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Global expression profiling reveals genetic programs underlying the developmental divergence between mouse and human embryogenesis.

Xue L, Cai JY, Ma J, Huang Z, Guo MX, Fu LZ, Shi YB, Li WX - BMC Genomics (2013)

Bottom Line: On the other hand, little information is known about the gene regulatory networks governing the subsequent organogenesis.Our studies have revealed distinct temporal regulation patterns for genes belonging to different functional (Gene Ontology or GO) categories that support their roles during organogenesis.In addition, our study might be useful for invesgtigating the molecular basis of vertebrate evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: College of Life Sciences, Wuhan University, Wuhan 430072, P,R China. shi@helix.nih.gov.

ABSTRACT

Background: Mouse has served as an excellent model for studying human development and diseases due to its similarity to human. Advances in transgenic and knockout studies in mouse have dramatically strengthened the use of this model and significantly improved our understanding of gene function during development in the past few decades. More recently, global gene expression analyses have revealed novel features in early embryogenesis up to gastrulation stages and have indeed provided molecular evidence supporting the conservation in early development in human and mouse. On the other hand, little information is known about the gene regulatory networks governing the subsequent organogenesis. Importantly, mouse and human development diverges during organogenesis. For instance, the mouse embryo is born around the end of organogenesis while in human the subsequent fetal period of ongoing growth and maturation of most organs spans more than 2/3 of human embryogenesis. While two recent studies reported the gene expression profiles during human organogenesis, no global gene expression analysis had been done for mouse organogenesis.

Results: Here we report a detailed analysis of the global gene expression profiles from egg to the end of organogenesis in mouse. Our studies have revealed distinct temporal regulation patterns for genes belonging to different functional (Gene Ontology or GO) categories that support their roles during organogenesis. More importantly, comparative analyses identify both conserved and divergent gene regulation programs in mouse and human organogenesis, with the latter likely responsible for the developmental divergence between the two species, and further suggest a novel developmental strategy during vertebrate evolution.

Conclusions: We have reported here the first genome-wide gene expression analysis of the entire mouse embryogenesis and compared the transcriptome atlas during mouse and human embryogenesis. Given our earlier observation that genes function in a given process tends to be developmentally co-regulated during organogenesis, our microarray data here should help to identify genes associated with mouse development and/or infer the developmental functions of unknown genes. In addition, our study might be useful for invesgtigating the molecular basis of vertebrate evolution.

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Early embryogenesis involves many more regulated genes than late organogenesis during mouse development. The gene expression levels were compared between each pair of adjacent developmental stages to identify developmentally regulated genes. The total number of the genes regulated between the two stages (p < 0.01) were shown as a horizontal column (open and purple shaded columns). The number of genes whose expression levels were changed only between the two indicated stages, thus termed unique regulated genes, was shown as the purple shaded portion of the columns and its percentage in the total regulated genes was shown next to the column. Some enriched function categories (Gene Ontology or GO) for each group of uniquely regulated genes are shown on the right.
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Figure 2: Early embryogenesis involves many more regulated genes than late organogenesis during mouse development. The gene expression levels were compared between each pair of adjacent developmental stages to identify developmentally regulated genes. The total number of the genes regulated between the two stages (p < 0.01) were shown as a horizontal column (open and purple shaded columns). The number of genes whose expression levels were changed only between the two indicated stages, thus termed unique regulated genes, was shown as the purple shaded portion of the columns and its percentage in the total regulated genes was shown next to the column. Some enriched function categories (Gene Ontology or GO) for each group of uniquely regulated genes are shown on the right.

Mentions: The goal of our study is to determine 1) whether and how transcriptome differs among different stages of mouse embryogenesis, and 2) how the changes in transcriptome correlate with the embryogenesis. To address these questions, we compared the expression profiles between adjacent stages during development. We observed that the extent of the changes in transcriptome, i.e., the number of genes that exhibited differential expression levels between two adjacent stages during mouse embryogenesis, correlated well with gross morphological changes of the embryo (Figure 2), that is, the more different the morphologies between two adjacent stages, the larger the number of genes whose expression was altered (Figure 2). For example, when embryos at the preimplanting zygote stage (TS01) developed into early gastrula stage (TS09), the individual zygotes or single cell fertilized eggs changed dramatically through zygotic division into differentiated gastrula embryos with three germinal layers [29]. Such drastic changes in morphology were accompanied by the largest number (about 13,000) of genes with different expression levels (Figure 2). A similar large number (about 10,000) of genes with altered expression levels were detected between TS16 and TS19 when both stages are at the early stages of organogenesis and the mouse embryo grew and changed rapidly as the somites formed during early organogenesis (Figure 2). In contrast, there were relatively few genes with significantly altered expression between unfertilized eggs and TS01 or between TS19 and TS21, when the gross morphology change was relatively minor (Figure 2). These results suggest that the extent of the morphological changes is well correlated with the number of genes whose expression is altered.


Global expression profiling reveals genetic programs underlying the developmental divergence between mouse and human embryogenesis.

Xue L, Cai JY, Ma J, Huang Z, Guo MX, Fu LZ, Shi YB, Li WX - BMC Genomics (2013)

Early embryogenesis involves many more regulated genes than late organogenesis during mouse development. The gene expression levels were compared between each pair of adjacent developmental stages to identify developmentally regulated genes. The total number of the genes regulated between the two stages (p < 0.01) were shown as a horizontal column (open and purple shaded columns). The number of genes whose expression levels were changed only between the two indicated stages, thus termed unique regulated genes, was shown as the purple shaded portion of the columns and its percentage in the total regulated genes was shown next to the column. Some enriched function categories (Gene Ontology or GO) for each group of uniquely regulated genes are shown on the right.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3924405&req=5

Figure 2: Early embryogenesis involves many more regulated genes than late organogenesis during mouse development. The gene expression levels were compared between each pair of adjacent developmental stages to identify developmentally regulated genes. The total number of the genes regulated between the two stages (p < 0.01) were shown as a horizontal column (open and purple shaded columns). The number of genes whose expression levels were changed only between the two indicated stages, thus termed unique regulated genes, was shown as the purple shaded portion of the columns and its percentage in the total regulated genes was shown next to the column. Some enriched function categories (Gene Ontology or GO) for each group of uniquely regulated genes are shown on the right.
Mentions: The goal of our study is to determine 1) whether and how transcriptome differs among different stages of mouse embryogenesis, and 2) how the changes in transcriptome correlate with the embryogenesis. To address these questions, we compared the expression profiles between adjacent stages during development. We observed that the extent of the changes in transcriptome, i.e., the number of genes that exhibited differential expression levels between two adjacent stages during mouse embryogenesis, correlated well with gross morphological changes of the embryo (Figure 2), that is, the more different the morphologies between two adjacent stages, the larger the number of genes whose expression was altered (Figure 2). For example, when embryos at the preimplanting zygote stage (TS01) developed into early gastrula stage (TS09), the individual zygotes or single cell fertilized eggs changed dramatically through zygotic division into differentiated gastrula embryos with three germinal layers [29]. Such drastic changes in morphology were accompanied by the largest number (about 13,000) of genes with different expression levels (Figure 2). A similar large number (about 10,000) of genes with altered expression levels were detected between TS16 and TS19 when both stages are at the early stages of organogenesis and the mouse embryo grew and changed rapidly as the somites formed during early organogenesis (Figure 2). In contrast, there were relatively few genes with significantly altered expression between unfertilized eggs and TS01 or between TS19 and TS21, when the gross morphology change was relatively minor (Figure 2). These results suggest that the extent of the morphological changes is well correlated with the number of genes whose expression is altered.

Bottom Line: On the other hand, little information is known about the gene regulatory networks governing the subsequent organogenesis.Our studies have revealed distinct temporal regulation patterns for genes belonging to different functional (Gene Ontology or GO) categories that support their roles during organogenesis.In addition, our study might be useful for invesgtigating the molecular basis of vertebrate evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: College of Life Sciences, Wuhan University, Wuhan 430072, P,R China. shi@helix.nih.gov.

ABSTRACT

Background: Mouse has served as an excellent model for studying human development and diseases due to its similarity to human. Advances in transgenic and knockout studies in mouse have dramatically strengthened the use of this model and significantly improved our understanding of gene function during development in the past few decades. More recently, global gene expression analyses have revealed novel features in early embryogenesis up to gastrulation stages and have indeed provided molecular evidence supporting the conservation in early development in human and mouse. On the other hand, little information is known about the gene regulatory networks governing the subsequent organogenesis. Importantly, mouse and human development diverges during organogenesis. For instance, the mouse embryo is born around the end of organogenesis while in human the subsequent fetal period of ongoing growth and maturation of most organs spans more than 2/3 of human embryogenesis. While two recent studies reported the gene expression profiles during human organogenesis, no global gene expression analysis had been done for mouse organogenesis.

Results: Here we report a detailed analysis of the global gene expression profiles from egg to the end of organogenesis in mouse. Our studies have revealed distinct temporal regulation patterns for genes belonging to different functional (Gene Ontology or GO) categories that support their roles during organogenesis. More importantly, comparative analyses identify both conserved and divergent gene regulation programs in mouse and human organogenesis, with the latter likely responsible for the developmental divergence between the two species, and further suggest a novel developmental strategy during vertebrate evolution.

Conclusions: We have reported here the first genome-wide gene expression analysis of the entire mouse embryogenesis and compared the transcriptome atlas during mouse and human embryogenesis. Given our earlier observation that genes function in a given process tends to be developmentally co-regulated during organogenesis, our microarray data here should help to identify genes associated with mouse development and/or infer the developmental functions of unknown genes. In addition, our study might be useful for invesgtigating the molecular basis of vertebrate evolution.

Show MeSH
Related in: MedlinePlus