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A small population of anterior cells patterns the forebrain during zebrafish gastrulation

Nature volume 391, pages 788–792 (1998)Cite this article

Abstract

During gastrulation in vertebrates, dorsal ectoderm is induced to form neural tissue that later gives rise to the brain and spinal cord. This induction depends on signals arising from a group of cells on the dorsal side of the gastrula. This group of cells constitutes the organizer1,2. It is thought that the organizer initially induces neural tissue with anterior, or forebrain, character, and that other signals subsequently posteriorize neural tissue in the trunk2,3. Here we show that development of the anterior central nervous system of the zebrafish embryo also depends on a small group of ectodermal cells located in the prospective head region. Removal of these ectodermal cells during gastrulation perturbs subsequent neural patterning and results in widespread cell death. Transplantation of these cells shows that they can induce forebrain-specific gene expression in more posterior regions of the neural plate. Our results indicate that an early step in neural patterning is the establishment of a small population of signalling cells within the most anterior region of the embryo. These cells are required for patterning and survival of the anterior brain.

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Figure 1: Ablation of row 1 removes ectodermal cells but does not affect the prechordal plate.
Figure 2: Ablation of row-1 cells at mid-gastrulation induces apoptosis in the brain.
Figure 3: Ablation of row 1 disturbs gene expression patterns in the anterior forebrain and inhibits neurogenesis.
Figure 4: Row-1 cells have signalling activity.
Figure 5: Row-1 cells signal during gastrulation.

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References

  1. Lemaire, P. & Kodjabachian, L. The vertebrate organizer: structure and molecules. Trends Genet 12, 525–531 (1996).

    Article  CAS  PubMed  Google Scholar 

  2. Sasai, Y. & DeRobertis, E. M. Ectodermal patterning in vertebrate embryos. Dev. Biol. 182, 5–20 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Woo, K. & Fraser, S. E. Specification of the zebrafish nervous system by nonaxial signals. Science 277, 254–257 (1997).

    Article  CAS  PubMed  Google Scholar 

  4. Li, Y., Allende, M. L., Finkelstein, R. & Weinberg, E. S. Expression of two zebrafish orthodenticle-related genes in the embryonic brain. Mech. Dev. 48, 229–244 (1994).

    Article  CAS  PubMed  Google Scholar 

  5. Neave, B., Rodaway, A., Wilson, S. W., Patient, R. & Holder, N. Expression of zebrafish GATA3 (gta3) during gastrulation and neurulation suggests a role in the specification of cell fate. Mech. Dev. 51, 169–182 (1995).

    Article  CAS  PubMed  Google Scholar 

  6. Brand, M. et al. Mutations affecting development of the midline and general body shape during zebrafish embryogenesis. Development 123, 129–142 (1996).

    CAS  PubMed  Google Scholar 

  7. Thisse, C., Thisse, B., Halpern, M. E. & Postlethwait, J. H. Goosecoid expression in neurectoderm and mesoderm is disrupted in cyclops gastrulas. Dev. Biol. 164, 420–429 (1994).

    Article  CAS  PubMed  Google Scholar 

  8. Morita, T., Nitta, H., Kiyama, Y., Mori, H. & Mishina, M. Differential expression of two zebrafish emx homeoprotein mRNAs in the developing brain. Neurosci. Lett. 198, 131–134 (1995).

    Article  CAS  PubMed  Google Scholar 

  9. Akimenko, M.-A., Ekker, M., Wegner, J., Lin, W. & Westerfield, M. Combinatorial expression of three zebrafish genes related to Distal-less: part of a homeobox gene code for the head. J. Neurosci. 14, 3475–3486 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Krauss, S., Concordet, J.-P. & Ingham, P. Afunctionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431–1444 (1993).

    Article  CAS  PubMed  Google Scholar 

  11. Macdonald, R. et al. Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the zebrafish forebrain. Neuron 13, 1039–1053 (1994).

    Article  CAS  PubMed  Google Scholar 

  12. Barth, K. A. & Wilson, S. W. Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755–1768 (1995).

    CAS  PubMed  Google Scholar 

  13. Allende, M. L. & Weinberg, E. The expression pattern of two zebrafish acheate-scute homologue (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev. Biol. 166, 509–530 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Shimamura, K. & Rubenstein, J. L. R. Inductive interactions direct early regionalisation of the mouse forebrain. Development 124, 2709–2718 (1997).

    CAS  PubMed  Google Scholar 

  15. Fürthauer, M., Thisse, C. & Thisse, B. Arole for FGF in the dorsoventral patterning of the zebrafish gastrula. Development 124, 4253–4264 (1997).

    PubMed  Google Scholar 

  16. Thomas, P. & Beddington, R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6, 1487–1496 (1996).

    Article  CAS  PubMed  Google Scholar 

  17. Varlet, I., Collingnon, J. & Robertson, E. J. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124, 1033–1044 (1997).

    CAS  PubMed  Google Scholar 

  18. Bouwmeester, T., Kim, S.-H., Sasai, Y., Lui, B. & DeRobertis, E. M. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 382, 595–601 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Bradley, L., Wainstock, D. & Sive, H. Positive and negative signals modulate formation of the Xenopus cement gland. Development 122, 2739–2750 (1996).

    CAS  PubMed  Google Scholar 

  20. Mizuno, T., Yamaha, E., Wakahara, M., Kuroiwa, A. & Takeda, H. Mesoderm induction in zebrafish. Nature 383, 131–132 (1996).

    Article  ADS  CAS  Google Scholar 

  21. Westerfield, M. The Zebrafish Book (Univ. Oregon Press, (1996)).

    Google Scholar 

  22. Heisenberg, C. P. et al. Genes involved in forebrain development in the zebrafish, Danio rerio. Development 123, 191–203 (1996).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank N. Holder, C. Kimmel, K. Whitlock and Z. Varga for comments on the manuscript and our colleagues for advice throughout this study. We thank many colleagues for providing antibodies and probes. The study was supported by grants from the BBSRC and Wellcome Trust (to S.W.W.) and from the NIH, NATO and W. M. Keck Foundation to M.W. C.H. received a Fellowship from the EC and is currently supported by the BBSRC. S.W. is a Wellcome Trust Senior Research Fellow.

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  1. Stephen W. Wilson

    Present address: Department of Anatomy and Development Biology, University College London, Gower Street, London, WC1E 6BT, UK

Authors and Affiliations

  1. Developmental Biology Research Centre, The Randall Institute, Kings College London, 2629 Drury Lane, WC2 5RL, London, UK

    Corinne Houart

  2. Institute of Neuroscience, University of Oregon, Eugene, 97403, Oregon, USA

    Corinne Houart & Monte Westerfield

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  1. Corinne Houart
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Correspondence to Corinne Houart.

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Houart, C., Westerfield, M. & Wilson, S. A small population of anterior cells patterns the forebrain during zebrafish gastrulation. Nature 391, 788–792 (1998). https://doi.org/10.1038/35853

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