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

Nature Cell Biology volume 4, pages 610615 (2002) | Download Citation

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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 movements1,2,3,4 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.

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Acknowledgements

We thank B. Appel, R. Blakely, A. Schier, and C.V.E. Wright for critical comments. We thank J. Clanton and C. Baccam for excellent fish care, M. Halpern for γ-ray-mutagenized fish, M. Westerfield, H. Takeda, P. Ingham, M. Ekker, Y. Grinblat, B. Thisse, C. Thisse, E. Weinberg and T. Jowett for probes, R. Harland, S. Sokol and M. Tada for constructs, and C.-P. Heisenberg and H. Okamoto for fish. S.B. and A.C. are indebted to K. Cooper and C. Moens for invaluable guidance in transplantation procedures. The Zeiss confocal microscope is supported by National Insitutes of Health (NIH) grant 1S10RR015682. J.R.J. and D.S.S. are supported by a National Institutes of Health Vascular Biology Training Grant (T32HL07751). S.B. is supported by a NSF-Missouri's Alliance for Graduate Education and the Professoriate (MAGEP) fellowship and A.C. by NIH grant NS40449. L.S.K. is supported by NIH grant GM55101 and Pew Scholars Program in the Biomedical Sciences.

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Affiliations

  1. Department of Biological Sciences, Vanderbilt University, VU Station B 351634, Nashville, TN 37235, USA

    • Jason R. Jessen
    • , Jacek Topczewski
    • , Diane S. Sepich
    • , Florence Marlow
    •  & Lilianna Solnica-Krezel
  2. Division of Biological Sciences, University of Missouri, Columbia, MO 65211, USA

    • Stephanie Bingham
    •  & Anand Chandrasekhar

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The authors declare no competing financial interests.

Corresponding author

Correspondence to Lilianna Solnica-Krezel.

Supplementary information

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    Supplementary Methods and Figures

    Figure S1. Positional cloning of tri.Figure S2. Tri/Stbm does not regulate anteroposterior neural patterning.Figure S3. Epistatic analysis of tri and PCP pathway components.

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DOI

https://doi.org/10.1038/ncb828

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