Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish

Jochen Holzschuh, Naoyuki Wada, Chikako Wada, Ashleigh Schaffer, Yashar Javidan, Alexandra Tallafuß, Laure Bally-Cuif, Thomas F. Schiling

Research output: Contribution to journalArticle

57 Citations (Scopus)

Abstract

Cranial sensory neurons largely derive from neurogenic placodes (epibranchial and dorsolateral), which are ectodermal thickenings that form the sensory ganglia associated with cranial nerves, but the molecular mechanisms of placodal development are unclear. Here, we show that the pharyngeal endoderm induces epibranchial neurogenesis in zebrafish, and that BMP signaling plays a crucial role in this process. Using a her5:egfp transgenic line to follow endodermal movements in living embryos, we show that contact between pharyngeal pouches and the surface ectoderm coincides with the onset of neurogenesis in epibranchial placodes. By genetic ablation and reintroduction of endoderm by cell transplantation, we show that these contacts promote neurogenesis. Using a genetic interference approach we further identify bmp2b and bmp5 as crucial components of the endodermal signals that induce epibranchial neurogenesis. Dorsolateral placodes (trigeminal, auditory, vestibular, lateral line) develop independently of the endoderm and BMP signaling, suggesting that these two sets of placodes are under separate genetic control. Our results show that the endoderm regulates the differentiation of cranial sensory ganglia, which coordinates the cranial nerves with the segments that they innervate.

Original languageEnglish (US)
Pages (from-to)3731-3742
Number of pages12
JournalDevelopment
Volume132
Issue number16
DOIs
StatePublished - Aug 1 2005
Externally publishedYes

Fingerprint

Endoderm
Neurogenesis
Zebrafish
Sensory Ganglia
Cranial Nerves
Ectoderm
Cell Transplantation
Sensory Receptor Cells
Embryonic Structures

Keywords

  • BMP
  • Endoderm
  • Epibranchial
  • Neural crest
  • Pharyngeal arches
  • Pharyngeal pouches
  • Placode
  • Segmentation
  • Zebrafish

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

Cite this

Holzschuh, J., Wada, N., Wada, C., Schaffer, A., Javidan, Y., Tallafuß, A., ... Schiling, T. F. (2005). Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development, 132(16), 3731-3742. https://doi.org/10.1242/dev.01936

Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. / Holzschuh, Jochen; Wada, Naoyuki; Wada, Chikako; Schaffer, Ashleigh; Javidan, Yashar; Tallafuß, Alexandra; Bally-Cuif, Laure; Schiling, Thomas F.

In: Development, Vol. 132, No. 16, 01.08.2005, p. 3731-3742.

Research output: Contribution to journalArticle

Holzschuh, J, Wada, N, Wada, C, Schaffer, A, Javidan, Y, Tallafuß, A, Bally-Cuif, L & Schiling, TF 2005, 'Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish', Development, vol. 132, no. 16, pp. 3731-3742. https://doi.org/10.1242/dev.01936
Holzschuh J, Wada N, Wada C, Schaffer A, Javidan Y, Tallafuß A et al. Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. Development. 2005 Aug 1;132(16):3731-3742. https://doi.org/10.1242/dev.01936
Holzschuh, Jochen ; Wada, Naoyuki ; Wada, Chikako ; Schaffer, Ashleigh ; Javidan, Yashar ; Tallafuß, Alexandra ; Bally-Cuif, Laure ; Schiling, Thomas F. / Requirements for endoderm and BMP signaling in sensory neurogenesis in zebrafish. In: Development. 2005 ; Vol. 132, No. 16. pp. 3731-3742.
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