Wnt/β-catenin signaling directly regulates Foxj1 expression and ciliogenesis in zebrafish Kupffer's vesicle

Development

Volumn 139, Issue 3, 2012, Pages 514-524

  Caron, Alissa ^a   Xu, Xiaolei ^a   Lin, Xueying ^a  

^a MAYO GRADUATE SCHOOL   (United States)

Author keywords

Ciliogenesis; Foxj1; Kupffer's vesicle zebrafish; Wnt catenin signaling

Indexed keywords

BETA CATENIN; PROTEIN FOXJ1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DOWN REGULATION; EUKARYOTIC FLAGELLUM; GENE EXPRESSION REGULATION; GENE LOSS; GENE OVEREXPRESSION; KIDNEY CYST; KUPFFER CELL; NONHUMAN; OTOLITH; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ZEBRA FISH;

ANIMALS; BETA CATENIN; BODY PATTERNING; CELL MOVEMENT; CILIA; CYTOSKELETAL PROTEINS; DOWN-REGULATION; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KIDNEY DISEASES, CYSTIC; KUPFFER CELLS; OTOLITHIC MEMBRANE; T CELL TRANSCRIPTION FACTOR 1; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT SIGNALING PATHWAY; WNT3A PROTEIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO;

EID: 84855433919     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.071746     Document Type: Article

References (81)

1. Aamar, E. and Dawid, I. B. (2008). Isolation and expression analysis of foxj1 and foxj1.2 in zebrafish embryos. Int. J. Dev. Biol. 52, 985-991.
2. Afzelius, B. A. (1976). A human syndrome caused by immotile cilia. Science 193, 317-319.
3. Alexander, J., Rothenberg, M., Henry, G. L. and Stainier, D. Y. (1999). Casanova plays an early and essential role in endoderm formation in zebrafish. Dev. Biol. 215, 343-357.
4. Amack, J. D. and Yost, H. J. (2004). The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr. Biol. 14, 685-690.
5. Badano, J. L., Mitsuma, N., Beales, P. L. and Katsanis, N. (2006). The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148.
6. 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.
7. Borovina, A., Superina, S., Voskas, D. and Ciruna, B. (2010). Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol. 12, 407-412.
8. Carl, M., Bianco, I. H., Bajoghli, B., Aghaallaei, N., Czerny, T. and Wilson, S. W. (2007). Wnt/Axin1/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of CNS asymmetries. Neuron 55, 393-405.
9. 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.
10. Colantonio, J. R., Vermot, J., Wu, D., Langenbacher, A. D., Fraser, S., Chen, J. N. and Hill, K. L. (2009). The dynein regulatory complex is required for ciliary motility and otolith biogenesis in the inner ear. Nature 457, 205-209.
11. Cooper, M. S. and D'Amico, L. A. (1996). A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 180, 184-198.
12. Corbit, K. C., Shyer, A. E., Dowdle, W. E., Gaulden, J., Singla, V., Chen, M. H., Chuang, P. T. and Reiter, J. F. (2008). Kif3a constrains beta-catenin-dependent Wnt signalling through dual ciliary and non-ciliary mechanisms. Nat. Cell Biol. 10, 70-76.
13. 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.
14. Eggenschwiler, J. T. and Anderson, K. V. (2007). Cilia and developmental signaling. Annu. Rev. Cell Dev. Biol. 23, 345-373.
15. El Zein, L., Ait-Lounis, A., Morle, 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.
16. Eley, L., Yates, L. M. and Goodship, J. A. (2005). Cilia and disease. Curr. Opin. Genet. Dev. 15, 308-314.
17. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. and Yost, H. J. (2005). Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132, 1247-1260.
18. Freisinger, C. M., Fisher, R. A. and Slusarski, D. C. (2010). Regulator of g protein signaling 3 modulates wnt5b calcium dynamics and somite patterning. PLoS Genet. 6, e1001020.
19. Fukukawa, C., Nagayama, S., Tsunoda, T., Toguchida, J., Nakamura, Y. and Katagiri, T. (2009). Activation of the non-canonical Dvl-Rac1-JNK pathway by Frizzled homologue 10 in human synovial sarcoma. Oncogene 28, 1110-1120.
20. Gerdes, J. M., Liu, Y., Zaghloul, N. A., Leitch, C. C., Lawson, S. S., Kato, M., Beachy, P. A., Beales, P. L., DeMartino, G. N., Fisher, S. et al. (2007). Disruption of the basal body compromises proteasomal function and perturbs intracellular Wnt response. Nat. Genet. 39, 1350-1360.
21. Glinka, A., Wu, W., Delius, H., Monaghan, A. P., Blumenstock, C. and Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362.
22. Gray, R. S., Abitua, P. B., Wlodarczyk, B. J., Szabo-Rogers, H. L., Blanchard, O., Lee, I., Weiss, G. S., Liu, K. J., Marcotte, E. M., Wallingford, J. B. et al. (2009). The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 11, 1225-1232.
23. Guirao, B., Meunier, A., Mortaud, S., Aguilar, A., Corsi, J. M., Strehl, L., Hirota, Y., Desoeuvre, A., Boutin, C., Han, Y. G. et al. (2010). Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat. Cell Biol. 12, 341-350.
24. Halloran, M. C., Sato-Maeda, M., Warren, J. T., Su, F., Lele, Z., Krone, P. H., Kuwada, J. Y. and Shoji, W. (2000). Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127, 1953-1960.
25. Hashimoto, H., Rebagliati, M., Ahmad, N., Muraoka, O., Kurokawa, T., Hibi, M. and Suzuki, T. (2004). The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 131, 1741-1753.
26. Hirokawa, N., Tanaka, Y., Okada, Y. and Takeda, S. (2006). Nodal flow and the generation of left-right asymmetry. Cell 125, 33-45.
27. Huang, P. and Schier, A. F. (2009). Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 136, 3089-3098.
28. 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.
29. Jayasena, C. S., Ohyama, T., Segil, N. and Groves, A. K. (2008). Notch signaling augments the canonical Wnt pathway to specify the size of the otic placode. Development 135, 2251-2261.
30. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
31. Kemp, C. R., Willems, E., Wawrzak, D., Hendrickx, M., Agbor Agbor, T. and Leyns, L. (2007). Expression of Frizzled5, Frizzled7, and Frizzled10 during early mouse development and interactions with canonical Wnt signaling. Dev. Dyn. 236, 2011-2019.
32. 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.
33. Lancaster, M. A., Louie, C. M., Silhavy, J. L., Sintasath, L., Decambre, M., Nigam, S. K., Willert, K. and Gleeson, J. G. (2009). Impaired Wnt-betacatenin signaling disrupts adult renal homeostasis and leads to cystic kidney ciliopathy. Nat. Med. 15, 1046-1054.
34. Lekven, A. C., Thorpe, C. J., Waxman, J. S. and Moon, R. T. (2001). Zebrafish wnt8 encodes two wnt8 proteins on a bicistronic transcript and is required for mesoderm and neurectoderm patterning. Dev. Cell 1, 103-114.
35. Lin, X. and Xu, X. (2009). Distinct functions of Wnt/{beta}-catenin signaling in KV development and cardiac asymmetry. Development 136, 207-217.
36. Lin, X., Rinaldo, L., Fazly, A. F. and Xu, X. (2007). Depletion of Med10 enhances Wnt and suppresses Nodal signaling during zebrafish embryogenesis. Dev. Biol. 303, 536-548.
37. Link, V., Shevchenko, A. and Heisenberg, C. P. (2006). Proteomics of early zebrafish embryos. BMC Dev. Biol. 6, 1.
38. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
39. Lopes, S. S., Lourenco, R., Pacheco, L., Moreno, N., Kreiling, J. and Saude, L. (2010). Notch signalling regulates left-right asymmetry through ciliary length control. Development 137, 3625-3632.
40. Lyman Gingerich, J., Westfall, T. A., Slusarski, D. C. and Pelegri, F. (2005). Hecate, a zebrafish maternal effect gene, affects dorsal organizer induction and intracellular calcium transient frequency. Dev. Biol. 286, 427-439.
41. Lyons, J. P., Miller, R. K., Zhou, X., Weidinger, G., Deroo, T., Denayer, T., Park, J. I., Ji, H., Hong, J. Y., Li, A. et al. (2009). Requirement of Wnt/beta-catenin signaling in pronephric kidney development. Mech. Dev. 126, 142-159.
42. Marose, T. D., Merkel, C. E., McMahon, A. P. and Carroll, T. J. (2008). Betacatenin is necessary to keep cells of ureteric bud/Wolffian duct epithelium in a precursor state. Dev. Biol. 314, 112-126.
43. Melby, A. E., Warga, R. M. and Kimmel, C. B. (1996). Specification of cell fates at the dorsal margin of the zebrafish gastrula. Development 122, 2225-2237.
44. Mitchell, B., Stubbs, J. L., Huisman, F., Taborek, P., Yu, C. and Kintner, C. (2009). The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr. Biol. 19, 924-929.
45. Momoi, A., Yoda, H., Steinbeisser, H., Fagotto, F., Kondoh, H., Kudo, A., Driever, W. and Furutani-Seiki, M. (2003). Analysis of Wnt8 for neural posteriorizing factor by identifying Frizzled 8c and Frizzled 9 as functional receptors for Wnt8. Mech. Dev. 120, 477-489.
46. Nagayama, S., Yamada, E., Kohno, Y., Aoyama, T., Fukukawa, C., Kubo, H., Watanabe, G., Katagiri, T., Nakamura, Y., Sakai, Y. et al. (2009). Inverse correlation of the up-regulation of FZD10 expression and the activation of betacatenin in synchronous colorectal tumors. Cancer Sci. 100, 405-412.
47. Nakaya, M. A., Biris, K., Tsukiyama, T., Jaime, S., Rawls, J. A. and Yamaguchi, T. P. (2005). Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 132, 5425-5436.
48. Nasevicius, A., Hyatt, T. M., Hermanson, S. B. and Ekker, S. C. (2000). Sequence, expression, and location of zebrafish frizzled 10. Mech. Dev. 92, 311-314.
49. 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.
50. Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M. and Hirokawa, N. (1998). Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95, 829-837.
51. Nonaka, S., Shiratori, H., Saijoh, Y. and Hamada, H. (2002). Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99.
52. Ocbina, P. J., Tuson, M. and Anderson, K. V. (2009). Primary cilia are not required for normal canonical Wnt signaling in the mouse embryo. PLoS ONE 4, e6839.
53. Ohyama, T., Mohamed, O. A., Taketo, M. M., Dufort, D. and Groves, A. K. (2006). Wnt signals mediate a fate decision between otic placode and epidermis. Development 133, 865-875.
54. Oishi, I., Kawakami, Y., Raya, A., Callol-Massot, C. and Izpisua Belmonte, J. C. (2006). Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet. 38, 1316-1322.
55. 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 leftright asymmetry. Nat. Genet. 30, 143-144.
56. Park, J. S., Valerius, M. T. and McMahon, A. P. (2007). Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 134, 2533-2539.
57. Park, K. S., Wells, J. M., Zorn, A. M., Wert, S. E., Laubach, V. E., Fernandez, L. G. and Whitsett, J. A. (2006). Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am. J. Respir. Cell Mol. Biol. 34, 151-157.
58. Park, T. J., Haigo, S. L. and Wallingford, J. B. (2006). Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 38, 303-311.
59. Park, T. J., Mitchell, B. J., Abitua, P. B., Kintner, C. and Wallingford, J. B. (2008). Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 40, 871-879.
60. Pedersen, L. B. and Rosenbaum, J. L. (2008). Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr. Top. Dev. Biol. 85, 23-61.
61. Placzek, M. and Briscoe, J. (2005). The floor plate: multiple cells, multiple signals. Nat. Rev. Neurosci. 6, 230-240.
62. Rawlins, E. L., Ostrowski, L. E., Randell, S. H. and Hogan, B. L. (2007). Lung development and repair: contribution of the ciliated lineage. Proc. Natl. Acad. Sci. USA 104, 410-417.
63. Riley, B. B., Zhu, C., Janetopoulos, C. and Aufderheide, K. J. (1997). A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. Dev. Biol. 191, 191-201.
64. Satir, P. and Christensen, S. T. (2007). Overview of structure and function of mammalian cilia. Annu. Rev. Physiol. 69, 377-400.
65. Schier, A. F. and Talbot, W. S. (2005). Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39, 561-613.
66. Simons, M., Gloy, J., Ganner, A., Bullerkotte, A., Bashkurov, M., Kronig, C., Schermer, B., Benzing, T., Cabello, O. A., Jenny, A. et al. (2005). Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37, 537-543.
67. 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.
68. 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.
69. Supp, D. M., Witte, D. P., Potter, S. S. and Brueckner, M. (1997). Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389, 963-966.
70. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
71. Terasaki, H., Saitoh, T., Shiokawa, K. and Katoh, M. (2002). Frizzled-10, upregulated in primary colorectal cancer, is a positive regulator of the WNT-betacatenin-TCF signaling pathway. Int. J. Mol. Med. 9, 107-112.
72. Thorpe, C. J., Weidinger, G. and Moon, R. T. (2005). Wnt/beta-catenin regulation of the Sp1-related transcription factor sp5l promotes tail development in zebrafish. Development 132, 1763-1772.
73. Tian, T., Zhao, L., Zhang, M., Zhao, X. and Meng, A. (2009). Both foxj1a and foxj1b are implicated in left-right asymmetric development in zebrafish embryos. Biochem. Biophys. Res. Commun. 380, 537-542.
74. Ueno, S., Weidinger, G., Osugi, T., Kohn, A. D., Golob, J. L., Pabon, L., Reinecke, H., Moon, R. T. and Murry, C. E. (2007). Biphasic role for Wnt/betacatenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 9685-9690.
75. Wallingford, J. B. and Mitchell, B. (2011). Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 25, 201-213.
76. Wang, S. and Ware, S. M. (2009). Use of FOXJ1CreER2T mice for inducible deletion of embryonic node gene expression. Genesis 47, 132-136.
77. Wang, Z., Shu, W., Lu, M. M. and Morrisey, E. E. (2005). Wnt7b activates canonical signaling in epithelial and vascular smooth muscle cells through interactions with Fzd1, Fzd10, and LRP5. Mol. Cell. Biol. 25, 5022-5030.
78. Willert, K. and Jones, K. A. (2006). Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394-1404.
79. 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.
80. 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.
81. 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.