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A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi
BACKGROUND: An important question in experimental embryology is to understand how the developmental potential responsible for the generation of distinct cell types is spatially segregated over developmental time. Classical embryological work showed that ctenophores, a group of gelatinous marine inve...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3909359/ https://www.ncbi.nlm.nih.gov/pubmed/24485336 http://dx.doi.org/10.1186/2041-9139-5-4 |
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author | Fischer, Antje HL Pang, Kevin Henry, Jonathan Q Martindale, Mark Q |
author_facet | Fischer, Antje HL Pang, Kevin Henry, Jonathan Q Martindale, Mark Q |
author_sort | Fischer, Antje HL |
collection | PubMed |
description | BACKGROUND: An important question in experimental embryology is to understand how the developmental potential responsible for the generation of distinct cell types is spatially segregated over developmental time. Classical embryological work showed that ctenophores, a group of gelatinous marine invertebrates that arose early in animal evolution, display a highly stereotyped pattern of early development and a precocious specification of blastomere fates. Here we investigate the role of autonomous cell specification and the developmental timing of two distinct ctenophore cell types (motile compound comb-plate-like cilia and light-emitting photocytes) in embryos of the lobate ctenophore, Mnemiopsis leidyi. RESULTS: In Mnemiopsis, 9 h after fertilization, comb plate cilia differentiate into derivatives of the E lineage, while the bioluminescent capability begins in derivatives of the M lineage. Arresting cleavage with cytochalasin B at the 1-, 2- or 4-cell stage does not result in blastomere death; however, no visible differentiation of the comb-plate-like cilia or bioluminescence was observed. Cleavage arrest at the 8- or 16-cell stage, in contrast, results in the expression of both differentiation products. Fate-mapping experiments indicate that only the lineages of cells that normally express these markers in an autonomous fashion during normal development express these traits in cleavage-arrested 8- and 16-cell stage embryos. Lineages that form comb plates in a non-autonomous fashion (derivatives of the M lineage) do not. Timed actinomycin D and puromycin treatments show that transcription and translation are required for comb formation and suggest that the segregated material might be necessary for activation of the appropriate genes. Interestingly, even in the absence of cytokinesis, differentiation markers appear to be activated at the correct times. Treatments with a DNA synthesis inhibitor, aphidicolin, show that the number of nuclear divisions, and perhaps the DNA to cytoplasmic ratio, are critical for the appearance of lineage-specific differentiation. CONCLUSION: Our work corroborates previous studies demonstrating that the cleavage program is causally involved in the spatial segregation and/or activation of factors that give rise to distinct cell types in ctenophore development. These factors are segregated independently to the appropriate lineage at the 8- and the 16-cell stages and have features of a clock, such that comb-plate-like cilia and light-emitting photoproteins appear at roughly the same developmental time in cleavage-arrested embryos as they do in untreated embryos. Nuclear division, which possibly affects DNA-cytoplasmic ratios, appears to be important in the timing of differentiation markers. Evidence suggests that the 60-cell stage, just prior to gastrulation, is the time of zygotic gene activation. Such cleavage-clock-regulated phenomena appear to be widespread amongst the Metazoa and these cellular and molecular developmental mechanisms probably evolved early in metazoan evolution. |
format | Online Article Text |
id | pubmed-3909359 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-39093592014-02-02 A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi Fischer, Antje HL Pang, Kevin Henry, Jonathan Q Martindale, Mark Q EvoDevo Research BACKGROUND: An important question in experimental embryology is to understand how the developmental potential responsible for the generation of distinct cell types is spatially segregated over developmental time. Classical embryological work showed that ctenophores, a group of gelatinous marine invertebrates that arose early in animal evolution, display a highly stereotyped pattern of early development and a precocious specification of blastomere fates. Here we investigate the role of autonomous cell specification and the developmental timing of two distinct ctenophore cell types (motile compound comb-plate-like cilia and light-emitting photocytes) in embryos of the lobate ctenophore, Mnemiopsis leidyi. RESULTS: In Mnemiopsis, 9 h after fertilization, comb plate cilia differentiate into derivatives of the E lineage, while the bioluminescent capability begins in derivatives of the M lineage. Arresting cleavage with cytochalasin B at the 1-, 2- or 4-cell stage does not result in blastomere death; however, no visible differentiation of the comb-plate-like cilia or bioluminescence was observed. Cleavage arrest at the 8- or 16-cell stage, in contrast, results in the expression of both differentiation products. Fate-mapping experiments indicate that only the lineages of cells that normally express these markers in an autonomous fashion during normal development express these traits in cleavage-arrested 8- and 16-cell stage embryos. Lineages that form comb plates in a non-autonomous fashion (derivatives of the M lineage) do not. Timed actinomycin D and puromycin treatments show that transcription and translation are required for comb formation and suggest that the segregated material might be necessary for activation of the appropriate genes. Interestingly, even in the absence of cytokinesis, differentiation markers appear to be activated at the correct times. Treatments with a DNA synthesis inhibitor, aphidicolin, show that the number of nuclear divisions, and perhaps the DNA to cytoplasmic ratio, are critical for the appearance of lineage-specific differentiation. CONCLUSION: Our work corroborates previous studies demonstrating that the cleavage program is causally involved in the spatial segregation and/or activation of factors that give rise to distinct cell types in ctenophore development. These factors are segregated independently to the appropriate lineage at the 8- and the 16-cell stages and have features of a clock, such that comb-plate-like cilia and light-emitting photoproteins appear at roughly the same developmental time in cleavage-arrested embryos as they do in untreated embryos. Nuclear division, which possibly affects DNA-cytoplasmic ratios, appears to be important in the timing of differentiation markers. Evidence suggests that the 60-cell stage, just prior to gastrulation, is the time of zygotic gene activation. Such cleavage-clock-regulated phenomena appear to be widespread amongst the Metazoa and these cellular and molecular developmental mechanisms probably evolved early in metazoan evolution. BioMed Central 2014-01-31 /pmc/articles/PMC3909359/ /pubmed/24485336 http://dx.doi.org/10.1186/2041-9139-5-4 Text en Copyright © 2013 Fischer et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Fischer, Antje HL Pang, Kevin Henry, Jonathan Q Martindale, Mark Q A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title | A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title_full | A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title_fullStr | A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title_full_unstemmed | A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title_short | A cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore Mnemiopsis leidyi |
title_sort | cleavage clock regulates features of lineage-specific differentiation in the development of a basal branching metazoan, the ctenophore mnemiopsis leidyi |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3909359/ https://www.ncbi.nlm.nih.gov/pubmed/24485336 http://dx.doi.org/10.1186/2041-9139-5-4 |
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