Introduction of cloned DNA into sea urchin egg cytoplasm: Replication and persistence during embryogenesis

McMahon, Andrew P.; Flytzanis, Constantin N.; Hough-Evans, Barbara R.; Katula, Karen S.; Britten, Roy J.; Davidson, Eric H.

doi:10.1016/0012-1606(85)90045-4

Cited by 222 publications

(135 citation statements)

References 38 publications

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“…WMISH was conducted essentially after Ransick (43), with modifications. Microinjection experiments in Et were done essentially as described elsewhere for euechinoids (44).…”

Section: Methodsmentioning

confidence: 99%

Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses

Erkenbrack

Davidson

2015

Proc. Natl. Acad. Sci. U.S.A.

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Evolution of animal body plans occurs with changes in the encoded genomic programs that direct development, by alterations in the structure of encoded developmental gene-regulatory networks (GRNs). However, study of this most fundamental of evolutionary processes requires experimentally tractable, phylogenetically divergent organisms that differ morphologically while belonging to the same monophyletic clade, plus knowledge of the relevant GRNs operating in at least one of the species. These conditions are met in the divergent embryogenesis of the two extant, morphologically distinct, echinoid (sea urchin) subclasses, Euechinoidea and Cidaroidea, which diverged from a common late Paleozoic ancestor. Here we focus on striking differences in the mode of embryonic skeletogenesis in a euechinoid, the well-known model Strongylocentrotus purpuratus (Sp), vs. the cidaroid Eucidaris tribuloides (Et). At the level of descriptive embryology, skeletogenesis in Sp and Et has long been known to occur by distinct means. The complete GRN controlling this process is known for Sp. We carried out targeted functional analyses on Et skeletogenesis to identify the presence, or demonstrate the absence, of specific regulatory linkages and subcircuits key to the operation of the Sp skeletogenic GRN. Remarkably, most of the canonical design features of the Sp skeletogenic GRN that we examined are either missing or operate differently in Et. This work directly implies a dramatic reorganization of genomic regulatory circuitry concomitant with the divergence of the euechinoids, which began before the end-Permian extinction.GRN evolution | network linkages | embryonic skeletogenesis | sea urchin embryogenesis T he mechanisms responsible for evolutionary divergence of animal body plans, as so extensively documented in the Phanerozoic fossil record, lie in alterations of the encoded genomic regulatory programs that direct development. This principle has long been evident a priori (1), and overwhelmingly, accumulating current evidence precludes any other general explanation (2). However, it still remains a challenge to adduce specific examples in which evolutionary rewiring of developmental gene-regulatory networks (GRNs) can be seen to account for observed differences in morphogenetic processes that distinguish descendants of a common ancestor. Knowledge of developmental GRNs remains insufficiently extensive, and it is not trivial to locate useful examples, which require comparison within a monophyletic clade at just sufficient distance so that the diverged morphology is clearly the output of homologous networks of developmental regulatory gene interactions.In recent years, largely complete developmental GRN models have been solved that causally explain spatial specification in large domains of the embryo of the sea urchin Strongylocentrotus purpuratus (Sp), up to gastrulation (3-5). The explanatory power of these networks was demonstrated, in these pages, by a predictive computational analysis that showed that they contain sufficient informat...

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“…WMISH was conducted essentially after Ransick (43), with modifications. Microinjection experiments in Et were done essentially as described elsewhere for euechinoids (44).…”

Section: Methodsmentioning

confidence: 99%

Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses

Erkenbrack

Davidson

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Microinjections were carried out by the methods established by McMahon et al [19] and Arnone et al [20].…”

Section: Methods and Materials Embryo Culture Micromere Culture Andmentioning

confidence: 99%

The dynamics of secretion during sea urchin embryonic skeleton formation

Wilt

Killian

Hamilton

et al. 2008

Experimental Cell Research

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Skeleton formation involves secretion of massive amounts of mineral precursor, usually a calcium salt, and matrix proteins, many of which are deposited on, or even occluded within, the mineral. The cell biological underpinnings of this secretion and subsequent assembly of the biomineralized skeletal element is not well understood. We ask here what is the relationship of the trafficking and secretion of the mineral and matrix within the primary mesenchyme cells of the sea urchin embryo, cells that deposit the endoskeletal spicule. Fluorescent labeling of intracellular calcium deposits show mineral precursors are present in granules visible by light microscopy, from whence they are deposited in the endoskeletal spicule, especially at its tip. In contrast, two different matrix proteins tagged with GFP are present in smaller post-Golgi vesicles only seen by electron microscopy, and the secreted protein are only incorporated into the spicule in the vicinity of the cell of origin. The matrix protein, SpSM30B, is post-translationally modified during secretion, and this processing continues after its incorporation into the spicule. Our findings also indicate that the mineral precursor and two well characterized matrix proteins are trafficked by different cellular routes.

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“…The procedure was essentially that of McMahon et al (1985) and Colin (1986), using modifications worked out by A. Colin, unpubl. Unfertilized eggs were collected after injection of 0.5 M KC1 into adult L. pictus and kept in Millipore-filtered seawater at 4°C.…”

Section: Microinjeciton Of Sea Urchin One-cell Zygotesmentioning

confidence: 99%

Both basal and ontogenic promoter elements affect the timing and level of expression of a sea urchin H1 gene during early embryogenesis.

Lai¹,

Maxson²,

Childs³

1988

Genes Dev.

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Late histone H1-B mRNA accumulates with the correct ontogenic pattern following microinjection of the cloned gene into fertilized sea urchin eggs. Sequences upstream of the gene encoding the sea urchin H1-B protein contain both basal and developmentally regulated elements. One late HI-specific activator sequence (USE IV) is required for the accumulation of mRNA following the blastula stage of development. All late H1 genes also contain a highly conserved GC-rich sequence resembling a low-affinity binding site for the mammalian transcription factor Spl that is required for basal expression of the H1-B gene at all stages of embryogenesis. When this GC-rich sequence (GGGCTG) is converted to a perfect core Spl sequence (GGGCGG), the H1-B transcripts accumulate to much greater levels and their peak accumulation is shifted to the early blastula stage rather than late blastula and gastrula stages of development. Coincidently, early HI genes, whose peak expression is also at the early blastula stage, all contain the same core consensus sequence (GGGCGG). Thus, both gene-specific activator sequences, as well as sequences that resemble sites for general transcription factors, may play a major role in determining the temporal patterns of gene expression during early embryogenesis.

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Introduction of cloned DNA into sea urchin egg cytoplasm: Replication and persistence during embryogenesis

Cited by 222 publications

References 38 publications

Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses

Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses

The dynamics of secretion during sea urchin embryonic skeleton formation

Both basal and ontogenic promoter elements affect the timing and level of expression of a sea urchin H1 gene during early embryogenesis.

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