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 journalArticle

12 Citations (Scopus)

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

Fingerprint

Zebrafish
Cadherins
Actin Cytoskeleton
Microtubules
Embryonic Development
Embryonic Structures
Exocytosis
Phenotype
Stored Messenger RNA
Tissue Adhesions
Cytoplasmic Granules
Gene Expression
Cell Polarity
Gastrulation
Mutation
Cell Adhesion
Ovum
Vertebrates
Actins
Mothers

Keywords

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

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

Li-Villarreal, N., Forbes, M. M., Loza, A. J., Chen, J., Ma, T., Helde, K., ... Solnica-Krezel, L. (2015). Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis. Development (Cambridge), 142(15), 2704-2718. https://doi.org/10.1242/dev.119800

Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis. / Li-Villarreal, Nanbing; Forbes, Meredyth M.; Loza, Andrew J.; Chen, Jiakun; Ma, Taylur; Helde, Kathryn; Moens, Cecilia B.; Shin, Jimann; Sawada, Atsushi; Hindes, Anna E.; Dubrulle, Julien; Schier, Alexander F.; Longmore, Gregory D.; Marlow, Florence L.; Solnica-Krezel, Lilianna.

In: Development (Cambridge), Vol. 142, No. 15, 01.08.2015, p. 2704-2718.

Research output: Contribution to journalArticle

Li-Villarreal, N, Forbes, MM, Loza, AJ, Chen, J, Ma, T, Helde, K, Moens, CB, Shin, J, Sawada, A, Hindes, AE, Dubrulle, J, Schier, AF, Longmore, GD, Marlow, FL & Solnica-Krezel, L 2015, 'Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis', Development (Cambridge), vol. 142, no. 15, pp. 2704-2718. https://doi.org/10.1242/dev.119800
Li-Villarreal, Nanbing ; Forbes, Meredyth M. ; Loza, Andrew J. ; Chen, Jiakun ; Ma, Taylur ; Helde, Kathryn ; Moens, Cecilia B. ; Shin, Jimann ; Sawada, Atsushi ; Hindes, Anna E. ; Dubrulle, Julien ; Schier, Alexander F. ; Longmore, Gregory D. ; Marlow, Florence L. ; Solnica-Krezel, Lilianna. / Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis. In: Development (Cambridge). 2015 ; Vol. 142, No. 15. pp. 2704-2718.
@article{a2b20538a71f40ec97b676ff8ffbf062,
title = "Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis",
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.",
keywords = "Actin, Cell fate, Dchs1b, Egg activation, Microtubule, Morphogenesis",
author = "Nanbing Li-Villarreal and Forbes, {Meredyth M.} and Loza, {Andrew J.} and Jiakun Chen and Taylur Ma and Kathryn Helde and Moens, {Cecilia B.} and Jimann Shin and Atsushi Sawada and Hindes, {Anna E.} and Julien Dubrulle and Schier, {Alexander F.} and Longmore, {Gregory D.} and Marlow, {Florence L.} and Lilianna Solnica-Krezel",
year = "2015",
month = "8",
day = "1",
doi = "10.1242/dev.119800",
language = "English (US)",
volume = "142",
pages = "2704--2718",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "15",

}

TY - JOUR

T1 - Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis

AU - Li-Villarreal, Nanbing

AU - Forbes, Meredyth M.

AU - Loza, Andrew J.

AU - Chen, Jiakun

AU - Ma, Taylur

AU - Helde, Kathryn

AU - Moens, Cecilia B.

AU - Shin, Jimann

AU - Sawada, Atsushi

AU - Hindes, Anna E.

AU - Dubrulle, Julien

AU - Schier, Alexander F.

AU - Longmore, Gregory D.

AU - Marlow, Florence L.

AU - Solnica-Krezel, Lilianna

PY - 2015/8/1

Y1 - 2015/8/1

N2 - 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.

AB - 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.

KW - Actin

KW - Cell fate

KW - Dchs1b

KW - Egg activation

KW - Microtubule

KW - Morphogenesis

UR - http://www.scopus.com/inward/record.url?scp=84938613446&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84938613446&partnerID=8YFLogxK

U2 - 10.1242/dev.119800

DO - 10.1242/dev.119800

M3 - Article

C2 - 26160902

AN - SCOPUS:84938613446

VL - 142

SP - 2704

EP - 2718

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 15

ER -