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Transcriptomic Responses of the Heart and Brain to Anoxia in the Western Painted Turtle.

Keenan SW, Hill CA, Kandoth C, Buck LT, Warren DE - PLoS ONE (2015)

Bottom Line: Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle.The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression).Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Saint Louis University, St. Louis, Missouri, United States of America.

ABSTRACT
Painted turtles are the most anoxia-tolerant tetrapods known, capable of surviving without oxygen for more than four months at 3°C and 30 hours at 20°C. To investigate the transcriptomic basis of this ability, we used RNA-seq to quantify mRNA expression in the painted turtle ventricle and telencephalon after 24 hours of anoxia at 19°C. Reads were obtained from 22,174 different genes, 13,236 of which were compared statistically between treatments for each tissue. Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle. The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression). When treatment effects were compared between anoxic and normoxic conditions in the two tissue types, 31 genes were increased (≥ 2x change) and 2 were decreased (≤ 0.5x change). Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest. No genes related to ion channels, synaptic transmission, cardiac contractility or excitation-contraction coupling changed. The generalized expression pattern in telencephalon and across tissues, but not in ventricle, correlated with the predicted metabolic cost of transcription, with the shortest genes and those with the fewest exons showing the largest increases in expression.

No MeSH data available.


Related in: MedlinePlus

Mean ± SEM FPKM values measured for differentially expressed genes.(A) Values in normoxic and anoxic telencephalon, (B) normoxic and anoxic ventricle and (C) all normoxic and anoxic tissue combined. Genes with green font indicate increases in expression resulting from anoxia. Genes with red font indicate decreases in expression resulting from anoxia. In each plate, genes are arranged in order of decreasing fold expression. Only genes that changed by ≥ 2.0 fold or ≤ 0.5-fold were included. Several genes were abbreviated for simplicity: “PPBP,PF4,CXCL” includes Ppbp/Pf4/Cxcl1/Pf4v1/ Cxcl6/ Cxcl3/ Cxcl5/ Cxcl2/ Il8/ Cxcl10/ Cxc11; “CLK,PPIL3” includes Clk3/Ppil3/Clk1/Clk4). The mean FPKM values, P-values, sequence length, and exon density for each of these genes can be found in S1–S3 Tables.
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pone.0131669.g004: Mean ± SEM FPKM values measured for differentially expressed genes.(A) Values in normoxic and anoxic telencephalon, (B) normoxic and anoxic ventricle and (C) all normoxic and anoxic tissue combined. Genes with green font indicate increases in expression resulting from anoxia. Genes with red font indicate decreases in expression resulting from anoxia. In each plate, genes are arranged in order of decreasing fold expression. Only genes that changed by ≥ 2.0 fold or ≤ 0.5-fold were included. Several genes were abbreviated for simplicity: “PPBP,PF4,CXCL” includes Ppbp/Pf4/Cxcl1/Pf4v1/ Cxcl6/ Cxcl3/ Cxcl5/ Cxcl2/ Il8/ Cxcl10/ Cxc11; “CLK,PPIL3” includes Clk3/Ppil3/Clk1/Clk4). The mean FPKM values, P-values, sequence length, and exon density for each of these genes can be found in S1–S3 Tables.

Mentions: Anoxic submergence decreased total tissue RNA content by 16% and 53% in telencephalon and ventricle, respectively (Fig 1). The reads from RNA-seq aligned to 22,174 human gene orthologs predicted from the OPTICS annotation file. After filtering genes such that only those where at least three of the four samples from each sampling group had FPKM values more than zero, 13,236 genes were compared statistically (Figs 2 and 3). In the telencephalon (Fig 4A) the expression of 19 genes increased (≥ 2x change), while no genes decreased (≤ 0.5x change). In the ventricle (Fig 4B), expression of 23 genes increased, while 4 decreased. The fold changes in tissue-specific gene expression have been published previously as supplemental material [23].


Transcriptomic Responses of the Heart and Brain to Anoxia in the Western Painted Turtle.

Keenan SW, Hill CA, Kandoth C, Buck LT, Warren DE - PLoS ONE (2015)

Mean ± SEM FPKM values measured for differentially expressed genes.(A) Values in normoxic and anoxic telencephalon, (B) normoxic and anoxic ventricle and (C) all normoxic and anoxic tissue combined. Genes with green font indicate increases in expression resulting from anoxia. Genes with red font indicate decreases in expression resulting from anoxia. In each plate, genes are arranged in order of decreasing fold expression. Only genes that changed by ≥ 2.0 fold or ≤ 0.5-fold were included. Several genes were abbreviated for simplicity: “PPBP,PF4,CXCL” includes Ppbp/Pf4/Cxcl1/Pf4v1/ Cxcl6/ Cxcl3/ Cxcl5/ Cxcl2/ Il8/ Cxcl10/ Cxc11; “CLK,PPIL3” includes Clk3/Ppil3/Clk1/Clk4). The mean FPKM values, P-values, sequence length, and exon density for each of these genes can be found in S1–S3 Tables.
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pone.0131669.g004: Mean ± SEM FPKM values measured for differentially expressed genes.(A) Values in normoxic and anoxic telencephalon, (B) normoxic and anoxic ventricle and (C) all normoxic and anoxic tissue combined. Genes with green font indicate increases in expression resulting from anoxia. Genes with red font indicate decreases in expression resulting from anoxia. In each plate, genes are arranged in order of decreasing fold expression. Only genes that changed by ≥ 2.0 fold or ≤ 0.5-fold were included. Several genes were abbreviated for simplicity: “PPBP,PF4,CXCL” includes Ppbp/Pf4/Cxcl1/Pf4v1/ Cxcl6/ Cxcl3/ Cxcl5/ Cxcl2/ Il8/ Cxcl10/ Cxc11; “CLK,PPIL3” includes Clk3/Ppil3/Clk1/Clk4). The mean FPKM values, P-values, sequence length, and exon density for each of these genes can be found in S1–S3 Tables.
Mentions: Anoxic submergence decreased total tissue RNA content by 16% and 53% in telencephalon and ventricle, respectively (Fig 1). The reads from RNA-seq aligned to 22,174 human gene orthologs predicted from the OPTICS annotation file. After filtering genes such that only those where at least three of the four samples from each sampling group had FPKM values more than zero, 13,236 genes were compared statistically (Figs 2 and 3). In the telencephalon (Fig 4A) the expression of 19 genes increased (≥ 2x change), while no genes decreased (≤ 0.5x change). In the ventricle (Fig 4B), expression of 23 genes increased, while 4 decreased. The fold changes in tissue-specific gene expression have been published previously as supplemental material [23].

Bottom Line: Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle.The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression).Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Saint Louis University, St. Louis, Missouri, United States of America.

ABSTRACT
Painted turtles are the most anoxia-tolerant tetrapods known, capable of surviving without oxygen for more than four months at 3°C and 30 hours at 20°C. To investigate the transcriptomic basis of this ability, we used RNA-seq to quantify mRNA expression in the painted turtle ventricle and telencephalon after 24 hours of anoxia at 19°C. Reads were obtained from 22,174 different genes, 13,236 of which were compared statistically between treatments for each tissue. Total tissue RNA contents decreased by 16% in telencephalon and 53% in ventricle. The telencephalon and ventricle showed ≥ 2x expression (increased expression) in 19 and 23 genes, respectively, while only four genes in ventricle showed ≤ 0.5x changes (decreased expression). When treatment effects were compared between anoxic and normoxic conditions in the two tissue types, 31 genes were increased (≥ 2x change) and 2 were decreased (≤ 0.5x change). Most of the effected genes were immediate early genes and transcription factors that regulate cellular growth and development; changes that would seem to promote transcriptional, translational, and metabolic arrest. No genes related to ion channels, synaptic transmission, cardiac contractility or excitation-contraction coupling changed. The generalized expression pattern in telencephalon and across tissues, but not in ventricle, correlated with the predicted metabolic cost of transcription, with the shortest genes and those with the fewest exons showing the largest increases in expression.

No MeSH data available.


Related in: MedlinePlus