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.
Highlights
Embryonic development is marked by cellular movements that generate the shape of the embryo in a process known as morphogenesis
We identified a maternal-effect mutant, betty boop, 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
We show that the regulation of MAPKAPK2 is conserved within a p38 MAP kinase pathway, identifying a new pathway in the regulation of this fundamental cell movement process
Summary
Embryonic development is marked by cellular movements that generate the shape of the embryo in a process known as morphogenesis. One of the earliest morphogenetic events in many animals is the process of epiboly, whereby embryonic tissues spread and thin [1,2,3,4,5]. The deep blastomeres radially intercalate, while the underlying yolk moves animalward in a process called doming. At completion of this initial phase of epiboly, an inverted bowl-shaped blastoderm covers ,50% of the yolk surface, referred to as the 50% epiboly stage (Fig. 1). Epiboly continues with all three cell layers spreading over the yolk to the vegetal pole of the embryo, resulting in the complete internalization of the yolk [6]. The morphogenetic process of epiboly occurs in numerous other vertebrates and invertebrates, including amphibia, sea urchins, and C.elegans [1,2,3,4]
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