Forkhead Transcription Factor Fd3F Cooperates with Rfx to Regulate a Gene Expression Program for Mechanosensory Cilia Specialization

Developmental Cell

Volumn 22, Issue 6, 2012, Pages 1221-1233

  Newton, Fay G ^a   zur Lage, Petra I ^a   Karak, Somdatta ^b   Moore, Daniel J ^a   Göpfert, Martin C ^b   Jarman, Andrew P ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FD3F PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; RFX PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR;

ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; DROSOPHILA; EUKARYOTIC FLAGELLUM; GENE EXPRESSION REGULATION; GENE TRANSFER; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CILIA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; MECHANOTRANSDUCTION, CELLULAR; NEUROGENESIS; TRANSCRIPTION FACTORS;

EID: 84862124475     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.05.010     Document Type: Article

References (45)

1. Amos L.A. The tektin family of microtubule-stabilizing proteins. Genome Biol. 2008, 9:229.
2. Avidor-Reiss T., Maer A.M., Koundakjian E., Polyanovsky A., Keil T., Subramaniam S., Zuker C.S. Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 2004, 117:527-539.
3. Baas D., Meiniel A., Benadiba C., Bonnafe E., Meiniel O., Reith W., Durand B. A deficiency in RFX3 causes hydrocephalus associated with abnormal differentiation of ependymal cells. Eur. J. Neurosci. 2006, 24:1020-1030.
4. Benayoun B.A., Caburet S., Veitia R.A. Forkhead transcription factors: key players in health and disease. Trends Genet. 2011, 27:224-232.
5. Bonnafe E., Touka M., AitLounis A., Baas D., Barras E., Ucla C., Moreau A., Flamant F., Dubruille R., Couble P., et al. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Cell. Biol. 2004, 24:4417-4427.
6. Brody S.L., Yan X.H., Wuerffel M.K., Song S.K., Shapiro S.D. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am. J. Respir. Cell Mol. Biol. 2000, 23:45-51.
7. Cachero S., Simpson T.I., Zur Lage P.I., Ma L., Newton F.G., Holohan E.E., Armstrong J.D., Jarman A.P. The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons. PLoS Biol. 2011, 9:e1000568.
8. Cheng L.E., Song W., Looger L.L., Jan L.Y., Jan Y.N. The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron 2010, 67:373-380.
9. Chu J.S., Baillie D.L., Chen N. Convergent evolution of RFX transcription factors and ciliary genes predated the origin of metazoans. BMC Evol. Biol. 2010, 10:130.
10. Cruz C., Ribes V., Kutejova E., Cayuso J., Lawson V., Norris D., Stevens J., Davey M., Blight K., Bangs F., et al. Foxj1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 2010, 137:4271-4282.
11. Dubruille R., Laurençon A., Vandaele C., Shishido E., Coulon-Bublex M., Swoboda P., Couble P., Kernan M., Durand B. Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 2002, 129:5487-5498.
12. Eberl D.F., Hardy R.W., Kernan M.J. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 2000, 20:5981-5988.
13. Effertz T., Wiek R., Göpfert M.C. NompC TRP channel is essential for Drosophila sound receptor function. Curr. Biol. 2011, 21:592-597.
14. Efimenko E., Bubb K., Mak H.Y., Holzman T., Leroux M.R., Ruvkun G., Thomas J.H., Swoboda P. Analysis of xbx genes in C. elegans. Development 2005, 132:1923-1934.
15. El Zein L., Ait-Lounis A., Morlé L., Thomas J., Chhin B., Spassky N., Reith W., Durand B. RFX3 governs growth and beating efficiency of motile cilia in mouse and controls the expression of genes involved in human ciliopathies. J. Cell Sci. 2009, 122:3180-3189.
16. Emery P., Strubin M., Hofmann K., Bucher P., Mach B., Reith W. A consensus motif in the RFX DNA binding domain and binding domain mutants with altered specificity. Mol. Cell. Biol. 1996, 16:4486-4494.
17. Gong Z., Son W., Chung Y.D., Kim J., Shin D.W., McClung C.A., Lee Y., Lee H.W., Chang D.-J., Kaang B.K., et al. Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 2004, 24:9059-9066.
18. Göpfert M.C., Robert D. Motion generation by Drosophila mechanosensory neurons. Proc. Natl. Acad. Sci. USA 2003, 100:5514-5519.
19. Göpfert M.C., Humphris A.D., Albert J.T., Robert D., Hendrich O. Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proc. Natl. Acad. Sci. USA 2005, 102:325-330.
20. Göpfert M.C., Albert J.T., Nadrowski B., Kamikouchi A. Specification of auditory sensitivity by Drosophila TRP channels. Nat. Neurosci. 2006, 9:999-1000.
21. Han Y.G., Kwok B.H., Kernan M.J. Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr. Biol. 2003, 13:1679-1686.
22. Hansen I.A., Sieglaff D.H., Munro J.B., Shiao S.H., Cruz J., Lee I.W., Heraty J.M., Raikhel A.S. Forkhead transcription factors regulate mosquito reproduction. Insect Biochem. Mol. Biol. 2007, 37:985-997.
23. Hou Y., Pazour G.J., Witman G.B. A dynein light intermediate chain, D1bLIC, is required for retrograde intraflagellar transport. Mol. Biol. Cell 2004, 15:4382-4394.
24. Ishikawa H., Marshall W.F. Ciliogenesis: building the cell's antenna. Nat. Rev. Mol. Cell Biol. 2011, 12:222-234.
25. Iwama A., Pan J., Zhang P., Reith W., Mach B., Tenen D.G., Sun Z. 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. 1999, 19:3940-3950.
26. Jacquet B.V., Salinas-Mondragon R., Liang H., Therit B., Buie J.D., Dykstra M., Campbell K., Ostrowski L.E., Brody S.L., Ghashghaei H.T. FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 2009, 136:4021-4031.
27. Kamiya R. Mutations at twelve independent loci result in absence of outer dynein arms in Chylamydomonas reinhardtii. J. Cell Biol. 1988, 107:2253-2258.
28. Kaufmann E., Müller D., Knöchel W. DNA recognition site analysis of Xenopus winged helix proteins. J. Mol. Biol. 1995, 248:239-254.
29. Kavlie R.G., Kernan M.J., Eberl D.F. Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 2010, 185:177-188.
30. Kernan M., Cowan D., Zuker C. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 1994, 12:1195-1206.
31. Kim J., Chung Y.D., Park D.Y., Choi S.K., Shin D.W., Soh H., Lee H.W., Son W., Yim J., Park C.S., et al. A TRPV family ion channel required for hearing in Drosophila. Nature 2003, 424:81-84.
32. Larroux C., Luke G.N., Koopman P., Rokhsar D.S., Shimeld S.M., Degnan B.M. Genesis and expansion of metazoan transcription factor gene classes. Mol. Biol. Evol. 2008, 25:980-996.
33. Laurençon A., Dubruille R., Efimenko E., Grenier G., Bissett R., Cortier E., Rolland V., Swoboda P., Durand B. Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species. Genome Biol. 2007, 8:R195.
34. Lee E., Sivan-Loukianova E., Eberl D.F., Kernan M.J. An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr. Biol. 2008, 18:1899-1906.
35. Lee H.H., Frasch M. Survey of forkhead domain encoding genes in the Drosophila genome: Classification and embryonic expression patterns. Dev. Dyn. 2004, 229:357-366.
36. Liang X., Madrid J., Saleh H.S., Howard J. NOMPC, a member of the TRP channel family, localizes to the tubular body and distal cilium of Drosophila campaniform and chordotonal receptor cells. Cytoskeleton (Hoboken) 2011, 68:1-7.
37. Mazet F., Yu J.K., Liberles D.A., Holland L.Z., Shimeld S.M. Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene 2003, 316:79-89.
38. Nadrowski B., Albert J.T., Göpfert M.C. Transducer-based force generation explains active process in Drosophila hearing. Curr. Biol. 2008, 18:1365-1372.
39. Pazour G.J., Wilkerson C.G., Witman G.B. A dynein light chain is essential for the retrograde particle movement of intraflagellar transport (IFT). J. Cell Biol. 1998, 141:979-992.
40. Piasecki B.P., Burghoorn J., Swoboda P. Regulatory Factor X (RFX)-mediated transcriptional rewiring of ciliary genes in animals. Proc. Natl. Acad. Sci. USA 2010, 107:12969-12974.
41. Silverman M.A., Leroux M.R. Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol. 2009, 19:306-316.
42. Stubbs J.L., Oishi I., Izpisúa Belmonte J.C., Kintner C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat. Genet. 2008, 40:1454-1460.
43. Thomas J., Morlé L., Soulavie F., Laurençon A., Sagnol S., Durand B. Transcriptional control of genes involved in ciliogenesis: a first step in making cilia. Biol. Cell 2010, 102:499-513.
44. Wang J., Schwartz H.T., Barr M.M. Functional specialization of sensory cilia by an RFX transcription factor isoform. Genetics 2010, 186:1295-1307.
45. Yu X., Ng C.P., Habacher H., Roy S. Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nat. Genet. 2008, 40:1445-1453.