The homeobox gene bozozok promotes anterior neuroectoderm formation in zebrafish through negative regulation of BMP2/4 and Wnt pathways

Development

Volumn 127, Issue 11, 2000, Pages 2333-2345

  Fekany Lee, Kimberly ^a   Gonzalez, Encina ^a   Miller Bertoglio, Valarie ^b   Solnica Krezel, Lilianna ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

BMP2 4; Bozozok; Chordino; Neuroectoderm; Wnt; Zebrafish

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; GASTRULA; GASTRULATION; GENE EXPRESSION; GENETIC REGULATION; HOMEOBOX; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; BRAIN; ECTODERM; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MUTAGENESIS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; ANURA; DANIO RERIO; VERTEBRATA;

EID: 0034098352     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (82)

1. Akimenko, M. A., Ekker, M., Wegner, J., Lin, W. and Westerfield, M. (1994). Combinatorial expression of three zebrafish genes related to distalless: part of a homeobox gene code for the head. J. Neurosci. 14, 3475-3486.
2. Barth, K. A., Kishimoto, Y., Rohr, K. B., Seydler, C., Schulte-Merker, S. and Wilson, S. W. (1999). Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development 126, 4977-4987.
3. Beddington, R. S. P. and Robertson, E. J. (1999). Axis development and early asymmetry in Mammals. Cell 96, 195-209.
4. Belo, J. A., Bouwmeester, T., Leyns, L., Kertesz, N., Gallo, M., Follettie, M. and De Robertis, E. M. (1997). Cerberus-like is a secreted factor with neuralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech. Dev. 68, 45-57.
5. Blumberg, B., Bolado, J. J., Moreno, T. A., Kintner, C., Evans, R. M. and Papalopulu, N. (1997). An essential role for retinoid signaling in anteroposterior neural patterning. Development 124, 373-379.
6. Chin, A. J., Chen, J. and Weinberg, E. S. (1997). Bone Morphogenetic protein-4 characterizes inductive boundaries in organs of the developing zebrafish. Dev. Genes Evol. 207, 107-114.
7. Detrich, H. W., Kieran, M. W., Chan, F. Y., Barone, L. M., Yee, K., Rundstadler, J. A. and Zon, L. I. (1995). Intra-embryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. USA 92, 10713-10717.
8. Doniach, T. (1995). Basic FGF as an inducer of anteroposterior neural pattern. Cell 83, 1067-1070.
9. Fekany, K., Yamanaka, Y., Leung, T., Sirotkin, H. I., Topczewski, J., Gates, M. A., Hibi, M., Renucci, A., Stemple, D., Radbill, A. et al. (1999). The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 126, 1427-1438.
10. Feldman, B., Gates, M. A., Egan, E. S., Dougan, S. T., Rennebeck, G., Sirotkin, H. I., Schier, A. F. and Talbot, W. S. (1998). Zebrafish organizer development and germ-layer formation require nodal-related signals. Nature 395, 181-185.
11. Glinka, A., Wu, W., 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.
12. Glinka, A., Wu, W., Onichtchouk, D., Blumenstock, C. and Niehrs, C. (1997). Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus. Nature 389, 517-519.
13. Grinblat, Y., Lane, M. E., Sagerstrom, C. and Sive, H. (1999). Analysis of zebrafish development using explant culture assays. Methods Cell Biol. 59, 127-156.
14. Gritsman, K., Zhang, J., Cheng, S., Heckscher, E., Talbot, W. S. and Schier, A. F. (1999). The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97, 121-132.
15. Hammerschmidt, M., Pelegri, F., Mullins, M. C., Kane, D. A., van Eeden, F. J. M., Granato, M., Brand, M., Furutani-Seiki, M., Hafter, P., Heisenberg, C.-P. et al. (1996a), dino and mercedes, two genes regulating dorsal development in the zebrafish embryo. Development 123, 95-102.
16. Hammerschmidt, M., Serbedzija, G. N. and McMahon, A. (1996b). Genetic analysis of dorsoventral pattern formation in the zebrafish: requirement of BMP-like ventralizing activity and its dorsal repressor. Genes Dev. 10, 2452-2461.
17. Harland, R. and Gerhart, J. (1997). Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667.
18. Hashimoto, H., Itoh, M., Yamanaka, Y., Yamashita, S., Shimizu, T., Solnica-Krezel, L., Hibi, M. and Hirano, T. (2000). Zebrafish dkk1 functions in forebrain specification and axial mesendoderm formation [In Process Citation]. Dev. Biol. 217, 138-152.
19. Hemmati-Brivanlou, A. and Melton, D. (1997). Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88, 13-17.
20. Ho, C.-Y., Houart, C., Wilson, S. W. and Stainier, D. Y. R. (1999). A role for the extraembryonic yolk syncytial layer in patterning the zebrafish embryo suggested by properties of the hex gene. Curr. Biol. 9, 1131-1134.
21. Hoppler, S., Brown, J. and Moon, R. T. (1996). Expression of a dominant-negative Wnt blocks induction of myoD in Xenopus embryos. Genes Dev. 10, 2805-2817.
22. Hoppler, S. and Moon, R. T. (1998). BMP-2/-4 and Wnt-8 cooperatively pattern the Xenopus mesoderm. Mech. Dev. 71, 119-129.
23. Houart, C., Westerfield, M. and Wilson, S. W. (1998). A small population of anterior cells patterns the forebrain during zebrafish gastrulation [see comments]. Nature 391, 788-792.
24. Hug, B., Walter, V. and Grunwald, D. J. (1997). tbx6, a Brachyury-related gene expressed by ventral mesendermal precursors in the zebrafish embryo. Dev. Biol. 183, 61-73.
25. Itoh, K. and Sokol, S. (1999). Axis determination by inhibition of Wnt signaling in Xenopus. Genes Dev. 13, 2328-2336.
26. Joly, J. S., Joly, C., Schulte-Merker, S., Boulekbache, H. and Condamine, H. (1993). The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos. Development 119, 1261-1275.
27. 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.
28. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dynam. 203, 253-310.
29. 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.
30. Kobayashi, M., Toyama, R., Takeda, H., Dawid, I. B. and Kawakami, K. (1998). Overexpression of the forebrain-specific homeobox gene six3 induces rostral forebrain enlargement in zebrafish. Development 125, 2973-2982.
31. Kolm, P. J. and Sive, H. L. (1997). Retinoids and posterior neural induction: a reevaluation of Nieuwkoop's two-step hypothesis. In Cold Spring Harbor Symposi, vol. LXII (ed. 511-521. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
32. Koos, D. S. and Ho, R. K. (1998). The nieuwkoid gene characterizes and mediates a Nieuwkoop-center-like activity in zebrafish. Curr. Biol. 8, 1199-1206.
33. Koos, D. S. and Ho, R. K. (1999). The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula. Dev. Biol. 215, 190-207.
34. Koshida, S., Shinya, M., Mizuno, T., Kuroiwa, A. and Takeda, H. (1998). Initial anteroposterior pattern of the zebrafish central nervous system is determined by differential competence of the epiblast. Development 125, 1957-1966.
35. Krauss, S., Johansen, T., Korzh, V. and Fjose, A. (1991). Expression pattern of zebrafish pax genes suggests a role in early brain regionalization. Nature 353, 267-270.
36. Lamb, T. M., Knecht, A. K., Smith, W. C., Stachel, S. E., Economides, A. N., Stahl, N., Yancopolous, G. D. and Harland, R. M. (1993). Neural induction by the secreted polypeptide noggin. Science 262, 713-718.
37. Laurent, M. N., Blitz, I. L., Hashimoto, C., Rothbacher, U. and Cho, K. W. (1997). The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer. Development 124, 4905-4916.
38. Lemaire, P., Garret, N. and Gurdon, J. B. (1995). Expression cloning of Siamois, a Xenopus homobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 81, 85-94.
39. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. and De Robertis, E. M. (1997). Frzb-1 is a secreted antagonist of Wnt signalling expressed in the Spemann organizer. Cell 88, 747-756.
40. Li, Y., Allende, M. L., Finkelstein, R. and Weinberg, E. S. (1994). Expression of two zebrafish orthodenticle-related genes in the embryonic brain. Mech. Dev. 48, 229-244.
41. Marlow, F., Zwartkruis, F., Malicki, J., Neuhauss, S. C. F., Abbas, L., Weaver, M., Driever, W. and Solnica-Krezel, L. (1998). Functional Interactions of genes mediating convergent extension, knypek and trilobite, during partitioning of the eye primordium in zebrafish. Dev. Biol. 203, 382-399.
42. McGrew, L. L., Hoppler, S. and Moon, R. T. (1997). Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. Mech. Dev. 69, 105-114.
43. McGrew, L. L., Lai, C. J. and Moon, R. T. (1995). Specification of the antero-posterior neural axis through synergistic interactions of the Wnt signaling cascade with noggin and follistatin. Dev. Biol. 172, 337-342.
44. Miller-Bertoglio, V., Carmany-Rampey, A., Furthauer, M., Gonzalez, E. M., Thisse, C., Thisse, B., Halpern, M. E. and Solnica-Krezel, L. (1999). Maternal and zygotic activity of the zebrafish ogon locus antagonizes BMP signaling. Dev. Biol. 214, 72-86.
45. Miller-Bertoglio, V. E., Fisher, S., Sanchez, A., Mullins, M. C. and Halpern, M. E. (1997). Differential regulation of chordin expression domains in mutant zebrafish. Dev. Biol. 192, 537-550.
46. Moon, R. T., Brown, J. D., Yang-Snyder, J. A. and Miller, J. R. (1998). Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell 88, 725-728.
47. Moon, R. T. and Kimelman, D. (1998). From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus. BioEssays 20, 536-545.
48. Muhr, J., Jessel, T. M. and Edlund, T. (1997). Assignment of Early Caudal Identity to Neural Plate Cells by a Signal from Caudal Paraxial Mesoderm. Neuron 19, 487-502.
49. Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., Brand, M., van Eeden, F. J. M., Furutani-Seiki, M., Granato, M., Hafter, P., Heisenberg, C.-P. et al. (1996). Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123, 81-93.
50. 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.
51. Neave, B., Rodway, A., Wilson, S. W., Patient, R. and Holder, N. (1995). Expression of zebrafish GATA3 (gta3) during gastrulation and neurulation suggests a role in the specification of cell fate. Mech. Dev. in press.
52. 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.
53. Nieuwkoop, P. D. (1973). The organization center of the amphibian embryo: its origin, spatial organization, and morphogenetic action. Adv. Morphog. 10, 1-39.
54. Nieuwkoop, P. D., Boterenbrood, E. C., Kremer, A., Bloesma, F. F. S. N., Hoessels, E. L. M. J., Meyer, G. and Verheyen, F. J. (1952). Activation and organization of the central nervous system in amphibians. J. Exp. Zool. 120, 1-108.
55. Nikaido, M., Tada, M., Saji, T. and Ueno, N. (1997). Conservation of BMP signaling in zebrafish mesoderm patterning. Mech. Dev. 61, 75-88.
56. Nikaido, M., Tada, M., Takeda, H., Kuroiwa, A. and Ueno, N. (1999). In vivo analysis using variants of zebrafish BMPR-IA: range of action and involvement of BMP in ectoderm patterning. Development 126, 181-190.
57. Oxtoby, E. and Jowett, T. (1993). Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucl. Acids Res. 21, 1087-1095.
58. Pelegri, F. and Maischein, H.-M. (1998). Function of zebrafish b-catenin and TCF-3 in dorsoventral patterning. Mech. Dev. 77, 63-74.
59. Piccolo, S., Agius, E., Leyns, L., Phattacharyya, S., Grunz, H., Bouwmeester, T. and De Robertis, E. M. (1999) The head inducer cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710.
60. Piccolo, S., Sasai, Y., Lu, B. and De Robertis, E. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
61. Sampath, K., Rubinstein, A. L., Cheng, A. M. S., Liang, J. O., Fekany, K., Solnica-Krezel, L., Korzh, V., Halpern, M. E. and Wright, C. V. E. (1998). Induction of the zebrafish ventral brain and floor plate requires Cyclops/Nodal Signaling. Nature 395, 185-189.
62. Sasai, Y. and De Robertis, E. (1997). Ectodermal patterning in vertebrate embryos. Dev. Biol. 182, 5-20.
63. Sasai, Y., Lu, B., Steinbeisser, H. and De Robertis, E. M. (1995). Regulation of neural induction by the chordin and Bmp-4 antagonistic patterning signals in Xenopus. Nature 376, 333-337.
64. Schneider, S., Steinbesser, H., Warga, R. M. and Hausen, P. (1996). β-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech. Dev. 57, 191-198.
65. Schulte-Merker, S., Lee, K. J., McMahon, A. P. and Hammerschmidt, M. (1997). The zebrafish organizer requires chordino. Nature 387, 862-863.
66. Shawlot, W., Deng, J. M. and Behringer, R. R. (1998). Expression of the mouse cerberus-related gene, Cerr1, suggests a role in anterior neural induction and somitogenesis. Proc. Natl. Acad. Sci. USA 95, 6198-6203.
67. Smith, W. and Harland, R. (1992). Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
68. Solnica-Krezel, L., Schier, A. F. and Driever, W. (1994). Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 136, 1401-1420.
69. Solnica-Krezel, L., Stemple, D. L., Mountcastle-Shah, E., Rangini, Z., Neuhauss, S. C. F., Malicki, J., Schier, A., Stainier, D. Y. R., Zwartkruis, F., Abdelilah, S. et al. (1996). Mutations affecting cell fates and cellular rearrangements during gastrulation in zebrafish. Development 123, 117-128.
70. Spemann, H. (1938). Embryonic Development and Induction. New Haven, CT: Yale University Press.
71. Talbot, W. S., Trevarrow, W., Halpern, M. E., Melby, A. E., Farr, G., Postlethwait, J. H., Jowett, T., Kimmel, C. B. and Kimelman, D. (1995). A homeobox gene essential for zebrafish notochord development. Nature 378, 150-157.
72. Thisse, C. and Thisse, B. (1998). High resolution whole-mount in situ hybridization. In Zebrafish Science Monitor, vol. 5. Eugene: University of Oregon Press.
73. Thomas, P. and Beddington, R. (1996). Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Current Biology 6, 1487-1496.
74. Wang, S., Krinks, M., Lin, K., Luyten, F. P. and Moos, M. J. (1997). Frzb, a secreted protein expressed in the Spemann organiser, binds and inhibits Wnt-8. Cell 88, 757-766.
75. Westerfield, M. (1996). The Zebrafish Book. Eugene: University of Oregon Press.
76. Wilson, P. A. and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331-333.
77. 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.
78. Woo, K. and Fraser, S. (1997). Specification of the zebrafish nervous system by nonaxial signals. Science 277, 254-257.
79. Woo, K. and Fraser, S. E. (1995). Order and coherence in the fate map of the zebratish nervous system. Development 121, 2595-2609.
80. Yamamoto, A., Amacher, S. L., Kim, S. H., Geissert, D., Kimmel, C. B. and De Robertis, E. M. (1998). Zebrafish paraxial protocadherin is a downstream target of spadetail involved in morphogenesis of gastrula mesoderm. Development 125, 3389-3397.
81. Yamanaka, Y., Mizuna, T., Sasai, Y., Khishi, M., Takeda, H., Kim, C.-H., Hibi, M. and Hirano, T. (1998). A novel homeohox gene, dharma, can induce the organizer in a non-cell-autonomous manner. Genes Dev. 12, 2345-2353.
82. Zimmerman, L. B., De Jesus-Escobar, J. M. and Harland, R. M. (1996). The Spemann Organizer signal Noggin binds and inactivates Bone Morphogentic Protein 4. Cell 86, 599-606.