Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements

Jason R. Jessen, Jacek Topczewski, Stephanie Bingham, Diane S. Sepich, Florence Marlow, Anand Chandrasekhar, Lilianna Solnica-Krezel

Research output: Contribution to journalArticle

369 Citations (Scopus)

Abstract

Embryonic morphogenesis is driven by a suite of cell behaviours, including coordinated shape changes, cellular rearrangements and individual cell migrations, whose molecular determinants are largely unknown. In the zebrafish, Dani rerio, trilobite mutant embryos have defects in gastrulation movements1-4 and posterior migration of hindbrain neurons5. Here, we have used positional cloning to demonstrate that trilobite mutations disrupt the transmembrane protein Strabismus (Stbm)/Van Gogh (Vang), previously associated with planar cell polarity (PCP) in Drosophila melanogaster6,7, and PCP and canonical Wnt/β-catenin signalling in vertebrates8,9. Our genetic and molecular analyses argue that during gastrulation, trilobite interacts with the PCP pathway without affecting canonical Wnt signalling. Furthermore, trilobite may regulate neuronal migration independently of PCP molecules. We show that trilobite mediates polarization of distinct movement behaviours. During gastrulation convergence and extension movements, trilobite regulates mediolateral cell polarity underlying effective intercalation and directed dorsal migration at increasing velocities. In the hindbrain, trilobite controls effective migration of branchiomotor neurons towards posterior rhombomeres. Mosaic analyses show trilobite functions cell-autonomously and non-autonomously in gastrulae and the hindbrain. We propose Trilobite/Stbm mediates cellular interactions that confer directionality on distinct movements during vertebrate embryogenesis.

Original languageEnglish (US)
Pages (from-to)610-615
Number of pages6
JournalNature Cell Biology
Volume4
Issue number8
DOIs
StatePublished - 2002
Externally publishedYes

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Cell Polarity
Gastrulation
Strabismus
Zebrafish
Rhombencephalon
Gastrula
Catenins
Morphogenesis
Drosophila
Embryonic Development
Cell Movement
Vertebrates
Organism Cloning
Molecular Biology
Embryonic Structures
Neurons
Mutation
Proteins

ASJC Scopus subject areas

  • Cell Biology

Cite this

Jessen, J. R., Topczewski, J., Bingham, S., Sepich, D. S., Marlow, F., Chandrasekhar, A., & Solnica-Krezel, L. (2002). Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nature Cell Biology, 4(8), 610-615. https://doi.org/10.1038/ncb828

Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. / Jessen, Jason R.; Topczewski, Jacek; Bingham, Stephanie; Sepich, Diane S.; Marlow, Florence; Chandrasekhar, Anand; Solnica-Krezel, Lilianna.

In: Nature Cell Biology, Vol. 4, No. 8, 2002, p. 610-615.

Research output: Contribution to journalArticle

Jessen, JR, Topczewski, J, Bingham, S, Sepich, DS, Marlow, F, Chandrasekhar, A & Solnica-Krezel, L 2002, 'Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements', Nature Cell Biology, vol. 4, no. 8, pp. 610-615. https://doi.org/10.1038/ncb828
Jessen JR, Topczewski J, Bingham S, Sepich DS, Marlow F, Chandrasekhar A et al. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nature Cell Biology. 2002;4(8):610-615. https://doi.org/10.1038/ncb828
Jessen, Jason R. ; Topczewski, Jacek ; Bingham, Stephanie ; Sepich, Diane S. ; Marlow, Florence ; Chandrasekhar, Anand ; Solnica-Krezel, Lilianna. / Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. In: Nature Cell Biology. 2002 ; Vol. 4, No. 8. pp. 610-615.
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