Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish

Florence Marlow, Fried Zwartkruis, Jarema Malicki, Stephan C F Neuhauss, Leila Abbas, Molly Weaver, Wolfgang Driever, Lilianna Solnica-Krezel

Research output: Contribution to journalArticle

106 Citations (Scopus)

Abstract

Vertebrate eye development in the anterior region of the neural plate involves a series of inductive interactions dependent on the underlying prechordal plate and signals from the midline of the neural plate, including Hedgehog. The mechanisms controlling the spatiotemporal expression pattern of hedgehog genes are currently not understood. Cyclopia is observed in trilobite (tri) and knypek (kny) mutants with affected convergent extension of the embryonic axis during gastrulation. Here, we demonstrate that tri mutants show a high frequency of partial or complete cyclopia, kny mutants exhibit cyclopia infrequently, while kny(m119) tri(m209) double-mutant embryos have dramatically reduced convergent extension and are completely cyclopic. We analyzed the relationships between the convergent extension defect, the expression of hedgehog and prechordal plate genes, and the formation of cyclopia in kny(m119) and tri(m209) mutants. Our results correlate the cyclopia phenotype with the abnormal location of hh-expressing cells with respect to the optic primordium. We show that cyclopia in these mutants is not due to an incompetence of tri and kny cells to respond to Hedgehog signaling. Rather, it is a consequence of exceeding a critical distance (>40-50 μm) between hedgehog-expressing cells and the prospective eye field. We hypothesize that at this distance, midline cells are not in an appropriate position to physically separate the eye field and that HH and other signals do not reach the appropriate target cells. Furthermore, tri and kny have overlapping functions in establishing proper alignment of the anterior neural plate and midline cells expressing shh and twhh genes when the partitioning of the eye primordium takes place.

Original languageEnglish (US)
Pages (from-to)382-399
Number of pages18
JournalDevelopmental Biology
Volume203
Issue number2
DOIs
StatePublished - Nov 15 1998
Externally publishedYes

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Zebrafish
Hedgehogs
Neural Plate
Genes
Gastrulation
Vertebrates
Cyclopia
Embryonic Structures
Phenotype

Keywords

  • Cyclopia
  • Gastrulation
  • Hedgehog
  • Midline signaling
  • Prechordal plate

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Marlow, F., Zwartkruis, F., Malicki, J., Neuhauss, S. C. F., Abbas, L., Weaver, M., ... Solnica-Krezel, L. (1998). Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. Developmental Biology, 203(2), 382-399. https://doi.org/10.1006/dbio.1998.9032

Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. / Marlow, Florence; Zwartkruis, Fried; Malicki, Jarema; Neuhauss, Stephan C F; Abbas, Leila; Weaver, Molly; Driever, Wolfgang; Solnica-Krezel, Lilianna.

In: Developmental Biology, Vol. 203, No. 2, 15.11.1998, p. 382-399.

Research output: Contribution to journalArticle

Marlow, F, Zwartkruis, F, Malicki, J, Neuhauss, SCF, Abbas, L, Weaver, M, Driever, W & Solnica-Krezel, L 1998, 'Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish', Developmental Biology, vol. 203, no. 2, pp. 382-399. https://doi.org/10.1006/dbio.1998.9032
Marlow, Florence ; Zwartkruis, Fried ; Malicki, Jarema ; Neuhauss, Stephan C F ; Abbas, Leila ; Weaver, Molly ; Driever, Wolfgang ; Solnica-Krezel, Lilianna. / Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. In: Developmental Biology. 1998 ; Vol. 203, No. 2. pp. 382-399.
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