Dose-dependent nuclear β-catenin response segregates endomesoderm along the sea star primary axis

Development (Cambridge)

Volumn 142, Issue 1, 2015, Pages 207-217

  McCauley, Brenna S ^a   Akyar, Eda ^a   Rosa Saad, H ^a   Hinman, Veronica F ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; NOTCH RECEPTOR; NUCLEAR BETA CATENIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BRA; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR FOXA; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 5; TRANSCRIPTION FACTOR GATA 6; UNCLASSIFIED DRUG; HEPATOCYTE NUCLEAR FACTOR 3GAMMA; LITHIUM CHLORIDE;

ARTICLE; CELL FATE; EMBRYO DEVELOPMENT; ENDODERM; ENDOMESODERM; GENE REGULATORY NETWORK; HYPOTHESIS; INVERTEBRATE; MESODERM; NONHUMAN; PATIRIA MINIATA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STARFISH; TRANSCRIPTION REGULATION; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; BLASTULA; CELL NUCLEUS; DRUG EFFECTS; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MORPHOGENESIS; TIME;

ASTEROIDEA; INVERTEBRATA; VERTEBRATA;

ANIMALS; BETA CATENIN; BLASTULA; BODY PATTERNING; CELL NUCLEUS; EMBRYO, NONMAMMALIAN; ENDODERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HEPATOCYTE NUCLEAR FACTOR 3-GAMMA; LITHIUM CHLORIDE; MESODERM; MODELS, BIOLOGICAL; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STARFISH; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84918551138     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113043     Document Type: Article

References (58)

1. Ben-Taboude-Leon, S. and Davidson, E. H. (2010). Information processing at the foxa node of the sea urchin endomesoderm specification network. Proc. Natl. Acad. Sci. USA 107, 10103-10108.
2. Chan, T.-M., Longabaugh, W., Bolouri, H., Chen, H.-L., Tseng, W.-F., Chao, C.-H., Jang, T.-H., Lin, Y.-I., Hung, S.-C., Wang, H.-D. et al. (2009). Developmental gene regulatory networks in the zebrafish embryo. Biochim. Biophys. Acta 1789, 279-298.
3. Cheatle Jarvela, A. M. and Hinman, V. (2014). A method for microinjection of Patiria miniata zygotes. J. Vis. Exp. 1, e51913.
4. Croce, J. C. and McClay, D. R. (2010). Dynamics of Delta/Notch signaling on endomesoderm segregation in the sea urchin embryo. Development 137, 83-91.
5. Darras, S., Gerhart, J., Terasaki, M., Kirschner, M. and Lowe, C. J. (2011). β-Catenin specifies the endomesoderm and defines the posterior organizer of the hemichordate Saccoglossus kowalevskii. Development 138, 959-970.
6. Davidson, E. H. (2006). The Regulatory Genome: Gene Regulatory Networks in Development and Evolution. Academic Press.
7. Davidson, E. H. and Erwin, D. H. (2006). Gene regulatory networks and the evolution of animal body plans. Science 311, 796-800.
8. Green, J. B. A. and Smith, J. C. (1991). Growth factors as morphogens: do gradients and thresholds establish body plan? Trends Genet. 7, 245-250.
9. Henry, J. Q., Perry, K. J., Wever, J., Seaver, E. and Martindale, M. Q. (2008). β-Catenin is required for the establishment of vegetal embryonic fates in the nemertean, Cerebratulus lacteus. Dev. Biol. 317, 368-379.
10. Henry, J. Q., Perry, K. J. and Martindale, M. Q. (2010). β-catenin and early development in the gastropod, Crepidula fornicata. Integr. Comp. Biol. 50, 707-719.
11. Hinman, V. F. and Cheatle Jarvela, A. M. (2014). Developmental gene regulatory network evolution: Insights from comparative studies in echinoderms. Genesis 52, 193-207.
12. Hinman, V. F. and Davidson, E. H. (2003a). Expression of AmKrox, a starfish ortholog of a sea urchin transcription factor essential for endomesodermal specification. Gene Expr. Patterns 3, 423-426.
13. Hinman, V. F. and Davidson, E. H. (2003b). Expression of a gene encoding a Gata transcription factor during embryogenesis of the starfish Asterina miniata. Gene Expr. Patterns 3, 419-422.
14. Hinman, V. F. and Davidson, E. H. (2007). Evolutionary plasticity of developmental gene regulatory network architecture. Proc. Natl. Acad. Sci. USA 104, 19404-19409.
15. Hinman, V. F., Nguyen, A. T. and Davidson, E. H. (2003a). Expression and function of a starfish Otx ortholog, AmOtx: a conserved role for Otx proteins in endoderm development that predates divergence of the eleutherozoa. Mech. Dev. 120, 1165-1176.
16. Hinman, V. F., Nguyen, A. T., Cameron, R. A. and Davidson, E. H. (2003b). Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proc. Natl. Acad. Sci. USA 100, 13356-13361.
17. Hinman, V. F., Yankura, K. A. and McCauley, B. S. (2009). Evolution of gene regulatory network architectures: examples of subcircuit conservation and plasticity between classes of echinoderms. Biochim. Biophys. Acta 1789, 326-332.
18. Hudson, C., Kawai, N., Negishi, T. and Yasuo, H. (2013). β-catenin-driven binary fate specification segregates germ layers in ascidian embryos. Curr. Biol. 23, 491-495.
19. Imai, K., Takada, N., Satoh, N. and Satou, Y. (2000). (beta)-catenin mediates the specification of endoderm cells in ascidian embryos. Development 127, 3009-3020.
20. In der Rieden, P. M. J., Vilaspasa, F. L. and Durston, A. J. (2010). Xwnt8 directly initiates expression of labial Hox genes. Dev. Dyn. 239, 126-139.
21. Ip, Y. T., Levine, M. and Small, S. J. (1992). The bicoid and dorsal morphogens use a similar strategy to make stripes in the Drosophila embryo. J. Cell Sci. 1992 Suppl. 16, 33-38.
22. Jaeger, J. (2011). The gap gene network. Cell. Mol. Life Sci. 68, 243-274.
23. Kiecker, C. and Niehrs, C. (2001). A morphogen gradient of Wnt/β-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128, 4189-4201.
24. Kuraishi, R. and Osanai, K. (1992). Cell movements during gastrulation of starfish larvae. Biol. Bull. 183, 258-268.
25. Kuraishi, R. and Osanai, K. (1994). Contribution of maternal factors and cellular interaction to determination of archenteron in the starfish embryo. Development 120, 2619-2628.
26. Levine, M. and Davidson, E. H. (2005). Gene regulatory networks for development. Proc. Natl. Acad. Sci. USA 102, 4936-4942.
27. Lhomond, G., McClay, D. R., Gache, C. and Croce, J. C. (2012). Frizzled1/2/7 signaling directs β-catenin nuclearisation and initiates endoderm specification in macromeres during sea urchin embryogenesis. Development 139, 816-825.
28. Logan, C. Y. and Nusse, R. (2004). The wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
29. Logan, C. Y., Miller, J. R., Ferkowicz, M. J. and McClay, D. R. (1999). Nuclear β-catenin is required to specify vegetal cell fates in the sea urchin embryo. Development 126, 345-357.
30. Longabaugh, W. J. R. (2012). BioTapestry: a tool to visualize the dynamic properties of gene regulatory networks. Methods Mol. Biol. 786, 359-394.
31. Loose, M. and Patient, R. (2004). A genetic regulatory network for Xenopus mesendoderm formation. Dev. Biol. 271, 467-478.
32. Maduro, M. F. (2009). Structure and evolution of the C. elegans embryonic endomesoderm network. Biochim. Biophys. Acta 1789, 250-260.
33. Materna, S. C. and Davidson, E. H. (2012). A comprehensive analysis of Delta signaling in pre-gastrular sea urchin embryos. Dev. Biol. 364, 77-87.
34. McCauley, B. S., Weideman, E. P. and Hinman, V. F. (2010). A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev. Biol. 340, 200-208.
35. McCauley, B. S., Wright, E. P., Exner, C., Kitazawa, C. and Hinman, V. F. (2012). Development of an embryonic skeletogenic mesenchyme lineage in a sea cucumber reveals the trajectory of change for the evolution of novel structures in echinoderms. EvoDevo 3, 17.
36. McCauley, B. S., Akyar, E., Filliger, L. and Hinman, V. F. (2013). Expression of wnt and frizzled genes during early sea star development. Gene Expr. Patterns 13, 437-444.
37. McLin, V. A., Rankin, S. A. and Zorn, A. M. (2007). Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development 134, 2207-2217.
38. Miyawaki, K., Yamamoto, M., Saito, K., Saito, S., Kobayashi, N. and Matsuda, S. (2003). Nuclear localization of beta-catenin in vegetal pole cells during early embryogenesis of the starfish Asterina pectinifera. Dev. Growth Differ. 45, 121-128.
39. Niehrs, C. (2010). On growth and form: a Cartesian coordinate system of Wnt and BMP signaling specifies bilaterian body axes. Development 137, 845-857.
40. Oliveri, P., Walton, K. D., Davidson, E. H. and McClay, D. R. (2006). Repression of mesodermal fate by foxa, a key endoderm regulator of the sea urchin embryo. Development 133, 4173-4181.
41. Peter, I. S. and Davidson, E. H. (2011). A gene regulatory network controlling the embryonic specification of endoderm. Nature 474, 635-639.
42. Poustka, A. J., Kühn, A., Groth, D., Weise, V., Yaguchi, S., Burke, R. D., Herwig, R., Lehrach, H. and Panopoulou, G. (2007). A global view of gene expression in lithium and zinc treated sea urchin embryos: new components of gene regulatory networks. Genome Biol. 8, pR85.
43. Ransick, A. and Davidson, E. H. (2006). cis-regulatory processing of Notch signaling input to the sea urchin glial cells missing gene during mesoderm specification. Dev. Biol. 297, 587-602.
44. Röttinger, E., Croce, J., Lhomond, G., Besnardeau, L., Gache, C. and Lepage, T. (2006). Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development 133, 4341-4353.
45. Röttinger, E., Dahlin, P. and Martindale, M. Q. (2012). A framework for the establishment of a cnidarian gene regulatory network for “Endomesoderm” specification: the inputs of β-catenin/TCF signaling. PLoS Genet. 8, e1003164.
46. Schneider, S. Q. and Bowerman, B. (2007). β-catenin asymmetries after all animal/ vegetal-oriented cell divisions in Platynereis dumerilii embryos mediate binary cell-fate specification. Dev. Cell 13, 73-86.
47. Schneider, V. A. and Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15, 304-315.
48. Sethi, A. J., Wikramanayake, R. M., Angerer, R. C., Range, R. C. and Angerer, L. M. (2012). Sequential signaling crosstalk regulates endomesoderm segregation in sea urchin embryos. Science 335, 590-593.
49. Sherwood, D. R. and McClay, D. R. (1999). LvNotch signaling mediates secondary mesenchymespecification in the sea urchin embryo. Development 125, 1703-1713.
50. Stambolic, V., Ruel, L. and Woodgett, J. R. (1996). Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 6, 1664-1669.
51. Sweet, H. C., Gehring, M. and Ettensohn, C. A. (2002). LvDelta is a mesoderminducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 129, 1945-1955.
52. Thorpe, C. J., Schlesinger, A., Carter, J. C. and Bowerman, B. (1997). Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90, 695-705.
53. Veeman, M. T., Slusarski, D. C., Kaykas, A., Louie, S. H. and Moon, R. T. (2003). Zebrafish prickle, a modulator of noncanonical wnt/fz signaling, regulates gastrulation movements. Curr. Biol. 13, 680-685.
54. Wang, D. G., Britten, R. J. and Davidson, E. H. (1995). Maternal and embryonic provenance of a sea urchin embryo transcription factor, SpZ12-1. Mol. Marine Biol. Biotechnol. 4, 148-153.
55. Weitzel, H. E., Illies, M. R., Byrum, C. A., Xu, R., Wikramanayake, A. H. and Ettensohn, C. A. (2004). Differential stability of beta-catenin along the animalvegetal axis of the sea urchin embryo mediated by dishevelled. Development 131, 2947-2956.
56. Wikramanayake, A. H., Huang, L. and Klein, W. H. (1998). beta-Catenin is essential for patterning the maternally specified animal-vegetal axis in the sea urchin embryo. Proc. Natl. Acad. Sci. USA 95, 9343-9348.
57. Wikramanayake, A. H., Hong, M., Lee, P. N., Pang, K., Byrum, C. A., Bince, J. M., Xu, R. and Martindale, M. Q. (2003). An ancient role for nuclear β-catenin in the evolution of axial polarity and germ layer segregation. Nature 426, 446-450.
58. Yankura, K. A., Martik, M. L., Jennings, C. K. and Hinman, V. F. (2010). Uncoupling of complex regulatory patterning during evolution of larval development in echinoderms. BMC Biol. 8, 143.