A BMP regulatory network controls ectodermal cell fate decisions at the neural plate border

Development (Cambridge)

Volumn 140, Issue 21, 2013, Pages 4435-4444

  Reichert, Sabine ^a   Randall, Rebecca A ^a   Hill, Caroline S ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Bambib; BMP signalling; Bmper; Neural crest; Neural plate border; Preplacodal ectoderm; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CROSSVEINLESS 2; GROWTH DIFFERENTIATION FACTOR 5; GROWTH DIFFERENTIATION FACTOR 6; LIGAND; OSTEOGENIC PROTEIN 1; PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL POPULATION; CONTROLLED STUDY; DNA BINDING; DNA FLANKING REGION; EMBRYO; EPIDERMIS; FLUORESCENCE IN SITU HYBRIDIZATION; GASTRULATION; HALF LIFE TIME; NERVOUS TISSUE; NEURAL CREST; NEURAL STEM CELL; NEUROECTODERM; NEURULATION; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SOMITE; WESTERN BLOTTING; ZEBRA FISH;

BAMBIB; BMP SIGNALLING; BMPER; NEURAL CREST; NEURAL PLATE BORDER; PREPLACODAL ECTODERM; ZEBRAFISH;

ALCIAN BLUE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; ECTODERM; GTPASE-ACTIVATING PROTEINS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION, FLUORESCENCE; NEURAL CREST; NEURAL PLATE; NEURULATION; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84885659822     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.098707     Document Type: Article

References (59)

1. Ahrens, K. and Schlosser, G. (2005). Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis. Dev. Biol. 288, 40-59.
2. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. and Westerfield, M. (1994). Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475-3486.
3. Ambrosio, A. L., Taelman, V. F., Lee, H. X., Metzinger, C. A., Coffinier, C. and De Robertis, E. M. (2008). Crossveinless-2 Is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning. Dev. Cell 15, 248-260.
4. Baker, C. V. and Bronner-Fraser, M. (2001). Vertebrate cranial placodes I. Embryonic induction. Dev. Biol. 232, 1-61.
5. Binnerts, M. E., Wen, X., Canté-Barrett, K., Bright, J., Chen, H. T., Asundi, V., Sattari, P., Tang, T., Boyle, B., Funk, W. et al. (2004). Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 315, 272-280.
6. Blanco Calvo, M., Bolós Fernández, V., Medina Villaamil, V., Aparicio Gallego, G., Díaz Prado, S. and Grande Pulido, E. (2009). Biology of BMP signalling and cancer. Clin. Transl. Oncol. 11, 126-137.
7. Bruneau, S., Mourrain, P. and Rosa, F. M. (1997). Expression of contact, a new zebrafish DVR member, marks mesenchymal cell lineages in the developing pectoral fins and head and is regulated by retinoic acid. Mech. Dev. 65, 163-173.
8. Christensen, R. G., Enuameh, M. S., Noyes, M. B., Brodsky, M. H., Wolfe, S. A. and Stormo, G. D. (2012). Recognition models to predict DNA-binding specificities of homeodomain proteins. Bioinformatics 28, i84-i89.
9. Conley, C. A., Silburn, R., Singer, M. A., Ralston, A., Rohwer-Nutter, D., Olson, D. J., Gelbart, W. and Blair, S. S. (2000). Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127, 3947-3959.
10. Daly, A. C., Randall, R. A. and Hill, C. S. (2008). Transforming growth factor β-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol. Cell. Biol. 28, 6889-6902.
11. Dorey, K. and Hill, C. S. (2006). A novel Cripto-related protein reveals an essential role for EGF-CFCs in Nodal signalling in Xenopus embryos. Dev. Biol. 292, 303-316.
12. Dreesen, O. and Brivanlou, A. H. (2007). Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev. 3, 7-17.
13. Dutton, K. A., Pauliny, A., Lopes, S. S., Elworthy, S., Carney, T. J., Rauch, J., Geisler, R., Haffter, P. and Kelsh, R. N. (2001). Zebrafish colourless encodes sox10 and specifies non-ectomesenchymal neural crest fates. Development 128, 4113-4125.
14. Esterberg, R. and Fritz, A. (2009). dlx3b/4b are required for the formation of the preplacodal region and otic placode through local modulation of BMP activity. Dev. Biol. 325, 189-199.
15. French, C. R., Erickson, T., French, D. V., Pilgrim, D. B. and Waskiewicz, A. J. (2009). Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development. Dev. Biol. 333, 37-47.
16. Gajavelli, S., Wood, P. M., Pennica, D., Whittemore, S. R. and Tsoulfas, P. (2004). BMP signaling initiates a neural crest differentiation program in embryonic rat CNS stem cells. Exp. Neurol. 188, 205-223.
17. Germain, S., Howell, M., Esslemont, G. M. and Hill, C. S. (2000). Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev. 14, 435-451.
18. Glavic, A., Maris Honoré, S., Gloria Feijóo, C., Bastidas, F., Allende, M. L. and Mayor, R. (2004). Role of BMP signaling and the homeoprotein Iroquois in the specification of the cranial placodal field. Dev. Biol. 272, 89-103.
19. Howell, M. and Hill, C. S. (1997). XSmad2 directly activates the activin-inducible, dorsal mesoderm gene XFKH1 in Xenopus embryos. EMBO J. 16, 7411-7421.
20. Huang, X. and Saint-Jeannet, J. P. (2004). Induction of the neural crest and the opportunities of life on the edge. Dev. Biol. 275, 1-11.
21. Kamimura, M., Matsumoto, K., Koshiba-Takeuchi, K. and Ogura, T. (2004). Vertebrate crossveinless 2 is secreted and acts as an extracellular modulator of the BMP signaling cascade. Dev. Dyn. 230, 434-445.
22. Kho, A. T., Zhao, Q., Cai, Z., Butte, A. J., Kim, J. Y., Pomeroy, S. L., Rowitch, D. H. and Kohane, I. S. (2004). Conserved mechanisms across development and tumorigenesis revealed by a mouse development perspective of human cancers. Genes Dev. 18, 629-640.
23. Kishimoto, Y., Lee, K. H., Zon, L., Hammerschmidt, M. and Schulte-Merker, S. (1997). The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124, 4457-4466.
24. Kwon, H. J., Bhat, N., Sweet, E. M., Cornell, R. A. and Riley, B. B. (2010). Identification of early requirements for preplacodal ectoderm and sensory organ development. PLoS Genet. 6, e1001133.
25. Lele, Z., Folchert, A., Concha, M., Rauch, G. J., Geisler, R., Rosa, F., Wilson, S. W., Hammerschmidt, M. and Bally-Cuif, L. (2002). parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129, 3281-3294.
26. Levy, L., Howell, M., Das, D., Harkin, S., Episkopou, V. and Hill, C. S. (2007). Arkadia activates Smad3/Smad4-dependent transcription by triggering signalinduced SnoN degradation. Mol. Cell. Biol. 27, 6068-6083.
27. Litsiou, A., Hanson, S. and Streit, A. (2005). A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. Development 132, 4051-4062.
28. Lowery, J. W. and de Caestecker, M. P. (2010). BMP signaling in vascular development and disease. Cytokine Growth Factor Rev. 21, 287-298.
29. Moser, M., Binder, O., Wu, Y., Aitsebaomo, J., Ren, R., Bode, C., Bautch, V. L., Conlon, F. L. and Patterson, C. (2003). BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol. Cell. Biol. 23, 5664-5679.
30. Moser, M., Yu, Q., Bode, C., Xiong, J. W. and Patterson, C. (2007). BMPER is a conserved regulator of hematopoietic and vascular development in zebrafish. J. Mol. Cell. Cardiol. 43, 243-253.
31. Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Haffter, P., Heisenberg, C. P. et al. (1996). Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123, 81-93.
32. Neave, B., Holder, N. and Patient, R. (1997). A graded response to BMP-4 spatially coordinates patterning of the mesoderm and ectoderm in the zebrafish. Mech. Dev. 62, 183-195.
33. Nguyen, V. H., Schmid, B., Trout, J., Connors, S. A., Ekker, M. and Mullins, M. C. (1998). Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev. Biol. 199, 93-110.
34. Onichtchouk, D., Chen, Y. G., Dosch, R., Gawantka, V., Delius, H., Massagué, J. and Niehrs, C. (1999). Silencing of TGF-β signalling by the pseudoreceptor BAMBI. Nature 401, 480-485.
35. Oxtoby, E. and Jowett, T. (1993). Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res. 21, 1087-1095.
36. Pieper, M., Ahrens, K., Rink, E., Peter, A. and Schlosser, G. (2012). Differential distribution of competence for panplacodal and neural crest induction to non-neural and neural ectoderm. Development 139, 1175-1187.
37. Pyati, U. J., Webb, A. E. and Kimelman, D. (2005). Transgenic zebrafish reveal stage-specific roles for BMP signaling in ventral and posterior mesoderm development. Development 132, 2333-2343.
38. Ramel, M. C. and Hill, C. S. (2012). Spatial regulation of BMP activity. FEBS Lett. 586, 1929-1941.
39. Ramel, M. C. and Hill, C. S. (2013). The ventral to dorsal BMP activity gradient in the early zebrafish embryo is determined by graded expression of BMP ligands. Dev. Biol. 378, 170-182.
40. Rentzsch, F., Zhang, J., Kramer, C., Sebald, W. and Hammerschmidt, M. (2006). Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133, 801-811.
41. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A. and Ekker, S. C. (2007). p53 activation by knockdown technologies. PLoS Genet. 3, e78.
42. Schier, A. F. and Talbot, W. S. (2005). Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39, 561-613.
43. Schmid, B., Fürthauer, M., Connors, S. A., Trout, J., Thisse, B., Thisse, C. and Mullins, M. C. (2000). Equivalent genetic roles for bmp7/snailhouse and bmp2b/swirl in dorsoventral pattern formation. Development 127, 957-967.
44. Schumacher, J. A., Hashiguchi, M., Nguyen, V. H. and Mullins, M. C. (2011). An intermediate level of BMP signaling directly specifies cranial neural crest progenitor cells in zebrafish. PLoS ONE 6, e27403.
45. Serpe, M., Umulis, D., Ralston, A., Chen, J., Olson, D. J., Avanesov, A., Othmer, H., O'Connor, M. B. and Blair, S. S. (2008). The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev. Cell 14, 940-953.
46. Sidi, S., Goutel, C., Peyriéras, N. and Rosa, F. M. (2003). Maternal induction of ventral fate by zebrafish radar. Proc. Natl. Acad. Sci. USA 100, 3315-3320.
47. Solomon, K. S. and Fritz, A. (2002). Concerted action of two dlx paralogs in sensory placode formation. Development 129, 3127-3136.
48. Steventon, B., Araya, C., Linker, C., Kuriyama, S. and Mayor, R. (2009). Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction. Development 136, 771-779.
49. Stuhlmiller, T. J. and García-Castro, M. I. (2012). Current perspectives of the signaling pathways directing neural crest induction. Cell. Mol. Life Sci. 69, 3715-3737.
50. Thisse, C., Thisse, B. and Postlethwait, J. H. (1995). Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Dev. Biol. 172, 86-99.
51. Tucker, J. A., Mintzer, K. A. and Mullins, M. C. (2008). The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev. Cell 14, 108-119.
52. Tzahor, E. (2007). Wnt/β-catenin signaling and cardiogenesis: timing does matter. Dev. Cell 13, 10-13.
53. van Boxtel, A. L., Gansner, J. M., Hakvoort, H. W., Snell, H., Legler, J. and Gitlin, J. D. (2011). Lysyl oxidase-like 3b is critical for cartilage maturation during zebrafish craniofacial development. Matrix Biol. 30, 178-187.
54. von der Hardt, S., Bakkers, J., Inbal, A., Carvalho, L., Solnica-Krezel, L., Heisenberg, C. P. and Hammerschmidt, M. (2007). The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr. Biol. 17, 475-487.
55. Westerfield, M. (2000) The Zebrafish Book. A Guide for the Laboratory Use of Zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
56. Wilson, P. A., Lagna, G., Suzuki, A. and Hemmati-Brivanlou, A. (1997). Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smad1. Development 124, 3177-3184.
57. Wu, M. Y. and Hill, C. S. (2009). Tgf-β superfamily signaling in embryonic development and homeostasis. Dev. Cell 16, 329-343.
58. Wu, M. Y., Ramel, M. C., Howell, M. and Hill, C. S. (2011). SNW1 is a critical regulator of spatial BMP activity, neural plate border formation, and neural crest specification in vertebrate embryos. PLoS Biol. 9, e1000593.
59. Zhang, J. L., Patterson, L. J., Qiu, L. Y., Graziussi, D., Sebald, W. and Hammerschmidt, M. (2010). Binding between Crossveinless-2 and Chordin von Willebrand factor type C domains promotes BMP signaling by blocking Chordin activity. PLoS ONE 5, e12846.