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A novel role for MAPKAPK2 in morphogenesis during zebrafish development
Journal article   Open access   Peer reviewed

A novel role for MAPKAPK2 in morphogenesis during zebrafish development

Beth A Holloway, Sol Gomez de la Torre Canny, Diane C Slusarski, Ying Ye, Christina M Freisinger, Roland Dosch, Margaret M Chou, Daniel S Wagner and Mary C Mullins
PLoS genetics, Vol.5(3), e1000413
03/2009
DOI: 10.1371/journal.pgen.1000413
PMCID: PMC2652113
PMID: 19282986
url
https://doi.org/10.1371/journal.pgen.1000413View
Published (Version of record) Open Access

Abstract

One of the earliest morphogenetic processes in the development of many animals is epiboly. In the zebrafish, epiboly ensues when the animally localized blastoderm cells spread, thin over, and enclose the vegetally localized yolk. Only a few factors are known to function in this fundamental process. We identified a maternal-effect mutant, betty boop (bbp), which displays a novel defect in epiboly, wherein the blastoderm margin constricts dramatically, precisely when half of the yolk cell is covered by the blastoderm, causing the yolk cell to burst. Whole-blastoderm transplants and mRNA microinjection rescue demonstrate that Bbp functions in the yolk cell to regulate epiboly. We positionally cloned the maternal-effect bbp mutant gene and identified it as the zebrafish homolog of the serine-threonine kinase Mitogen Activated Protein Kinase Activated Protein Kinase 2, or MAPKAPK2, which was not previously known to function in embryonic development. We show that the regulation of MAPKAPK2 is conserved and p38 MAP kinase functions upstream of MAPKAPK2 in regulating epiboly in the zebrafish embryo. Dramatic alterations in calcium dynamics, together with the massive marginal constrictive force observed in bbp mutants, indicate precocious constriction of an F-actin network within the yolk cell, which first forms at 50% epiboly and regulates epiboly progression. We show that MAPKAPK2 activity and its regulator p38 MAPK function in the yolk cell to regulate the process of epiboly, identifying a new pathway regulating this cell movement process. We postulate that a p38 MAPKAPK2 kinase cascade modulates the activity of F-actin at the yolk cell margin circumference allowing the gradual closure of the blastopore as epiboly progresses.
Morphogenesis Calcium - metabolism Protein-Serine-Threonine Kinases - physiology Actins - metabolism Intracellular Signaling Peptides and Proteins - metabolism Embryonic Development Zebrafish - embryology Zebrafish - growth & development Mutant Proteins Animals Egg Yolk Gastrula p38 Mitogen-Activated Protein Kinases - metabolism Intracellular Signaling Peptides and Proteins - physiology Protein-Serine-Threonine Kinases - metabolism Cell Movement

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