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Evolutionarily Ancient Association of the FoxJ1 Transcription Factor with the Motile Ciliogenic Program


It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved structure, and their mechanism of motility, the evolution of the transcriptional program controlling ciliogenesis has remained incompletely understood. In particular, it is presently not known how the generation of motile cilia is programmed outside of the vertebrates, and whether and to what extent the FoxJ1-dependent regulation is conserved. We have performed a survey of numerous eukaryotic genomes and discovered that genes homologous to foxJ1 are restricted only to organisms belonging to the unikont lineage. Using a mis-expression assay, we then obtained evidence of a conserved ability of FoxJ1 proteins from a number of diverse phyletic groups to activate the expression of a host of motile ciliary genes in zebrafish embryos. Conversely, we found that inactivation of a foxJ1 gene in Schmidtea mediterranea, a platyhelminth (flatworm) that utilizes motile cilia for locomotion, led to a profound disruption in the differentiation of motile cilia. Together, all of these findings provide the first evolutionary perspective into the transcriptional control of motile ciliogenesis and allow us to propose a conserved FoxJ1-regulated mechanism for motile cilia biogenesis back to the origin of the metazoans.


Vyšlo v časopise: Evolutionarily Ancient Association of the FoxJ1 Transcription Factor with the Motile Ciliogenic Program. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003019
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003019

Souhrn

It is generally believed that the last eukaryotic common ancestor (LECA) was a unicellular organism with motile cilia. In the vertebrates, the winged-helix transcription factor FoxJ1 functions as the master regulator of motile cilia biogenesis. Despite the antiquity of cilia, their highly conserved structure, and their mechanism of motility, the evolution of the transcriptional program controlling ciliogenesis has remained incompletely understood. In particular, it is presently not known how the generation of motile cilia is programmed outside of the vertebrates, and whether and to what extent the FoxJ1-dependent regulation is conserved. We have performed a survey of numerous eukaryotic genomes and discovered that genes homologous to foxJ1 are restricted only to organisms belonging to the unikont lineage. Using a mis-expression assay, we then obtained evidence of a conserved ability of FoxJ1 proteins from a number of diverse phyletic groups to activate the expression of a host of motile ciliary genes in zebrafish embryos. Conversely, we found that inactivation of a foxJ1 gene in Schmidtea mediterranea, a platyhelminth (flatworm) that utilizes motile cilia for locomotion, led to a profound disruption in the differentiation of motile cilia. Together, all of these findings provide the first evolutionary perspective into the transcriptional control of motile ciliogenesis and allow us to propose a conserved FoxJ1-regulated mechanism for motile cilia biogenesis back to the origin of the metazoans.


Zdroje

1. SatirP, ChristensenST (2007) Overview of structure and function of mammalian cilia. Annu Rev Physiol 69: 377–400.

2. IshikawaH, MarshallWF (2011) Ciliogenesis: building the cell's antenna. Nat Rev Mol Cell Biol 12: 222–234.

3. FliegaufM, BenzingT, OmranH (2007) When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8: 880–893.

4. BakerK, BealesPL (2009) Making sense of cilia in disease: the human ciliopathies. Am J Med Genet C Semin Med Genet 151C: 281–295.

5. RoyS (2009) The motile cilium in development and disease: emerging new insights. Bioessays 31: 694–699.

6. ThomasJ, MorleL, SoulavieF, LaurenconA, SagnolS, et al. (2010) Transcriptional control of genes involved in ciliogenesis: a first step in making cilia. Biol Cell 102: 499–513.

7. BlacqueOE, PerensEA, BoroevichKA, InglisPN, LiC, et al. (2005) Functional genomics of the cilium, a sensory organelle. Curr Biol 15: 935–941.

8. ChenN, MahA, BlacqueOE, ChuJ, PhgoraK, et al. (2006) Identification of ciliary and ciliopathy genes in Caenorhabditis elegans through comparative genomics. Genome Biol 7: R126.

9. EfimenkoE, BubbK, MakHY, HolzmanT, LerouxMR, et al. (2005) Analysis of xbx genes in C. elegans. Development 132: 1923–1934.

10. LaurenconA, DubruilleR, EfimenkoE, GrenierG, BissettR, et al. (2007) Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species. Genome Biol 8: R195.

11. SwobodaP, AdlerHT, ThomasJH (2000) The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 5: 411–421.

12. Ait-LounisA, BaasD, BarrasE, BenadibaC, CharollaisA, et al. (2007) Novel function of the ciliogenic transcription factor RFX3 in development of the endocrine pancreas. Diabetes 56: 950–959.

13. BonnafeE, ToukaM, AitLounisA, BaasD, BarrasE, et al. (2004) The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol Cell Biol 24: 4417–4427.

14. DornA, DurandB, MarfingC, Le MeurM, BenoistC, et al. (1987) Conserved major histocompatibility complex class II boxes–X and Y–are transcriptional control elements and specifically bind nuclear proteins. Proc Natl Acad Sci U S A 84: 6249–6253.

15. CruzC, RibesV, KutejovaE, CayusoJ, LawsonV, et al. (2010) FoxJ1 regulates floor plate cilia architecture and modifies the response of cells to sonic hedgehog signalling. Development 137: 4271–4282.

16. StubbsJL, OishiI, Izpisua BelmonteJC, KintnerC (2008) The forkhead protein FoxJ1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat Genet 40: 1454–1460.

17. YuX, NgCP, HabacherH, RoyS (2008) FoxJ1 transcription factors are master regulators of the motile ciliogenic program. Nat Genet 40: 1445–1453.

18. AltenL, Schuster-GosslerK, BeckersA, GroosS, UlmerB, et al. (2012) Differential regulation of node formation, nodal ciliogenesis and cilia positioning by Noto and FoxJ1. Development 139: 1276–1284.

19. ChuJS, BaillieDL, ChenN (2010) Convergent evolution of RFX transcription factors and ciliary genes predated the origin of metazoans. BMC Evol Biol 10: 130.

20. PiaseckiBP, BurghoornJ, SwobodaP (2010) Regulatory Factor X (RFX)-mediated transcriptional rewiring of ciliary genes in animals. Proc Natl Acad Sci U S A 107: 12969–12974.

21. Mitchell DR (2006) The evolution of eukaryotic cilia and flagella as motile and sensory organelles. In: Jékely G, editors. Origins and Evolution of Eukaryotic Endomembranes and Cytoskeleton. Eurekah.com. pp 1–11.

22. BrodySL, YanXH, WuerffelMK, SongSK, ShapiroSD (2000) Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23: 45–51.

23. ChenJ, KnowlesHJ, HebertJL, HackettBP (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.

24. Ait-LounisA, BonalC, Seguin-EstevezQ, SchmidCD, BucherP, et al. (2010) The transcription factor Rfx3 regulates beta-cell differentiation, function, and glucokinase expression. Diabetes 59: 1674–1685.

25. HannenhalliS, KaestnerKH (2009) The evolution of Fox genes and their role in development and disease. Nat Rev Genet 10: 233–240.

26. LarrouxC, LukeGN, KoopmanP, RokhsarDS, ShimeldSM, et al. (2008) Genesis and expansion of metazoan transcription factor gene classes. Mol Biol Evol 25: 980–996.

27. DellaportaSL, XuA, SagasserS, JakobW, MorenoMA, et al. (2006) Mitochondrial genome of Trichoplax adhaerens supports placozoa as the basal lower metazoan phylum. Proc Natl Acad Sci U S A 103: 8751–8756.

28. SchierwaterB (2005) My favorite animal, Trichoplax adhaerens. Bioessays 27: 1294–1302.

29. SchierwaterB, EitelM, JakobW, OsigusHJ, HadrysH, et al. (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7: e20 doi:10.1371/journal.pbio.1000020.

30. PhilippeH, DerelleR, LopezP, PickK, BorchielliniC, et al. (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19: 706–712.

31. SrivastavaM, BegovicE, ChapmanJ, PutnamNH, HellstenU, et al. (2008) The Trichoplax genome and the nature of placozoans. Nature 454: 955–960.

32. ClevidenceDE, OverdierDG, PetersonRS, PorcellaA, YeH, et al. (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.

33. LimL, ZhouH, CostaRH (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.

34. TuQ, BrownCT, DavidsonEH, OliveriP (2006) Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev Biol 300: 49–62.

35. RompolasP, Patel-KingRS, KingSM (2009) Schmidtea mediterranea: a model system for analysis of motile cilia. Methods Cell Biol 93: 81–98.

36. RinkJC, GurleyKA, ElliottSA, Sanchez AlvaradoA (2009) Planarian Hh signaling regulates regeneration polarity and links Hh pathway evolution to cilia. Science 326: 1406–1410.

37. RinkJC, VuHT, AlvaradoAS (2011) The maintenance and regeneration of the planarian excretory system are regulated by EGFR signaling. Development 138: 3769–3780.

38. ShimeldSM, DegnanB, LukeGN (2010) Evolutionary genomics of the Fox genes: origin of gene families and the ancestry of gene clusters. Genomics 95: 256–260.

39. Sebe-PedrosA, de MendozaA, LangBF, DegnanBM, Ruiz-TrilloI (2011) Unexpected repertoire of metazoan transcription factors in the unicellular holozoan Capsaspora owczarzaki. Mol Biol Evol 28: 1241–1254.

40. Kramer-ZuckerAG, OlaleF, HaycraftCJ, YoderBK, SchierAF, et al. (2005) Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132: 1907–1921.

41. ChoiVM, HarlandRM, KhokhaMK (2006) Developmental expression of FoxJ1.2, FoxJ2 and FoxQ1 in Xenopus tropicalis. Gene Expr Patterns 6: 443–447.

42. PohlBS, KnöchelW (2004) Isolation and developmental expression of Xenopus FoxJ1 and FoxK1. Dev Genes Evol 214: 200–205.

43. YuX, LauD, NgCP, RoyS (2011) Cilia-driven fluid flow as an epigenetic cue for otolith biomineralization on sensory hair cells of the inner ear. Development 138: 487–494.

44. MolinaMD, SaloE, CebriaF (2009) Expression pattern of the expanded noggin gene family in the planarian Schmidtea mediterranea. Gene Expr Patterns 9: 246–253.

45. GurleyKA, ElliottSA, SimakovO, SchmidtHA, HolsteinTW, et al. (2010) Expression of secreted Wnt pathway components reveals unexpected complexity of the planarian amputation response. Dev Biol 347: 24–39.

46. ChaiG, MaC, BaoK, ZhengL, WangX, et al. (2010) Complete functional segregation of planarian beta-catenin-1 and -2 in mediating Wnt signaling and cell adhesion. J Biol Chem 285: 24120–24130.

47. El ZeinL, Ait-LounisA, MorleL, ThomasJ, ChhinB, et al. (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.

48. ThompsonJD, HigginsDG, GibsonTJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.

49. PageRD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358.

50. EitelM, SchierwaterB (2010) The phylogeography of the Placozoa suggests a taxon rich phylum in tropical and subtropical waters. Molecular Ecology 19: 2315–2327.

51. EitelM, GuidiL, HadrysH, BalsamoM, SchierwaterB (2011) New insights into placozoan sexual reproduction and development. PLoS ONE 6: e19639 doi:10.1371/journal.pone.0019639.

52. GurleyKA, RinkJC, Sanchez AlvaradoA (2008) Beta-catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319: 323–327.

53. PearsonBJ, EisenhofferGT, GurleyKA, RinkJC, MillerDE, et al. (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238: 443–450.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 11
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