Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction

Xiaoyan Ge, Danielle Grotjahn, Elaine Welch, Jamie Lyman-Gingerich, Christiana Holguin, Eva Dimitrova, Elliot W. Abrams, Tripti Gupta, Florence L. Marlow, Taijiro Yabe, Anna Adler, Mary C. Mullins, Francisco Pelegri

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Maternal homozygosity for three independent mutant hecate alleles results in embryos with reduced expression of dorsal organizer genes and defects in the formation of dorsoanterior structures. A positional cloning approach identified all hecate mutations as stop codons affecting the same gene, revealing that hecate encodes the Glutamate receptor interacting protein 2a (Grip2a), a protein containing multiple PDZ domains known to interact with membrane-associated factors including components of the Wnt signaling pathway. We find that grip2a mRNA is localized to the vegetal pole of the oocyte and early embryo, and that during egg activation this mRNA shifts to an off-center vegetal position corresponding to the previously proposed teleost cortical rotation. hecate mutants show defects in the alignment and bundling of microtubules at the vegetal cortex, which result in defects in the asymmetric movement of wnt8a mRNA as well as anchoring of the kinesin-associated cargo adaptor Syntabulin. We also find that, although short-range shifts in vegetal signals are affected in hecate mutant embryos, these mutants exhibit normal long-range, animally directed translocation of cortically injected dorsal beads that occurs in lateral regions of the yolk cortex. Furthermore, we show that such animally-directed movement along the lateral cortex is not restricted to a single arc corresponding to the prospective dorsal region, but occur in multiple meridional arcs even in opposite regions of the embryo. Together, our results reveal a role for Grip2a function in the reorganization and bundling of microtubules at the vegetal cortex to mediate a symmetry-breaking short-range shift corresponding to the teleost cortical rotation. The slight asymmetry achieved by this directed process is subsequently amplified by a general cortical animally-directed transport mechanism that is neither dependent on hecate function nor restricted to the prospective dorsal axis.

Original languageEnglish (US)
Article numbere1004422
JournalPLoS Genetics
Volume10
Issue number6
DOIs
StatePublished - 2014
Externally publishedYes

Fingerprint

Embryonic Induction
Receptor-Interacting Protein Serine-Threonine Kinases
Glutamate Receptors
cytoskeleton
Cytoskeleton
symmetry
embryo
cortex
embryo (animal)
Embryonic Structures
defect
mutants
protein
teleost
Microtubules
Messenger RNA
microtubules
proteins
PDZ Domains
Kinesin

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

Ge, X., Grotjahn, D., Welch, E., Lyman-Gingerich, J., Holguin, C., Dimitrova, E., ... Pelegri, F. (2014). Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction. PLoS Genetics, 10(6), [e1004422]. https://doi.org/10.1371/journal.pgen.1004422

Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction. / Ge, Xiaoyan; Grotjahn, Danielle; Welch, Elaine; Lyman-Gingerich, Jamie; Holguin, Christiana; Dimitrova, Eva; Abrams, Elliot W.; Gupta, Tripti; Marlow, Florence L.; Yabe, Taijiro; Adler, Anna; Mullins, Mary C.; Pelegri, Francisco.

In: PLoS Genetics, Vol. 10, No. 6, e1004422, 2014.

Research output: Contribution to journalArticle

Ge, X, Grotjahn, D, Welch, E, Lyman-Gingerich, J, Holguin, C, Dimitrova, E, Abrams, EW, Gupta, T, Marlow, FL, Yabe, T, Adler, A, Mullins, MC & Pelegri, F 2014, 'Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction', PLoS Genetics, vol. 10, no. 6, e1004422. https://doi.org/10.1371/journal.pgen.1004422
Ge, Xiaoyan ; Grotjahn, Danielle ; Welch, Elaine ; Lyman-Gingerich, Jamie ; Holguin, Christiana ; Dimitrova, Eva ; Abrams, Elliot W. ; Gupta, Tripti ; Marlow, Florence L. ; Yabe, Taijiro ; Adler, Anna ; Mullins, Mary C. ; Pelegri, Francisco. / Hecate/Grip2a Acts to Reorganize the Cytoskeleton in the Symmetry-Breaking Event of Embryonic Axis Induction. In: PLoS Genetics. 2014 ; Vol. 10, No. 6.
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abstract = "Maternal homozygosity for three independent mutant hecate alleles results in embryos with reduced expression of dorsal organizer genes and defects in the formation of dorsoanterior structures. A positional cloning approach identified all hecate mutations as stop codons affecting the same gene, revealing that hecate encodes the Glutamate receptor interacting protein 2a (Grip2a), a protein containing multiple PDZ domains known to interact with membrane-associated factors including components of the Wnt signaling pathway. We find that grip2a mRNA is localized to the vegetal pole of the oocyte and early embryo, and that during egg activation this mRNA shifts to an off-center vegetal position corresponding to the previously proposed teleost cortical rotation. hecate mutants show defects in the alignment and bundling of microtubules at the vegetal cortex, which result in defects in the asymmetric movement of wnt8a mRNA as well as anchoring of the kinesin-associated cargo adaptor Syntabulin. We also find that, although short-range shifts in vegetal signals are affected in hecate mutant embryos, these mutants exhibit normal long-range, animally directed translocation of cortically injected dorsal beads that occurs in lateral regions of the yolk cortex. Furthermore, we show that such animally-directed movement along the lateral cortex is not restricted to a single arc corresponding to the prospective dorsal region, but occur in multiple meridional arcs even in opposite regions of the embryo. Together, our results reveal a role for Grip2a function in the reorganization and bundling of microtubules at the vegetal cortex to mediate a symmetry-breaking short-range shift corresponding to the teleost cortical rotation. The slight asymmetry achieved by this directed process is subsequently amplified by a general cortical animally-directed transport mechanism that is neither dependent on hecate function nor restricted to the prospective dorsal axis.",
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