Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

Nanbing Li-Villarreal, Meredyth M. Forbes, Andrew J. Loza, Jiakun Chen, Taylur Ma, Kathryn Helde, Cecilia B. Moens, Jimann Shin, Atsushi Sawada, Anna E. Hindes, Julien Dubrulle, Alexander F. Schier, Gregory D. Longmore, Florence L. Marlow, Lilianna Solnica-Krezel

Research output: Contribution to journalArticlepeer-review

14 Scopus citations

Abstract

Dachsous (Dchs), an atypical cadherin, is an evolutionarily conserved regulator of planar cell polarity, tissue size and cell adhesion. In humans, DCHS1 mutations cause pleiotropic Van Maldergem syndrome. Here, we report that mutations in zebrafish dchs1b and dchs2 disrupt several aspects of embryogenesis, including gastrulation. Unexpectedly, maternal zygotic (MZ) dchs1b mutants show defects in the earliest developmental stage, egg activation, including abnormal cortical granule exocytosis (CGE), cytoplasmic segregation, cleavages and maternal mRNA translocation, in transcriptionally quiescent embryos. Later, MZdchs1b mutants exhibit altered dorsal organizer and mesendodermal gene expression, due to impaired dorsal determinant transport and Nodal signaling. Mechanistically, MZdchs1b phenotypes can be explained in part by defective actin or microtubule networks, which appear bundled in mutants. Accordingly, disruption of actin cytoskeleton in wild-type embryos phenocopied MZdchs1b mutant defects in cytoplasmic segregation and CGE, whereas interfering with microtubules in wildtype embryos impaired dorsal organizer and mesodermal gene expression without perceptible earlier phenotypes. Moreover, the bundled microtubule phenotype was partially rescued by expressing either full-length Dchs1b or its intracellular domain, suggesting that Dchs1b affects microtubules and some developmental processes independent of its known ligand Fat. Our results indicate novel roles for vertebrate Dchs in actin and microtubule cytoskeleton regulation in the unanticipated context of the single-celled embryo.

Original languageEnglish (US)
Pages (from-to)2704-2718
Number of pages15
JournalDevelopment (Cambridge)
Volume142
Issue number15
DOIs
StatePublished - Aug 1 2015

Keywords

  • Actin
  • Cell fate
  • Dchs1b
  • Egg activation
  • Microtubule
  • Morphogenesis

ASJC Scopus subject areas

  • Molecular Biology
  • Developmental Biology

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