Notch and Nodal control forkhead factor expression in the specification of multipotent progenitors in sea urchin

Development (Cambridge)

Volumn 140, Issue 8, 2013, Pages 1796-1806

  Materna, Stefan C ^a,d   Swartz, S Zachary ^b   Smith, Joel ^a,b,c  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b BROWN UNIVERSITY   (United States)

^c MARINE BIOLOGICAL LABORATORY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Coelomic pouch; FoxY; Hedgehog; Left right asymmetry; Multipotency; Notch; Strongylocentrotus purpuratus

Indexed keywords

NOTCH RECEPTOR; PROTEIN NODAL; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR PITX2;

ARTICLE; BLASTULA; CELL MATURATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; EPITHELIUM; ESOPHAGUS; GENE; LARVA; MORPHOGENESIS; MUSCLE CONTRACTION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEA URCHIN; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; IN SITU HYBRIDIZATION; MORPHOGENESIS; MORPHOLINOS; MULTIPOTENT STEM CELLS; NODAL PROTEIN; PHALLOIDINE; RECEPTORS, NOTCH; STRONGYLOCENTROTUS PURPURATUS;

ECHINOIDEA; ERINACEIDAE; STRONGYLOCENTROTUS PURPURATUS;

EID: 84875469203     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.091157     Document Type: Article

References (59)

1. Arenas-Mena, C. (2010). Indirect development, transdifferentiation and the macroregulatory evolution of metazoans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 653-669.
2. Berger, M. F., Badis, G., Gehrke, A. R., Talukder, S., Philippakis, A. A., Peña-Castillo, L., Alleyne, T. M., Mnaimneh, S., Botvinnik, O. B., Chan, E. T. et al. (2008). Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133, 1266-1276.
3. Bessodes, N., Haillot, E., Duboc, V., Röttinger, E., Lahaye, F. and Lepage, T. (2012). Reciprocal signaling between the ectoderm and a mesendodermal left-right organizer directs left-right determination in the sea urchin embryo. PLoS Genet. 8, e1003121.
4. Burke, R. D. and Alvarez, C. M. (1988). Development of the esophageal muscles in embryos of the sea urchin Strongylocentrotus purpuratus. Cell Tissue Res. 252, 411-417.
5. Cameron, R. A., Britten, R. J. and Davidson, E. H. (1989). Expression of two actin genes during larval development in the sea urchin Strongylocentrotus purpuratus. Mol. Reprod. Dev. 1, 149-155.
6. Cameron, R. A., Fraser, S. E., Britten, R. J. and Davidson, E. H. (1991). Macromere cell fates during sea urchin development. Development 113, 1085-1091.
7. Chen, J. K., Taipale, J., Cooper, M. K. and Beachy, P. A. (2002). Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 16, 2743-2748.
8. Chen, L., Liao, G., Yang, L., Campbell, K., Nakafuku, M., Kuan, C.-Y. and Zheng, Y. (2006). Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc. Natl. Acad. Sci. USA 103, 16520-16525.
9. Chia, F. S. and Walker, C. W. (1991). Echinodermata: asteroidea. In Reproduction of Marine Invertebrates, Echinoderms and Lophophorates, Vol. 4 (ed. A. C. Giese, J. S. Pearse and V. B. Pearse), pp. 301-353. Pacific Grove, CA: Boxwood Press.
10. Cox, K. H., Angerer, L. M., Lee, J. J., Davidson, E. H. and Angerer, R. C. (1986). Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis. J. Mol. Biol. 188, 159-172.
11. Damle, S. S. and Davidson, E. H. (2012). Synthetic in vivo validation of gene network circuitry. Proc. Natl. Acad. Sci. USA 109, 1548-1553.
12. Davidson, E. H. (2010). Emerging properties of animal gene regulatory networks. Nature 468, 911-920.
13. del Álamo, D., Rouault, H. and Schweisguth, F. (2011). Mechanism and significance of cis-inhibition in Notch signalling. Curr. Biol. 21, R40-R47.
14. Duboc, V., Röttinger, E., Besnardeau, L. and Lepage, T. (2004). Nodal and BMP2/4 signaling organizes the oral-aboral axis of the sea urchin embryo. Dev. Cell 6, 397-410.
15. Duboc, V., Röttinger, E., Lapraz, F., Besnardeau, L. and Lepage, T. (2005). Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev. Cell 9, 147-158.
16. Geiss, G., Bumgarner, R., Birditt, B., Dahl, T., Dowidar, N., Dunaway, D., Fell, H., Ferree, S., George R., Grogan, T. et al. (2008). Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26, 317-325.
17. Grande, C. and Patel, N. H. (2009). Lophotrochozoa get into the game: the nodal pathway and left/right asymmetry in bilateria. Cold Spring Harb. Symp. Quant. Biol. 74, 281-287.
18. Gustafson, E. A. and Wessel, G. M. (2010). Vasa genes: emerging roles in the germ line and in multipotent cells. BioEssays 32, 626-637.
19. Howard-Ashby, M., Materna, S. C., Brown, C. T., Chen, L., Cameron, R. A. and Davidson, E. H. (2006a). Gene families encoding transcription factors expressed in early development of Strongylocentrotus purpuratus. Dev. Biol. 300, 90-107.
20. Howard-Ashby, M., Materna, S. C., Brown, C. T., Chen, L., Cameron, R. A. and Davidson, E. H. (2006b). Identification and characterization of homeobox transcription factor genes in Strongylocentrotus purpuratus, and their expression in embryonic development. Dev. Biol. 300, 74-89.
21. Ingham, P. W. and McMahon, A. P. (2001). Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
22. Juliano, C. E., Yajima, M. and Wessel, G. M. (2010). Nanos functions to maintain the fate of the small micromere lineage in the sea urchin embryo. Dev. Biol. 337, 220-232.
23. Li, E., Materna, S. C. and Davidson, E. H. (2012). Direct and indirect control of oral ectoderm regulatory gene expression by Nodal signaling in the sea urchin embryo. Dev. Biol. 369, 377-385.
24. Luo, Y. J. and Su, Y. H. (2012). Opposing nodal and BMP signals regulate left-right asymmetry in the sea urchin larva. PLoS Biol. 10, e1001402.
25. 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.
26. Materna, S. C. and Oliveri, P. (2008). A protocol for unraveling gene regulatory networks. Nat. Protoc. 3, 1876-1887.
27. Materna, S. C., Howard-Ashby, M., Gray, R. and Davidson, E. H. (2006). The C2H2 zinc finger genes of Strongylocentrotus purpuratus and their expression in embryonic development. Dev. Biol. 300, 108-120.
28. Materna, S. C., Nam, J. and Davidson, E. H. (2010). High accuracy, high-resolution prevalence measurement for the majority of locally expressed regulatory genes in early sea urchin development. Gene Expr. Patterns 10, 177-184.
29. Materna, S. C., Ransick, A., Li, E. and Davidson, E. H. (2013). Diversification of oral and aboral mesodermal regulatory states in pregastrular sea urchin embryos. Dev. Biol. 375, 92-104.
30. Minelli, A. (2009). Perspectives in Animal Phylogeny and Evolution. New York, USA: Oxford University Press.
31. Morris, V. B., Zhao, J.-T., Shearman, D. C. A., Byrne, M. and Frommer, M. (2004). Expression of an Otx gene in the adult rudiment and the developing central nervous system in the vestibula larva of the sea urchin Holopneustes purpurescens. Int. J. Dev. Biol. 48, 17-22.
32. Nakamura, T. and Hamada, H. (2012). Left-right patterning: conserved and divergent mechanisms. Development 139, 3257-3262.
33. Pearse, J. S. and Cameron, R. A. (1991). Echinodermata: Echinoidea. In Reproduction of Marine Invertebrates, Echinoderms and Lophophorates, Vol. 4 (ed. A. C. Giese, J. S. Pearse and V. B. Pearse), pp. 513-662. Pacific Grove, CA: Boxwood Press.
34. Pehrson, J. R. and Cohen, L. H. (1986). The fate of the small micromeres in sea urchin development. Dev. Biol. 113, 522-526.
35. 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, R85.
36. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C. and Melton, D. A. (2002). 'Stemness': transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600.
37. 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.
38. Ransick, A., Rast, J. P., Minokawa, T., Calestani, C. and Davidson, E. H. (2002). New early zygotic regulators expressed in endomesoderm of sea urchin embryos discovered by differential array hybridization. Dev. Biol. 246, 132-147.
39. Rebscher, N., Zelada-González, F., Banisch, T. U., Raible, F. and Arendt, D. (2007). Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev. Biol. 306, 599-611.
40. Rebscher, N., Volk, C., Teo, R. and Plickert, G. (2008). The germ plasm component Vasa allows tracing of the interstitial stem cells in the cnidarian Hydractinia echinata. Dev. Dyn. 237, 1736-1745.
41. Roessler, E., Belloni, E., Gaudenz, K., Jay, P., Berta, P., Scherer, S. W., Tsui, L. C. and Muenke, M. (1996). Mutations in the human sonic hedgehog gene cause holoprosencephaly. Nat. Genet. 14, 357-360.
42. Ruffins, S. W. and Ettensohn, C. A. (1996). A fate map of the vegetal plate of the sea urchin (Lytechinus variegatus) mesenchyme blastula. Development 122, 253-263.
43. Schachter, K. A. and Krauss, R. S. (2008). Murine models of holoprosencephaly. Curr. Top. Dev. Biol. 84, 139-170.
44. Sherwood, D. R. and McClay, D. R. (1999). LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126, 1703-1713.
45. Smith, J. (2008). A protocol describing the principles of cis-regulatory analysis in the sea urchin. Nat. Protoc. 3, 710-718.
46. Smith, J. and Davidson, E. H. (2008). Gene regulatory network subcircuit controlling a dynamic spatial pattern of signaling in the sea urchin embryo. Proc. Natl. Acad. Sci. USA 105, 20089-20094.
47. Song, J. L. and Wessel, G. M. (2012). The forkhead transcription factor FoxY regulates Nanos. Mol. Reprod. Dev. 79, 680-688.
48. Spradling, A., Fuller, M. T., Braun, R. E. and Yoshida, S. (2011). Germline stem cells. Cold Spring Harb. Perspect. Biol. 3, a002642.
49. Strickland, L., von Dassow, G., Ellenberg, J., Foe, V., Lenart, P. and Burgess, D. (2004). Light microscopy of echinoderm embryos. Methods Cell Biol. 74, 371-409.
50. Sweet, H. C., Gehring, M. and Ettensohn, C. A. (2002). LvDelta is a mesoderm-inducing signal in the sea urchin embryo and can endow blastomeres with organizer-like properties. Development 129, 1945-1955.
51. Tanaka, S. and Dan, K. (1990). Study of the lineage and cell cycle of small micromeres in embryos of the sea urchin, Hemicentrotus pulcherrimus. Dev. Growth Differ. 32, 145-156.
52. Tsiairis, C. D. and McMahon, A. P. (2009). An Hh-dependent pathway in lateral plate mesoderm enables the generation of left/right asymmetry. Curr. Biol. 19, 1912-1917.
53. Tu, Q., Brown, C. T., Davidson, E. H. and Oliveri, P. (2006). Sea urchin Forkhead gene family: phylogeny and embryonic expression. Dev. Biol. 300, 49-62.
54. Voronina, E., Lopez, M., Juliano, C. E., Gustafson, E., Song, J. L., Extavour, C., George, S., Oliveri, P., McClay, D. and Wessel, G. (2008). Vasa protein expression is restricted to the small micromeres of the sea urchin, but is inducible in other lineages early in development. Dev. Biol. 314, 276-286.
55. Walton, K. D., Croce, J. C., Glenn, T. D., Wu, S.-Y. and McClay, D. R. (2006). Genomics and expression profiles of the Hedgehog and Notch signaling pathways in sea urchin development. Dev. Biol. 300, 153-164.
56. Walton, K. D., Warner, J., Hertzler, P. H. and McClay, D. R. (2009). Hedgehog signaling patterns mesoderm in the sea urchin. Dev. Biol. 331, 26-37.
57. Yajima, M. and Wessel, G. M. (2011). Small micromeres contribute to the germline in the sea urchin. Development 138, 237-243.
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.
59. Zhang, X. M., Ramalho-Santos, M. and McMahon, A. P. (2001). Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node. Cell 106, 781-792.