nathalie ^c   Reith, Walter ^b   Durand, Bénédicte ^a,d  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Axonemal dyneins; Cilia; Mouse primary cell cultures; Primary ciliary dyskinesia; RFX proteins

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXJ1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL GROWTH; CELL MOTILITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CILIARY DYSKINESIA; CILIOPATHY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING;

CAENORHABDITIS ELEGANS; MUS;

EID: 70350362831     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.048348     Document Type: Article

References (73)

1. 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.
2. Ait-Lounis, A., Baas, D., Barras, E., Benadiba, C., Charollais, A., Nlend Nlend, R., Liegeois, 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.
3. Andersen, J. S., Wilkinson, C. J., Mayor, T., Mortensen, P., Nigg, E. A. and Mann, M. (2003). Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574.
4. 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.
5. 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.
6. 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.
7. Bartoloni, L., Blouin, J. L., Pan, Y., Gehrig, C., Maiti, A. K., Scamuffa, N., Rossier, C., Jorissen, M., Armengot, M., Meeks, M. et al. (2002). Mutations in the DNAH11 (axonemal heavy chain dynein type 11) gene cause one form of situs inversus totalis and most likely primary ciliary dyskinesia. Proc. Natl. Acad. Sci. USA 99, 10282-10286.
8. 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.
9. Bisgrove, B. W. and Yost, H. J. (2006). The roles of cilia in developmental disorders and disease. Development 133, 4131-4143.
10. 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.
11. 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.
12. 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.
13. 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.
14. Bonneau, D., Raymond, F., Kremer, C., Klossek, J. M., Kaplan, J. and Patte, F. (1993). Usher syndrome type I associated with bronchiectasis and immotile nasal cilia in two brothers. J. Med. Genet. 30, 253-254.
15. 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. et al. (2006). Flagellar motility is required for the viability of the bloodstream trypanosome. Nature 440, 224-227.
16. 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.
17. Calaora, V., Chazal, G., Nielsen, P. J., Rougon, G. and Moreau, H. (1996). mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult. Neuroscience 73, 581-594.
18. Carson, J. L., Reed, W., Lucier, T., Brighton, L., Gambling, T. M., Huang, C. H. and Collier, A. M. (2002). Axonemal dynein expression in human fetal tracheal epithelium. Am. J. Physiol. Lung Cell Mol. Physiol. 282, L421-L430.
19. 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.
20. Chen, N., Mah, A., Blacque, O. E., Chu, J., Phgora, K., Bakhoum, M. W., Hunt 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.
21. Driscoll, J. A., Bhalla, S., Liapis, H., Ibricevic, A. and Brody, S. L. (2008). Autosomal dominant polycystic kidney disease is associated with an increased prevalence of radiographic bronchiectasis. Chest 133, 1181-1188.
22. Dubruille, R., Laurencon, 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.
23. 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.
24. 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 orthologue of human WDR19, is a component of the intraflagellar transport machinery in sensory cilia. Mol. Biol. Cell 17, 4801-4811.
25. Eggenschwiler, J. T. and Anderson, K. V. (2007). Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23, 345-373.
26. Emery, P., Durand, B., Mach, B. and Reith, W. (1996a). RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res. 24, 803-807.
27. Emery, P., Strubin, M., Hofmann, K., Bucher, P., Mach, B. and Reith, W. (1996b). A consensus motif in the RFX DNA binding domain and binding domain mutants with altered specificity. Mol. Cell. Biol. 16, 4486-4494.
28. Fliegauf, M., Olbrich, H., Horvath, J., Wildhaber, J. H., Zariwala, M. A., Kennedy, M., Knowles, M. R. and Omran, H. (2005). Mislocalization of DNAH5 and DNAH9 in Respiratory Cells from Patients with Primary Ciliary Dyskinesia. Am. J. Respir. Crit. Care Med. 171, 1343-1349.
29. Fliegauf, M., Benzing, T. and Omran, H. (2007). When cilia go bad: cilia defects and ciliopathies. Nat. Rev. Mol. Cell Biol. 8, 880-893.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. Haycraft, C. J., Schafer, J. C., Zhang, Q., Taulman, P. D. and Yoder, B. K. (2003). Identification of CHE-13, a novel intraflagellar transport protein required for cilia formation. Exp. Cell Res. 284, 249-261.
36. Hayes, J. M., Kim, S. K., Abitua, P. B., Park, T. J., Herrington, E. R., Kitayama, A., Grow, M. W., Ueno, N. and Wallingford, J. B. (2007). Identification of novel ciliogenesis factors using a new in vivo model for mucociliary epithelial development. Dev. Biol. 312, 115-130.
37. Huang, T., You, Y., Spoor, M. S., Richer, E. J., Kudva, V. V., Paige, R. C., Seiler, M. P., Liebler, J. M., Zabner, J., Plopper, C. G. et al. (2003). Foxj1 is required for apical localization of ezrin in airway epithelial cells. J. Cell Sci. 116, 4935-4945.
38. Ibanez-Tallon, I., Gorokhova, S. and Heintz, N. (2002). Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum. Mol. Genet. 11, 715-721.
39. Inglis, P. N., Boroevich, K. A. and Leroux, M. R. (2006). Piecing together a ciliome. Trends Genet. 22, 491-500.
40. 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.
41. Koudritsky, M. and Domany, E. (2008). Positional distribution of human transcription factor binding sites. Nucleic Acids Res. 36, 6795-6805.
42. Laurencon, 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.
43. Li, J. B., 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.
44. 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.
45. Lonergan, K. M., Chari, R., Deleeuw, R. J., Shadeo, A., Chi, B., Tsao, M. S., Jones, S., Marra, M., Ling, V., Ng, R. et al. (2006). Identification of novel lung genes in bronchial epithelium by serial analysis of gene expression. Am. J. Respir. Cell Mol. Biol. 35, 651-661.
46. Marshall, W. F. (2008). The cell biological basis of ciliary disease. J. Cell Biol. 180, 17-21.
47. Masternak, K. and Reith, W. (2002). Promoter-specific functions of CIITA and the MHC class II enhanceosome in transcriptional activation. EMBO J. 21, 1379-1388.
48. McClintock, T. S., Glasser, C. E., Bose, S. C. and Bergman, D. A. (2008). Tissue expression patterns identify mouse cilia genes. Physiol. Genomics 32, 198-206.
49. Moore, A., Escudier, E., Roger, G., Tamalet, A., Pelosse, B., Marlin, S., Clement, A., Geremek, M., Delaisi, B., Bridoux, A. M. et al. (2006). RPGR is mutated in patients with a complex X linked phenotype combining primary ciliary dyskinesia and retinitis pigmentosa. J. Med. Genet. 43, 326-333.
50. Olbrich, H., Haffner, K., Kispert, A., Volkel, A., Volz, A., Sasmaz, G., Reinhardt, R., Hennig, S., Lehrach, H., Konietzko, N. et al. (2002). Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat. Genet. 30, 143-144.
51. Osman, E. M., Abboud, O. I., Sulaiman, S. M., Musa, A. R., Beleil, O. M. and Sharfi, A. A. (1991). End-stage renal failure in Kartagener's syndrome. Nephrol. Dial. Transplant. 6, 747.
52. 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.
53. Pazour, G. J., Agrin, N., Leszyk, J. and Witman, G. B. (2005). Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170, 103-113.
54. Rebeiz, M. and Posakony, J. W. (2004). GenePalette: a universal software tool for genome sequence visualization and analysis. Dev. Biol. 271, 431-438.
55. Reith, W., Ucla, C., Barras, E., Gaud, A., Durand, B., Herrero-Sanchez, C., Kobr, M. and Mach, B. (1994). 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.
56. Ross, A. J., Dailey, L. A., Brighton, L. E. and Devlin, R. B. (2007). Transcriptional profiling of mucociliary differentiation in human airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 37, 169-185.
57. Schafer, J. A., Haycraft, C. J., Thomas, J. H., Yoder, B. K. and Swoboda, P. (2003). xbx-1 encodes a dynein light intermediate chain (DLIC) required for retrograde intraflagellar transport and cilia assembly in C. elegans. Mol. Biol. Cell 14, 2057-2070.
58. Schwabe, G. C., Hoffmann, K., Loges, N. T., Birker, D., Rossier, C., de Santi, M. M., Olbrich, H., Fliegauf, M., Failly, M., Liebers, U. et al. (2008). Primary ciliary dyskinesia associated with normal axoneme ultrastructure is caused by DNAH11 mutations. Hum. Mutat. 29, 289-298.
59. Shah, A. S., Farmen, S. L., Moninger, T. O., Businga, T. R., Andrews, M. P., Bugge, K., Searby, C. C., Nishimura, D., Brogden, K. A., Kline, J. N. et al. (2008). Loss of Bardet-Biedl syndrome proteins alters the morphology and function of motile cilia in airway epithelia. Proc. Natl. Acad. Sci. USA 105, 3380-3385.
60. Singla, V. and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
61. Spassky, N., Merkle, F. T., Flames, N., Tramontin, A. D., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (2005). Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J. Neurosci. 25, 10-18.
62. 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.
63. Stubbs, J. L., Oishi, I., Izpisua 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.
64. Supp, D. M., Witte, D. P., Potter, S. S. and Brueckner, M. (1997). Mutation of an axonemal dynein affects left-right asymmetri in inersus viscerum mice. Nature 389, 963-966.
65. 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.
66. Tabach, Y., Brosh, R., Buganim, Y., Reiner, A., Zuk, O., Yitzhaky, A., Koudritsky, M., Rotter, V. and Domany, E. (2007). Wide-scale analysis of human functional transcription factor binding reveals a strong bias towards the transcription start site. PLoS ONE 2, e807.
67. Tichelaar, J. W., Wert, S. E., Costa, R. H., Kimura, S. and Whitsett, J. A. (1999). HNF-3/forkhead homologue-4 (HFH-4) is expressed in ciliated epithelial cells in the developing mouse lung. J. Histochem. Cytochem. 47, 823-832.
68. Toskala, E., Smiley-Jewell, S. M., Wong, V. J., King, D. and Plopper, C. G. (2005). Temporal and spatial distribution of ciliogenesis in the tracheobronchial airways of mice. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L454-L459.
69. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, RESEARCH0034.
70. Whitsett, J. A. and Tichelaar, J. W. (1999). Forkhead transcription factor HFH-4 and respiratory epithelial cell differentiation. Am. J. Respir. Cell Mol. Biol. 21, 153-154.
71. 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. Lung Cell Mol. Physiol. 286, L650-L657.
72. 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.
73. Zhang, D., Zeldin, D. C. and Blackshear, P. J. (2007). Regulatory factor X4 variant 3, a transcription factor involved in brain development and disease. J. Neurosci. Res. 85, 3515-3522.