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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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Morphological comparisons of mouse and human embryo development. Mouse embryonic stages (Theiler stages or TS) are based on somite number and characteristics [26]. There are 28 TS stages from the fertilization to birth, which is about 20 days post conception (dpc). Only 11 stages are shown. Human embryo stages were described by the Carnegie Institution of Washington, which are based on the developmental structures, not by size or the number of days of development [27]. The 23 Carnegie stages (CS) only covers the first 60 days of human embryo development, thereafter that the term embryo is replaced with fetus. 5 human embryos at 4-9th week are shown here. The double headed arrows point to human and mouse embryos at similar stages of organogenesis.
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Figure 1: Morphological comparisons of mouse and human embryo development. Mouse embryonic stages (Theiler stages or TS) are based on somite number and characteristics [26]. There are 28 TS stages from the fertilization to birth, which is about 20 days post conception (dpc). Only 11 stages are shown. Human embryo stages were described by the Carnegie Institution of Washington, which are based on the developmental structures, not by size or the number of days of development [27]. The 23 Carnegie stages (CS) only covers the first 60 days of human embryo development, thereafter that the term embryo is replaced with fetus. 5 human embryos at 4-9th week are shown here. The double headed arrows point to human and mouse embryos at similar stages of organogenesis.

Mentions: The advent of microarray analysis has allowed systematic analysis of gene expression changes during development. Elucidating the transcriptomes of successive developmental stages in different animal species is critical for understanding the developmental mechanism and revealing the conservation and diversification at molecular level among species during embryogenesis. A number of reports on genome-wide expression profiles for different developmental periods during human and mouse embryogenesis have been published, which have provided valuable information on the gene and the molecular network underlining morphological changes during these periods [4-24] These earlier studies so far focused mainly on oocytes and preimplantation embryos in mouse and revealed a number of similarities between mouse and human gene expression profiles. This perhaps was not surprising given the similarities between the two species at early stages of development (Figure 1, Additional file 1A). On the other hand, the arguably more critical period of embryogenesis is the period of organogenesis, when most significant morphological differences occur between human and mouse (Figure 1) [25]. One of the most obvious differences between mouse and human embryogenesis is the time of birth. The mouse embryo is born almost immediately after all the organs develop (around TS27-TS28, 19–20 days post conception, Figure 1). On the other hand, at the end of organogenesis (CS23, corresponding to TS26/27, Figure 1), the human embryo has a disproportionally large head relative to the whole body and other organs. The embryo continues to stay in the uterus for a few more months, a period termed as the fetal stage. During this stage, many organs continue to grow and eventually develop into their proper sizes for birth. The underlying molecular basis for this developmental divergence remains unknown as there have been essentially no global gene expression data available for mammalian embryos past the peri-implantation period. Interestingly, two recent studies on the global gene expression profiles during human organogenesis (up to 9 weeks of human gestation) revealed very interesting and informative information on the gene regulation networks governing organogenesis, distinct from those involved in early embryogenesis, which utilizes many maternal genes [7,18,25].


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)

Morphological comparisons of mouse and human embryo development. Mouse embryonic stages (Theiler stages or TS) are based on somite number and characteristics [26]. There are 28 TS stages from the fertilization to birth, which is about 20 days post conception (dpc). Only 11 stages are shown. Human embryo stages were described by the Carnegie Institution of Washington, which are based on the developmental structures, not by size or the number of days of development [27]. The 23 Carnegie stages (CS) only covers the first 60 days of human embryo development, thereafter that the term embryo is replaced with fetus. 5 human embryos at 4-9th week are shown here. The double headed arrows point to human and mouse embryos at similar stages of organogenesis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Morphological comparisons of mouse and human embryo development. Mouse embryonic stages (Theiler stages or TS) are based on somite number and characteristics [26]. There are 28 TS stages from the fertilization to birth, which is about 20 days post conception (dpc). Only 11 stages are shown. Human embryo stages were described by the Carnegie Institution of Washington, which are based on the developmental structures, not by size or the number of days of development [27]. The 23 Carnegie stages (CS) only covers the first 60 days of human embryo development, thereafter that the term embryo is replaced with fetus. 5 human embryos at 4-9th week are shown here. The double headed arrows point to human and mouse embryos at similar stages of organogenesis.
Mentions: The advent of microarray analysis has allowed systematic analysis of gene expression changes during development. Elucidating the transcriptomes of successive developmental stages in different animal species is critical for understanding the developmental mechanism and revealing the conservation and diversification at molecular level among species during embryogenesis. A number of reports on genome-wide expression profiles for different developmental periods during human and mouse embryogenesis have been published, which have provided valuable information on the gene and the molecular network underlining morphological changes during these periods [4-24] These earlier studies so far focused mainly on oocytes and preimplantation embryos in mouse and revealed a number of similarities between mouse and human gene expression profiles. This perhaps was not surprising given the similarities between the two species at early stages of development (Figure 1, Additional file 1A). On the other hand, the arguably more critical period of embryogenesis is the period of organogenesis, when most significant morphological differences occur between human and mouse (Figure 1) [25]. One of the most obvious differences between mouse and human embryogenesis is the time of birth. The mouse embryo is born almost immediately after all the organs develop (around TS27-TS28, 19–20 days post conception, Figure 1). On the other hand, at the end of organogenesis (CS23, corresponding to TS26/27, Figure 1), the human embryo has a disproportionally large head relative to the whole body and other organs. The embryo continues to stay in the uterus for a few more months, a period termed as the fetal stage. During this stage, many organs continue to grow and eventually develop into their proper sizes for birth. The underlying molecular basis for this developmental divergence remains unknown as there have been essentially no global gene expression data available for mammalian embryos past the peri-implantation period. Interestingly, two recent studies on the global gene expression profiles during human organogenesis (up to 9 weeks of human gestation) revealed very interesting and informative information on the gene regulation networks governing organogenesis, distinct from those involved in early embryogenesis, which utilizes many maternal genes [7,18,25].

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