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.2012 Jul 9:12:112.
doi: 10.1186/1471-2148-12-112.

Tissue-specific differential induction of duplicated fatty acid-binding protein genes by the peroxisome proliferator, clofibrate, in zebrafish (Danio rerio)

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Tissue-specific differential induction of duplicated fatty acid-binding protein genes by the peroxisome proliferator, clofibrate, in zebrafish (Danio rerio)

Ananda B Venkatachalam et al. BMC Evol Biol..

Abstract

Background: Force, Lynch and Conery proposed the duplication-degeneration-complementation (DDC) model in which partitioning of ancestral functions (subfunctionalization) and acquisition of novel functions (neofunctionalization) were the two primary mechanisms for the retention of duplicated genes. The DDC model was tested by analyzing the transcriptional induction of the duplicated fatty acid-binding protein (fabp) genes by clofibrate in zebrafish. Clofibrate is a specific ligand of the peroxisome proliferator-activated receptor (PPAR); it activates PPAR which then binds to a peroxisome proliferator response element (PPRE) to induce the transcriptional initiation of genes primarily involved in lipid homeostasis. Zebrafish was chosen as our model organism as it has many duplicated genes owing to a whole genome duplication (WGD) event that occurred ~230-400 million years ago in the teleost fish lineage. We assayed the steady-state levels of fabp mRNA and heterogeneous nuclear RNA (hnRNA) transcripts in liver, intestine, muscle, brain and heart for four sets of duplicated fabp genes, fabp1a/fabp1b.1/fabp1b.2, fabp7a/fabp7b, fabp10a/fabp10b and fabp11a/fabp11b in zebrafish fed different concentrations of clofibrate.

Result: Electron microscopy showed an increase in the number of peroxisomes and mitochondria in liver and heart, respectively, in zebrafish fed clofibrate. Clofibrate also increased the steady-state level of acox1 mRNA and hnRNA transcripts in different tissues, a gene with a functional PPRE. These results demonstrate that zebrafish is responsive to clofibrate, unlike some other fishes. The levels of fabp mRNA and hnRNA transcripts for the four sets of duplicated fabp genes was determined by reverse transcription, quantitative polymerase chain reaction (RT-qPCR). The level of hnRNA coded by a gene is an indirect estimate of the rate of transcriptional initiation of that gene. Clofibrate increased the steady-state level of fabp mRNAs and hnRNAs for both the duplicated copies of fabp1a/fabp1b.1, and fabp7a/fabp7b, but in different tissues. Clofibrate also increased the steady-state level of fabp10a and fabp11a mRNAs and hnRNAs in liver, but not for fabp10b and fabp11b.

Conclusion: Some duplicated fabp genes have, most likely, retained PPREs, but induction by clofibrate is over-ridden by an, as yet, unknown tissue-specific mechanism(s). Regardless of the tissue-specific mechanism(s), transcriptional control of duplicated zebrafish fabp genes by clofibrate has markedly diverged since the WGD event.

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Figures

Figure 1
Figure 1
Electron micrographs of hepatocytes of zebrafish after clofibrate treatment. Staining of peroxisomes in the hepatocytes of zebrafish fed 0% clofibrate(A) and 1.00% clofibrate(B). Number of peroxisome per field of view in liver increased with increasing concentration of clofibrate fed zebrafish(C). Arrows point to peroxisomes. Bar = 2 μm.
Figure 2
Figure 2
Electron micrographs of heart cells of zebrafish after clofibrate treatment. Mitochondria in the heart cells of zebrafish fed 0% clofibrate(A) and 1.00% clofibrate(B). Number of mitochondria per field of view in heart increased with increasing concentration of clofibrate fed zebrafish(C). Bar = 2 μm.
Figure 3
Figure 3
The steady-state level of  acox1 mRNA and hnRNA in various tissues of zebrafish fed clofibrate. The level of mRNA and hnRNA of theacox1 gene in liver(A, F), intestine(B, G), muscle(C, H), heart(D, I) and brain(E, J) was determined by RT-qPCR using gene-specific primers. The steady-state level ofacox1 transcripts was normalized to the steady-state level ofrpl13α transcripts in the same sample. Data are presented as the mean ratio ± S.E.M. Significant differences (p < 0.05) in the relative steady-state level ofacox1 mRNA and hnRNA between zebrafish [n = 12, (male = 6, female = 6)] fed different concentrations of clofibrate compared to zebrafish not fed clofibrate are indicated by an asterisk.
Figure 4
Figure 4
The steady-state level of  fabp1a/fabp1b.1/fabp1b.2 mRNA and hnRNA in intestine (A, B, C, D), muscle (E, F, G, H) and heart (I, J, K, L) of zebrafish fed clofibrate. The level of mRNA and hnRNA was determined by RT-qPCR using gene-specific primers. The steady-state level offabp transcripts was normalized to the steady-state level ofrpl13α transcripts in the same sample. Data are presented as the mean ratio ± S.E.M. Significant differences (p < 0.05) in the relative steady-state level offabp mRNAs between zebrafish [n = 12, (male = 6, female = 6)] fed different concentrations of clofibrate compared to zebrafish not fed clofibrate are indicated by an asterisk.
Figure 5
Figure 5
The steady-state level of  fabp7a/fabp7b mRNA and hnRNA in liver (A, B, C), intestine (D, E, F) and muscle (G, H, I) of zebrafish fed clofibrate. The level of mRNA and hnRNA was determined by RT-qPCR using gene-specific primers. The steady-state level offabp transcripts was normalized to the steady-state level ofrpl13α transcripts in the same sample. Data are presented as the mean ratio ± S.E.M. Significant differences (p < 0.05) in the relative steady-state level offabp mRNAs between zebrafish [n = 12, (male = 6, female = 6)] fed different concentrations of clofibrate compared to zebrafish not fed clofibrate are indicated by an asterisk.
Figure 6
Figure 6
The steady-state level of  fabp10a/fabp10b mRNA and hnRNA in liver (A, B, C) and  fabp11a/fabp11b (mRNA and hnRNA) in liver (D, E, F) of zebrafish fed clofibrate. The level of mRNA and hnRNA was determined by RT-qPCR using gene-specific primers. The steady-state level offabp transcripts was normalized to the steady-state level ofrpl13α transcripts in the same sample. Data are presented as the mean ratio ± S.E.M. Significant differences (p < 0.05) in the relative steady-state level offabp mRNAs between zebrafish [n = 12, (male = 6, female = 6)] fed different concentrations of clofibrate compared to zebrafish not fed clofibrate are indicated by an asterisk.
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