Limits...
A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis

View Article: PubMed Central - PubMed

ABSTRACT

Background: The ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.

Results: In order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.

Conclusions: This work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

No MeSH data available.


Clustering analyses of the oral and physal time course. a. Gene-wise hierarchical clustering of the differentially expressed (DE) genes. The yellow rectangle highlights genes being largely upregulated during regeneration. The blue rectangle highlights genes largely being downregulated during regeneration. The color scale indicates z-scored expression values b. A dendrogram of sample-wise hierarchical clustering of the samples from the different regeneration-sides and time points. c. The six largest clusters of gene expression in oral and physal regeneration. Clusters are ordered by the number of genes in each cluster which is indicated in the bottom left corner. The number in the top left corner indicates the STEM cluster number. The full list of clusters can be found in Additional file 2: Figure S1 and a list of the genes and which cluster they belong to can be found in Additional file 3: Table S2
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC5015328&req=5

Fig2: Clustering analyses of the oral and physal time course. a. Gene-wise hierarchical clustering of the differentially expressed (DE) genes. The yellow rectangle highlights genes being largely upregulated during regeneration. The blue rectangle highlights genes largely being downregulated during regeneration. The color scale indicates z-scored expression values b. A dendrogram of sample-wise hierarchical clustering of the samples from the different regeneration-sides and time points. c. The six largest clusters of gene expression in oral and physal regeneration. Clusters are ordered by the number of genes in each cluster which is indicated in the bottom left corner. The number in the top left corner indicates the STEM cluster number. The full list of clusters can be found in Additional file 2: Figure S1 and a list of the genes and which cluster they belong to can be found in Additional file 3: Table S2

Mentions: We first examined the global nature of the gene response pattern in the oral and aboral regenerating parts. A hierarchical clustering analysis of all the DE genes indicated that more genes (about 60 %) were downregulated following dissection compared to the upregulated genes (Fig. 2a). Within the two groups many blocks of variation in one or more time point were evident, indicating temporal-, and tissue-specific differential gene expression. Similarly, sample-wise hierarchical clustering according to the temporal and spatial variables (Fig. 2b) indicates that gene expression patterns of the two tissues were largely shared at each time point, and that the different time points exhibited more distinct expression patterns from each other. As expected, the expression profiles of the two cut ends at time 0 were the most similar to each other and differed from all the ensuing regeneration time points. It was also evident that the 24 and 72 h expression profiles are more similar to each other than they are to 8 h (Fig. 2b), which is in line with previous studies defining the first 6–8 h as a distinct wound-healing stage [53, 57]. The similarity in the overall expression patterns of the two regions of regeneration, at each individual time point, suggests that a large part of the regeneration response is of a general nature which may govern general wound healing and tissue growth at large, and that side-specific differential expression patterns may be more limited. Interestingly though, the oral and physal 72 h samples were more diverse than in the other time points as reflected in their branch lengths (Fig. 2b), which may indicate that at 72 h there is an enriched expression of genes responsible for oral or aboral specific tissue traits compared to a more general earlier wound healing and initial regenerative response.Fig. 2


A transcriptional time-course analysis of oral vs. aboral whole-body regeneration in the Sea anemone Nematostella vectensis
Clustering analyses of the oral and physal time course. a. Gene-wise hierarchical clustering of the differentially expressed (DE) genes. The yellow rectangle highlights genes being largely upregulated during regeneration. The blue rectangle highlights genes largely being downregulated during regeneration. The color scale indicates z-scored expression values b. A dendrogram of sample-wise hierarchical clustering of the samples from the different regeneration-sides and time points. c. The six largest clusters of gene expression in oral and physal regeneration. Clusters are ordered by the number of genes in each cluster which is indicated in the bottom left corner. The number in the top left corner indicates the STEM cluster number. The full list of clusters can be found in Additional file 2: Figure S1 and a list of the genes and which cluster they belong to can be found in Additional file 3: Table S2
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5015328&req=5

Fig2: Clustering analyses of the oral and physal time course. a. Gene-wise hierarchical clustering of the differentially expressed (DE) genes. The yellow rectangle highlights genes being largely upregulated during regeneration. The blue rectangle highlights genes largely being downregulated during regeneration. The color scale indicates z-scored expression values b. A dendrogram of sample-wise hierarchical clustering of the samples from the different regeneration-sides and time points. c. The six largest clusters of gene expression in oral and physal regeneration. Clusters are ordered by the number of genes in each cluster which is indicated in the bottom left corner. The number in the top left corner indicates the STEM cluster number. The full list of clusters can be found in Additional file 2: Figure S1 and a list of the genes and which cluster they belong to can be found in Additional file 3: Table S2
Mentions: We first examined the global nature of the gene response pattern in the oral and aboral regenerating parts. A hierarchical clustering analysis of all the DE genes indicated that more genes (about 60 %) were downregulated following dissection compared to the upregulated genes (Fig. 2a). Within the two groups many blocks of variation in one or more time point were evident, indicating temporal-, and tissue-specific differential gene expression. Similarly, sample-wise hierarchical clustering according to the temporal and spatial variables (Fig. 2b) indicates that gene expression patterns of the two tissues were largely shared at each time point, and that the different time points exhibited more distinct expression patterns from each other. As expected, the expression profiles of the two cut ends at time 0 were the most similar to each other and differed from all the ensuing regeneration time points. It was also evident that the 24 and 72 h expression profiles are more similar to each other than they are to 8 h (Fig. 2b), which is in line with previous studies defining the first 6–8 h as a distinct wound-healing stage [53, 57]. The similarity in the overall expression patterns of the two regions of regeneration, at each individual time point, suggests that a large part of the regeneration response is of a general nature which may govern general wound healing and tissue growth at large, and that side-specific differential expression patterns may be more limited. Interestingly though, the oral and physal 72 h samples were more diverse than in the other time points as reflected in their branch lengths (Fig. 2b), which may indicate that at 72 h there is an enriched expression of genes responsible for oral or aboral specific tissue traits compared to a more general earlier wound healing and initial regenerative response.Fig. 2

View Article: PubMed Central - PubMed

ABSTRACT

Background: The ability of regeneration is essential for the homeostasis of all animals as it allows the repair and renewal of tissues and body parts upon normal turnover or injury. The extent of this ability varies greatly in different animals with the sea anemone Nematostella vectensis, a basal cnidarian model animal, displaying remarkable whole-body regeneration competence.

Results: In order to study this process in Nematostella we performed an RNA-Seq screen wherein we analyzed and compared the transcriptional response to bisection in the wound-proximal body parts undergoing oral (head) or aboral (tail) regeneration at several time points up to the initial restoration of the basic body shape. The transcriptional profiles of regeneration responsive genes were analyzed so as to define the temporal pattern of differential gene expression associated with the tissue-specific oral and aboral regeneration. The identified genes were characterized according to their GO (gene ontology) assignations revealing groups that were enriched in the regeneration process with particular attention to their affiliation to the major developmental signaling pathways. While some of the genes and gene groups thus analyzed were previously known to be active in regeneration, we have also revealed novel and surprising candidate genes such as cilia-associated genes that likely participate in this important developmental program.

Conclusions: This work highlighted the main groups of genes which showed polarization upon regeneration, notably the proteinases, multiple transcription factors and the Wnt pathway genes that were highly represented, all displaying an intricate temporal balance between the two sides. In addition, the evolutionary comparison performed between regeneration in different animal model systems may reveal the basic mechanisms playing a role in this fascinating process.

Electronic supplementary material: The online version of this article (doi:10.1186/s12864-016-3027-1) contains supplementary material, which is available to authorized users.

No MeSH data available.