Wnt-regulated dynamics of positional information in zebrafish somitogenesis

Development (Cambridge)

Volumn 141, Issue 6, 2014, Pages 1381-1391

  Bajard, Lola ^a,c   Morelli, Luis G ^a,b,d   Ares, Saúl ^b,e   Pécréaux, Jacques ^a,f   Jülicher, Frank ^b   Oates, Andrew C ^a,g  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^c MASARYK UNIVERSITY   (Czech Republic)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^e CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^f UNIVERSITÉ DE RENNES 1   (France)

^g NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Embryonic elongation; Fgf signaling; Segmentation clock; Signal gradient; Time lapse microscopy; Wnt signaling

Indexed keywords

WNT PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; FLOW RATE; FLUORESCENCE; GENE EXPRESSION; HEAT SHOCK; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MORPHOGENESIS; NONHUMAN; NOTOCHORD; OSCILLATION; PRIORITY JOURNAL; REGULATORY MECHANISM; SOMITE; SOMITOGENESIS; WNT SIGNALING PATHWAY; ZEBRA FISH;

EMBRYONIC ELONGATION; FGF SIGNALING; SEGMENTATION CLOCK; SIGNAL GRADIENT; TIME-LAPSE MICROSCOPY; WNT SIGNALING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK RESPONSE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; SOMITES; T-BOX DOMAIN PROTEINS; WNT PROTEINS; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84896814835     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093435     Document Type: Article

References (77)

1. Aulehla, A. and Herrmann, B. G. (2004). Segmentation in vertebrates: clock and gradient finally joined. Genes Dev. 18, 2060-2067.
2. Aulehla, A. and Pourquié, O. (2010). Signaling gradients during paraxial mesoderm development. Cold Spring Harb. Perspect. Biol. 2, a000869.
3. Aulehla, A., Wehrle, C., Brand-Saberi, B., Kemler, R., Gossler, A., Kanzler, B. and Herrmann, B. G. (2003). Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev. Cell 4, 395-406.
4. Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M. B., Deng, C., Taketo, M., Lewandoski, M. and Pourquié, O. (2008). A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat. Cell Biol. 10, 186-193.
5. Buchberger, A., Bonneick, S. and Arnold, H. (2000). Expression of the novel basichelix-loop-helix transcription factor cMespo in presomitic mesoderm of chicken embryos. Mech. Dev. 97, 223-226.
6. Chalamalasetty, R. B., Dunty, W. C., Jr, Biris, K. K., Ajima, R., Iacovino, M., Beisaw, A., Feigenbaum, L., Chapman, D. L., Yoon, J. K., Kyba, M. et al. (2011). The Wnt3a/β-catenin target gene Mesogenin1 controls the segmentation clock by activating a Notch signalling program. Nat. Commun. 2, 390.
7. Chen, H., Xu, Z., Mei, C., Yu, D. and Small, S. (2012). A system of repressor gradients spatially organizes the boundaries of Bicoid-dependent target genes. Cell 149, 618-629.
8. Chien, A. J., Conrad, W. H. and Moon, R. T. (2009). A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 129, 1614-1627.
9. Chisholm, R. H., Hughes, B. D. and Landman, K. A. (2010). Building a morphogen gradient without diffusion in a growing tissue. PLoS ONE 5, e12857.
10. Christ, B., Jacob, H. J. and Jacob, M. (1974). Somitogenesis in the chick embryo. Determination of the segmentation direction. Verh. Anat. Ges. 68, 573-579.
11. Cooke, J. and Zeeman, E. C. (1976). A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol. 58, 455-476.
12. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
13. Delaune, E. A., François, P., Shih, N. P. and Amacher, S. L. (2012). Single-cellresolution imaging of the impact of Notch signaling and mitosis on segmentation clock dynamics. Dev. Cell 23, 995-1005.
14. Dubrulle, J. and Pourquié, O. (2004). fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427, 419-422.
15. Dubrulle, J., McGrew, M. J. and Pourquié, O. (2001). FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106, 219-232.
16. Dunty, W. C., Jr, Biris, K. K., Chalamalasetty, R. B., Taketo, M. M., Lewandoski, M. and Yamaguchi, T. P. (2008). Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135, 85-94.
17. Fior, R., Maxwell, A. A., Ma, T. P., Vezzaro, A., Moens, C. B., Amacher, S. L., Lewis, J. and Saúde, L. (2012). The differentiation and movement of presomitic mesoderm progenitor cells are controlled by Mesogenin 1. Development 139, 4656-4665.
18. Galceran, J., Sustmann, C., Hsu, S. C., Folberth, S. and Grosschedl, R. (2004). LEF1-mediated regulation of Delta-like1 links Wnt and Notch signaling in somitogenesis. Genes Dev. 18, 2718-2723.
19. Gaunt, S. J., Drage, D. and Cockley, A. (2003). Vertebrate caudal gene expression gradients investigated by use of chick cdx-A/lacZ and mouse cdx-1/lacZ reporters in transgenic mouse embryos: evidence for an intron enhancer. Mech. Dev. 120, 573-586.
20. Gibb, S., Zagorska, A., Melton, K., Tenin, G., Vacca, I., Trainor, P., Maroto, M. and Dale, J. K. (2009). Interfering with Wnt signalling alters the periodicity of the segmentation clock. Dev. Biol. 330, 21-31.
21. Gomez, C., Ozbudak, E. M., Wunderlich, J., Baumann, D., Lewis, J. and Pourquié, O. (2008). Control of segment number in vertebrate embryos. Nature 454, 335-339.
22. Greco, T. L., Takada, S., Newhouse, M. M., McMahon, J. A., McMahon, A. P. and Camper, S. A. (1996). Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev. 10, 313-324.
23. Groves, J. A., Hammond, C. L. and Hughes, S. M. (2005). Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish. Development 132, 4211-4222.
24. Harima, Y., Takashima, Y., Ueda, Y., Ohtsuka, T., and Kageyama, R. (2013). Accelerating the tempo of the segmentation clock by reducing the number of introns in the Hes7 gene. Cell Rep. 3, 1-7.
25. Herrgen, L., Schröter, C., Bajard, L. and Oates, A. C. (2009). Multiple embryo timelapse imaging of zebrafish development. Methods Mol. Biol. 546, 243-254.
26. Herrgen, L., Ares, S., Morelli, L. G., Schroter, C., Julicher, F., and Oates, A. C. (2010). Intercellular coupling regulates the period of the segmentation clock. Curr. Biol. 20, 1244-1253.
27. Hofmann, M., Schuster-Gossler, K., Watabe-Rudolph, M., Aulehla, A., Herrmann, B. G. and Gossler, A. (2004). WNT signaling, in synergy with T/TBX6, controls Notch signaling by regulating Dll1 expression in the presomitic mesoderm of mouse embryos. Genes Dev. 18, 2712-2717.
28. Holley, S. A., Geisler, R. and Nüsslein-Volhard, C. (2000). Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity. Genes Dev. 14, 1678-1690.
29. Ibañes, M., Kawakami, Y., Rasskin-Gutman, D. and Izpisúa Belmonte, J. C. (2006). Cell lineage transport: a mechanism for molecular gradient formation. Mol. Syst. Biol. 2, 57.
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. Kagermeier-Schenk, B., Wehner, D., Ozhan-Kizil, G., Yamamoto, H., Li, J., Kirchner, K., Hoffmann, C., Stern, P., Kikuchi, A., Schambony, A. et al. (2011). Waif1/5T4 inhibits Wnt/β-catenin signaling and activates noncanonical Wnt pathways by modifying LRP6 subcellular localization. Dev. Cell 21, 1129-1143.
32. Kelly, G. M., Greenstein, P., Erezyilmaz, D. F. and Moon, R. T. (1995). Zebrafish wnt8 and wnt8b share a common activity but are involved in distinct developmental pathways. Development 121, 1787-1799.
33. 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.
34. Martin, B. L., and Kimelman, D. (2009). Wnt signaling and the evolution of embryonic posterior development. Curr. Biol. 19, R215-R219.
35. Martin, B. L. and Kimelman, D. (2010). Brachyury establishes the embryonic mesodermal progenitor niche. Genes Dev. 24, 2778-2783.
36. Martin, B. L. and Kimelman, D. (2012). Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev. Cell 22, 223-232.
37. Masamizu, Y., Ohtsuka, T., Takashima, Y., Nagahara, H., Takenaka, Y., Yoshikawa, K., Okamura, H. and Kageyama, R. (2006). Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc. Natl. Acad. Sci. USA 103, 1313-1318.
38. Menkes, B. and Sandor, S. (1969). Researches on the formation of axial organs of the chick embryo. V. Revue Roumaine d'Embryologie et de Cytologie 6, 65-77.
39. Menkes, B., Sandor, S. and Elias, S. (1968). Researches on the formation of axial organs of the chick embryo. IV. Revue Roumaine d'Embryologie et de Cytologie 5, 131-137.
40. Morelli, L. G., Ares, S., Herrgen, L., Schröter, C., Jülicher, F. and Oates, A. C. (2009). Delayed coupling theory of vertebrate segmentation. HFSP J. 3, 55-66.
41. Morelli, L. G., Uriu, K., Ares, S. and Oates, A. C. (2012). Computational approaches to developmental patterning. Science 336, 187-191.
42. Moreno, T. A. and Kintner, C. (2004). Regulation of segmental patterning by retinoic acid signaling during Xenopus somitogenesis. Dev. Cell 6, 205-218.
43. Moreno, T. A., Jappelli, R., Izpisúa Belmonte, J. C. and Kintner, C. (2008). Retinoic acid regulation of the Mesp-Ripply feedback loop during vertebrate segmental patterning. Dev. Biol. 315, 317-330.
44. Murray, P. J., Maini, P. K. and Baker, R. E. (2011). The clock and wavefront model revisited. J. Theor. Biol. 283, 227-238.
45. Naiche, L. A., Holder, N. and Lewandoski, M. (2011). FGF4 and FGF8 comprise the wavefront activity that controls somitogenesis. Proc. Natl. Acad. Sci. USA 108, 4018-4023.
46. Nikaido, M., Kawakami, A., Sawada, A., Furutani-Seiki, M., Takeda, H. and Araki, K. (2002). Tbx24, encoding a T-box protein, is mutated in the zebrafish somitesegmentation mutant fused somites. Nat. Genet. 31, 195-199.
47. Oates, A. C., Rohde, L. A. and Ho, R. K. (2005). Generation of segment polarity in the paraxial mesoderm of the zebrafish through a T-box-dependent inductive event. Dev. Biol. 283, 204-214.
48. Oates, A. C., Morelli, L. G. and Ares, S. (2012). Patterning embryos with oscillations: structure, function and dynamics of the vertebrate segmentation clock. Development 139, 625-639.
49. Palmeirim, I., Henrique, D., Ish-Horowicz, D. and Pourquié, O. (1997). Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91, 639-648.
50. Palmeirim, I., Dubrulle, J., Henrique, D., Ish-Horowicz, D. and Pourquié, O. (1998). Uncoupling segmentation and somitogenesis in the chick presomitic mesoderm. Dev. Genet. 23, 77-85.
51. Pfeiffer, S., Alexandre, C., Calleja, M., and Vincent, J. P. (2000). The progeny of wingless-expressing cells deliver the signal at a distance in Drosophila embryos. Curr. Biol. 10, 321-324.
52. Picker, A., Cavodeassi, F., Machate, A., Bernauer, S., Hans, S., Abe, G., Kawakami, K., Wilson, S. W. and Brand, M. (2009). Dynamic coupling of pattern formation and morphogenesis in the developing vertebrate retina. PLoS Biol. 7, e1000214.
53. Porcher, A., and Dostatni, N. (2010). The bicoid morphogen system. Curr. Biol. 20, R249-R254.
54. Pourquié, O. (2011). Vertebrate segmentation: from cyclic gene networks to scoliosis. Cell 145, 650-663.
55. Pourquié, O. and Tam, P. P. (2001). A nomenclature for prospective somites and phases of cyclic gene expression in the presomitic mesoderm. Dev. Cell 1, 619-620.
56. Preibisch, S., Saalfeld, S. and Tomancak, P. (2009). Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25, 1463-1465.
57. Rogers, K. W. and Schier, A. F. (2011). Morphogen gradients: from generation to interpretation. Annu. Rev. Cell Dev. Biol. 27, 377-407.
58. Row, R. H. and Kimelman, D. (2009). Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud. Dev. Biol. 329, 55-63.
59. Saga, Y., Hata, N., Koseki, H. and Taketo, M. M. (1997). Mesp2: a novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev. 11, 1827-1839.
60. Sawada, A., Fritz, A., Jiang, Y. J., Yamamoto, A., Yamasu, K., Kuroiwa, A., Saga, Y. and Takeda, H. (2000). Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites. Development 127, 1691-1702.
61. Sawada, A., Shinya, M., Jiang, Y. J., Kawakami, A., Kuroiwa, A. and Takeda, H. (2001). Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 128, 4873-4880.
62. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an opensource platform for biological-image analysis. Nat. Methods 9, 676-682.
63. Schroter, C., and Oates, A. C. (2010). Segment number and axial identity in a segmentation clock period mutant. Curr. Biol. 20, 1254-1258.
64. Schröter, C., Herrgen, L., Cardona, A., Brouhard, G. J., Feldman, B. and Oates, A. C. (2008). Dynamics of zebrafish somitogenesis. Dev. Dyn. 237, 545-553.
65. Shimizu, T., Bae, Y. K., Muraoka, O. and Hibi, M. (2005). Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev. Biol. 279, 125-141.
66. Stoick-Cooper, C. L., Weidinger, G., Riehle, K. J., Hubbert, C., Major, M. B., Fausto, N. and Moon, R. T. (2007). Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489.
67. Stulberg, M. J., Lin, A., Zhao, H. and Holley, S. A. (2012). Crosstalk between Fgf and Wnt signaling in the zebrafish tailbud. Dev. Biol. 369, 298-307.
68. Szeto, D. P. and Kimelman, D. (2004). Combinatorial gene regulation by Bmp and Wnt in zebrafish posterior mesoderm formation. Development 131, 3751-3760.
69. 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.
70. van Eeden, F. J., Granato, M., Schach, U., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C. P., Jiang, Y. J., Kane, D. A. et al. (1996). Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153-164.
71. Wahl, M. B., Deng, C., Lewandoski, M. and Pourquié, O. (2007). FGF signaling acts upstream of the NOTCH and WNT signaling pathways to control segmentation clock oscillations in mouse somitogenesis. Development 134, 4033-4041.
72. Weidinger, G., Thorpe, C. J., Wuennenberg-Stapleton, K., Ngai, J., and Moon, R. T. (2005). The Sp1-related transcription factors sp5 and sp5-like act downstream of Wnt/beta-catenin signaling in mesoderm and neuroectoderm patterning. Curr. Biol. 15, 489-500.
73. Wilson, V., Olivera-Martinez, I. and Storey, K. G. (2009). Stem cells, signals and vertebrate body axis extension. Development 136, 1591-1604.
74. Wittler, L., Shin, E. H., Grote, P., Kispert, A., Beckers, A., Gossler, A., Werber, M. and Herrmann, B. G. (2007). Expression of Msgn1 in the presomitic mesoderm is controlled by synergism of WNT signalling and Tbx6. EMBO Rep. 8, 784-789.
75. Yabe, T. and Takada, S. (2012). Mesogenin causes embryonic mesoderm progenitors to differentiate during development of zebrafish tail somites. Dev. Biol. 370, 213-222.
76. Yasuhiko, Y., Haraguchi, S., Kitajima, S., Takahashi, Y., Kanno, J. and Saga, Y. (2006). Tbx6-mediated Notch signaling controls somite-specific Mesp2 expression. Proc. Natl. Acad. Sci. USA 103, 3651-3656.
77. Yu, S. R., Burkhardt, M., Nowak, M., Ries, J., Petrásek, Z., Scholpp, S., Schwille, P. and Brand, M. (2009). Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536.