Differential transcriptional modulation of duplicated fatty acid-binding protein genes by dietary fatty acids in zebrafish (Danio rerio): evidence for subfunctionalization or neofunctionalization of duplicated genes
© Karanth et al; licensee BioMed Central Ltd. 2009
Received: 2 March 2009
Accepted: 2 September 2009
Published: 2 September 2009
In the Duplication-Degeneration-Complementation (DDC) model, subfunctionalization and neofunctionalization have been proposed as important processes driving the retention of duplicated genes in the genome. These processes are thought to occur by gain or loss of regulatory elements in the promoters of duplicated genes. We tested the DDC model by determining the transcriptional induction of fatty acid-binding proteins (Fabps) genes by dietary fatty acids (FAs) in zebrafish. We chose zebrafish for this study for two reasons: extensive bioinformatics resources are available for zebrafish at zfin.org and zebrafish contains many duplicated genes owing to a whole genome duplication event that occurred early in the ray-finned fish lineage approximately 230-400 million years ago. Adult zebrafish were fed diets containing either fish oil (12% lipid, rich in highly unsaturated fatty acid), sunflower oil (12% lipid, rich in linoleic acid), linseed oil (12% lipid, rich in linolenic acid), or low fat (4% lipid, low fat diet) for 10 weeks. FA profiles and the steady-state levels of fabp mRNA and heterogeneous nuclear RNA in intestine, liver, muscle and brain of zebrafish were determined.
FA profiles assayed by gas chromatography differed in the intestine, brain, muscle and liver depending on diet. The steady-state level of mRNA for three sets of duplicated genes, fabp1a/fabp1b.1/fabp1b.2, fabp7a/fabp7b, and fabp11a/fabp11b, was determined by reverse transcription, quantitative polymerase chain reaction (RT-qPCR). In brain, the steady-state level of fabp7b mRNAs was induced in fish fed the linoleic acid-rich diet; in intestine, the transcript level of fabp1b.1 and fabp7b were elevated in fish fed the linolenic acid-rich diet; in liver, the level of fabp7a mRNAs was elevated in fish fed the low fat diet; and in muscle, the level of fabp7a and fabp11a mRNAs were elevated in fish fed the linolenic acid-rich or the low fat diets. In all cases, induction of the steady-state level of fabp mRNAs by dietary FAs correlated with induced levels of hnRNA for a given fabp gene. As such, up-regulation of the steady-state level of fabp mRNAs by FAs occurred at the level of initiation of transcription. None of the sister duplicates of these fabp genes exhibited an increase in their steady-state transcript levels in a specific tissue following feeding zebrafish any of the four experimental diets.
Differential induction of only one of the sister pair of duplicated fabp genes by FAs provides evidence to support the DDC model for retention of duplicated genes in the zebrafish genome by either subfunctionalization or neofunctionalization.
In his seminal book, 'Evolution by Gene Duplication', Susumu Ohno  argued that one of the major mechanisms that facilitate the increasing complexity in the evolution of life is duplication of genes and whole genomes. Models to explain retention of duplicated genes in eukaryotic genomes have undergone a development of thought since Ohno proposed his model almost 40 years ago. Ohno  argued that most duplicated genes are lost from the genome owing to nonfunctionalization, a claim which has been validated by empirical evidence from Lynch and Conery . Nonfunctionalization is a process where deleterious mutations accumulate in the coding region of a gene giving rise to either a dysfunctional protein or no protein product. Duplicated genes might, however, be retained in the genome owing to mutations in the coding region that led to a novel function for the protein product of a gene, a process Ohno termed 'neofunctionalization'. This model by Ohno for the preservation of duplicated genes came to be known as the 'classical model'. Data primarily derived from genome sequencing projects over the past decade suggest that a much higher proportion of gene duplicates is preserved in the eukaryotic genome than predicted by Ohno's "classical model". To explain this apparent "conundrum", Force et al.  proposed the Duplication-Degeneration-Complementation (DDC) model in which subfunctionalization serves as an alternative mechanism, but not to the exclusion of neofunctionalization, for the preservation of duplicated genes. According to the DDC model, duplicated genes are retained in the genome either by subfunctionalization, where the functions of the ancestral gene are sub-divided between sister duplicate genes, or by neofunctionalization, where one of the duplicates acquires a new function. In this model, both processes occur by either loss or gain of cis-acting regulatory elements in the promoters of the duplicated genes. As with the "classical model" of Ohno , the DDC model proposes that most duplicated genes are lost from the genome (i.e., nonfunctionalization) owing to an accumulation of deleterious mutations in coding or control regions leading to functional decay.
We chose to test the DDC model of Force et al.  that subfunctionalization or neofunctionalization results in the retention of duplicated genes in the genome by investigating the expression of duplicated copies of fatty acid-binding protein (Fabp) genes, members of the multigene family of intracellular lipid-binding protein (iLBP) genes, in zebrafish for two reasons. First, bioinformatic resources for zebrafish are readily available, including linkage maps, extensive expressed sequence tags (EST) http://www.zfin.org and an almost complete genome sequence database http://www.ensembl.org/Danio_rerio. Second, and most importantly, owing to a whole genome duplication (WGD) event, an event that occurred early in the ray-finned fish radiation about 230-400 million years ago [4–7], we predicted that many members of the iLBP multigene family might exist as duplicated copies. This prediction has proved to be correct (see below).
The iLBPs are encoded by a highly conserved multigene family, which consists of the fatty acid- (FABP), cellular retinol- (CRBP) and cellular retinoic acid-binding protein (CRABP) genes [reviewed in [8–12]]. Currently, 17 paralogous iLBP genes have been identified in animals, but no member of this multigene family has been identified in plants and fungi. Schaap et al.  have suggested, therefore, that the first iLBP gene emerged after the divergence of animals from plants ~930-1000 million years ago. This ancestral iLBP gene presumably underwent a series of duplications followed by sequence divergence, giving rise to the diversity of the extant iLBP multigene family. This multigene family has been further augmented in ray-finned fishes by the WGD event mentioned above [4–7].
Originally, iLBP genes and their proteins were named according to the initial tissue of isolation, e.g., liver-type FABP (L-FABP), brain-type FABP (B-FABP), etc. Owing to some confusion with this earlier nomenclature, here we use the nomenclature proposed by Hertzel and Bernlohr  in which numerals distinguish the different FABP proteins and their genes, (e.g., FABP1 (liver-type), FABP7 (brain-type)).
FABP1, the first FABP isolated, was described almost 40 years ago . Although extensive studies in mammals have focused on the tissue distribution and binding activities of FABPs, the regulation and evolution of their genes, and mice FABP gene knock-outs [8, 10–12], the precise physiological roles of FABPs remain unclear. However, accumulated data have provided evidence that FABPs play an important role in uptake, sequestering and transport of fatty acids and interaction with other transport and enzyme systems. Indirect evidence suggests other putative physiological functions for FABPs, such as: (i) transport of fatty acids to the nucleus to regulate gene transcription via activation of the nuclear receptors, the peroxisome proliferator-activated receptors (PPAR) [see e.g., [12, 16]]; (ii) essential functions in early development, especially neural growth and differentiation [see [17, 18] and references therein]; and (iii) a role in human diseases [10, 12].
Although the coding sequence and structure of the FABP genes has been well conserved over millions of years, each FABP gene exhibits a distinct, yet sometimes overlapping pattern of tissue-specific expression with other FABP genes. If all FABP genes in this multigene family arose from a single ancestral gene as proposed , the regulatory elements in the promoters must have evolved different functions in the subsequent duplicated genes giving rise to the complexity of the spatio-temporal expression of this multigene family. Regulatory elements in the promoters of some mammalian FABP genes and one insect have been identified [8, 19]. As such, cis-acting elements that determine the spatio-temporal expression of these genes, with a few exceptions, are not well defined. From sequence data, it appears that mammalian iLBP gene-promoters consist of a modular structure similar to many eukaryotic promoters, comprised commonly of a TATA box with proximal and distal regulatory elements . Currently, our understanding of the regulatory elements that control the expression of the FABP genes is modest and limited primarily to mammals [but see [21–23]]. Based on the zebrafish fabp10 sequence , Her et al.,  cloned its promoter and by functional analysis, identified a 435 bp regulatory element that is sufficient to modulate the liver regional expression in transgenic zebrafish. How this cis-acting element functions is not known. In addition to functional promoter studies, fatty acids and peroxisome proliferators have been shown to induce the transcription of some FABP genes in mammals [25, 26] via activation of PPAR, or other unknown transcription factors, that bind to a fatty acid (FA) response element (FARE) .
To date, we have characterized 11 zebrafish FABP genes with respect to their cDNA sequence, gene structure, chromosome location, conserved gene synteny with their mammalian orthologs, and their spatio-temporal patterns of expression in embryos, larvae and adults [17, 18, 24, 27–34]. Based on phylogenetic analyses and conserved gene synteny with their single-copy, mammalian orthologs, eight (four pairs) out of 11 of the extant members of the zebrafish FABP genes arose as a result of the ray-finned fish-specific WGD event [[18, 32, 33] and unpublished data]. One pair of genes, fabp1b.1 and fabp1b.2, are tandemly-arrayed on chromosome 8 separated by ~4 kb of DNA [unpublished data]. This duplication, which was subsequent to the WGD but is not yet dated, is presumably the result of unequal crossing-over between homologous chromosomes during meiosis. The number of duplicated FABP genes (63%) retained in the zebrafish genome owing to the WGD event in the ray-finned fishes lineage is remarkable as Postlethwaith et al.  estimate that only 20% of all the duplicated genes following WGD have been retained in the zebrafish genome. Other estimates for retention of duplicated genes in the zebrafish genome from the WGD are 14-30% . Three zebrafish FABP genes, fabp2, fabp3 and fabp6 exist as single copies (a duplicate of fabp10 has recently been identified by us [unpublished data]). Following the WGD event, the sister duplicates of these genes have presumably been lost by accumulation of mutations leading to functional decay.
In mammals, FAs up-regulate the expression of some FABP genes as evidenced by an increase in mRNA and protein levels [25, 26]. We hypothesized that (i) zebrafish fabp genes might be up-regulated by dietary FAs, and (ii) sister duplicated fabp genes might be differentially modulated by dietary FAs. We show by assaying steady-state mRNA and heterogeneous nuclear RNA (hnRNA) levels for three sets of duplicated fapb genes, fabp1a/fabp1b.1/fabp1b.2, fabp7a/fabp7b and fabp11a/fabp11b, that dietary FAs modulate the transcriptional initiation of only one of the duplicated fabp genes in specific tissues of zebrafish. This result provides compelling evidence that these duplicated fabp genes were retained in the genome by either subfunctionalization or neofunctionalization owing to the divergence of cis-acting regulatory elements in the fabp gene promoters.
The steady-state level of fabpmRNAs does not differ between sexes of zebrafish
Several authors have argued that lipid metabolism is influenced by the sex of an organism. For example, long-chain fatty acids are cleared from plasma by the liver more rapidly in female rats than male rats . Bass et al.  reported that female rats have a higher intracellular concentration of FABP3 than male rats. We, therefore, assayed by reverse transcription, quantitative polymerase chain reaction (RT- qPCR) the steady-state level of mRNA encoded by each fabp gene in intestine, liver, muscle and brain of male and female zebrafish reared on Tetramin® (Tetrawerke, Melle, Germany) flake diet. No difference in the steady-state level of fabp mRNAs in a specific tissue (i.e., intestine, liver, muscle or brain) was observed between male and female zebrafish (data not shown).
Effect of diet on the FA composition in different tissues of zebrafish
Composition of experimental diets (g/100 g of dry diet)
Vitamin free Casein1
Corn starch (pre-gelatinized)5
Effect of diet on the steady-state level of fabp1a/fabp1b.1/fabp1b.2mRNAs in different tissues
Effect of diet on the steady-state level of fabp7a and fabp7bmRNAs in different tissues
The steady-state level of fabp7a mRNAs was 4-fold higher in the liver of fish fed LFD compared to the transcript levels in the liver of fish fed one of the three other diets (Fig. 3C). The steady-state level of fabp7a mRNAs was 3-fold higher in muscle of fish fed LND compared to mRNAs levels for this gene in muscle of fish fed LD, but was not different in the muscle of fish fed HD and LFD (Fig. 3E). No difference was observed in the steady-state level of fabp7b mRNAs in liver of fish fed any of the four experimental diets (Fig. 3D). Finally, fabp7b mRNAs were not quantifiable by RT-qPCR in muscle (Fig. 3F).
Effect of diet on steady-state level of fabp11a and fabp11bmRNAs in different tissues
Modulation of the steady-state level of fabpmRNAs is due to up-regulation of transcriptional initiation
Heterogeneous RNA (hnRNA) for a given gene is rapidly processed to a mature mRNA transcript by removal of intervening sequences and the addition of a 5' cap and a poly(A) tail . As such, the level of hnRNA for a given gene indirectly correlates with the rate of initiation of transcription for that gene. To test whether the observed increase in the steady-state level of fabp mRNAs by dietary FAs was due to increased transcriptional initiation, the steady-state level of hnRNA for a specific fabp gene was assayed by RT-qPCR in different tissues of zebrafish fed the four experimental diets.
Effect of diet on FA profiles in tissues of zebrafish
The FA composition in tissues of fish is mediated by various metabolic activities, such as fatty acid desaturation, elongation , and β-oxidation . The composition of FAs in tissues is also influenced by dietary lipids [40–42]. In the current study, the FA composition of the four diets fed zebrafish affected the FA profiles of intestine, liver, muscle, and brain (Fig. 1 and additional file 1: Tables S1-S4). Our results are consistent with other studies in which dietary FAs modified the FA profile in zebrafish and other fishes [43–48].
Dietary FAs modulate the steady-state level of fabpmRNAs
Induction of the steady-state level of mRNA and hnRNA coded by fabp genes in tissues of zebrafish fed one of the four diets differing in FA content.
Differential modulation of fabp1b.1, but not fabp1a and fabp1b.2transcription by dietary FAs
FAs are known to induce the expression of the Fabp1 gene in the mammalian intestine [25, 36, 49, 70, 71]. Feeding of high-fat diets rich in vegetable oils resulted in a 30-40% increase in the cytosolic content of FABP1 in the rat intestine [36, 49]. Rats weaned to a high-fat diet showed higher levels of Fabp1 mRNAs in their intestine than those weaned to a low-fat diet [70, 71]. Also, feeding rats a diet containing 6% sunflower oil (rich in linoleic acid) resulted in the greater induction of Fabp1 in intestine compared to rats fed a diet containing 3% sunflower oil .
Since FAs, such as oleic acid, linoleic acid and linolenic acid, induce the expression of the mammalian FABP1 gene [25, 26, 70, 71], we anticipated that the steady-state level of mRNAs for all the duplicated copies of zebrafish fabp1 (fabp1a, fabp1b.1, and fabp1b.2), might be modulated by the different FAs in one or more of the experimental diets. However, in this study, we only observed up-regulation of the steady-state level of fabp1b.1 mRNAs in the intestine of fish fed LND (Fig. 2) at the level of transcriptional initiation (Fig. 5). The steady-state level of fabp1a (Fig. 2) and fabp1b.2 mRNAs remained unchanged in the different tissues of zebrafish fed experimental diets. We conclude, therefore, that the fabp1a and fabp1b.2 genes, but not the fabp1b.1 gene, no longer respond to dietary FAs owing to loss of cis-regulatory elements in their respective promoters. In their study of cis-regulatory elements after a WGD event in yeast, Papp et al.  concluded that the total number of cis-regulatory elements remained unchanged over time between duplicated genes. They further suggest that the number of shared cis-regulatory elements between duplicated genes decreased. The difference in the mode of gene regulation reported here for the duplicated fabp1s may be due to loss of cis-regulatory elements in the fabp1a and fabp1b.2 genes, a mechanism consistent with the process of subfunctionalization.
In contrast, zebrafish fabp1s exhibit a divergent pattern in their tissue-specific distribution of transcripts when compared to their mammalian ortholog. Mammalian Fabp1 transcripts were abundant in the intestine, liver and were detected at lower levels in kidney, ovary, and lung [12, 73]. In adult zebrafish, fabp1a transcripts were detected in the intestine , whereas fabp1b.1 transcripts were abundant in the intestine  but detected at lower levels in the liver, heart, gills, ovary and testes [unpublished data]. Zebrafish fabp1b.2 transcripts were abundant in the intestine, ovary and skin, and detected at lower levels in the brain, heart and eye [unpublished data]. This divergent tissue-specific distribution of transcripts for the duplicate fabp1 genes differs from previously reported examples of subfunctionalization , where the combined tissue-specific expression of duplicated zebrafish genes equals the tissue-specific expression of their mammalian ortholog, as described for the duplicated hoxb1a and hoxb1b , mitfa and mitfb [75, 76], and sox11a and sox11b  genes. Comparative functional analysis of cis-regulatory elements of Fabp1 genes will be necessary to determine if the duplicated fabp1 genes are retained in the zebrafish genome due to either subfunctionalization or neofunctionalization.
Tissue-specific transcriptional modulation of fabp7a and fabp7bmRNAs by dietary FAs
In this study, duplicated copies of zebrafish fabp7, fabp7a and fabp7b, exhibited distinct patterns of up-regulation by dietary FAs in different tissues for steady-state levels of both mRNA and hnRNA (Figs. 3 and 5). The steady-state level of fabp7a mRNAs in muscle and liver were elevated in zebrafish fed LND and LFD, whereas the steady-state level of fabp7b mRNAs was modulated in brain and intestine of the fish fed LD and LND.
Mammalian Fabp7 transcripts are detected in brain, retina, spinal cord and mammary gland [8, 12]. Zebrafish fabp7a transcripts are detected in brain, spinal cord, retina, testis, liver, intestine, and muscle  and zebrafish fabp7b transcripts are detected in brain, retina, testis, liver, intestine, skin, and swim bladder . In addition, the steady-state level of zebrafish fabp7b transcripts, but not fabp7a transcripts, was up-regulated in the brain of zebrafish fed LD (Fig 3).
Since the duplicated copies of the zebrafish fabp7, fabp7a and fabp7b, show a different tissue-specific pattern of expression compared to their mammalian ortholog and exhibit a different mode of gene regulation by dietary FAs from each other, it is possible that either subfunctionalization or neofunctionalization may account for the retention of both duplicated fabp7 genes in the zebrafish genome.
Transcriptional modulation of fabp11a, but not fabp11b, by dietary FAs
Previously, we reported that the duplicated copies of the zebrafish fabp11 gene and the tetrapod FABP4, FABP5, FABP8 and FABP9 genes are derived from a common ancestral gene . To date, the fabp11 gene has only been identified in fishes [33, 78]. This study shows that both the steady-state level of fabp11a mRNAs (Fig. 4) and hnRNAs (Fig. 5) was only elevated in muscle of fish fed LFD, but not in muscle of fish fed one of the other three diets. Although fabp11a and fabp11b exhibit different tissue-specific patterns of expression in embryos, larvae and adult zebrafish [29, 33] and differential regulation by dietary FAs, we are unable at this time to resolve whether these duplicated genes were retained in the genome by either subfunctionalization or neofunctionalization as no ortholog of this gene has been identified thus far in other species, such as birds or mammals.
In this study, we show that dietary FAs change the FA profile in intestine, liver, muscle and brain of zebrafish. The tissue-specific changes in FA content modulated the steady-state level of mRNAs for only one sister duplicate of three pairs of duplicated genes of the fabp multigene family in zebrafish (Table 2). Furthermore, changes in fabp hnRNA directly correlated with changes in the steady-state levels of fabp mRNAs, suggesting that the affects of FAs on these fabp genes occurred at the site of transcriptional initiation (Table 2). These findings indicate that the retention of duplicated fabp genes in the zebrafish genome is most likely the result of either subfunctionalization or neofunctionalization. To distinguish between these processes as outlined in the DDC model  will require functional analysis of the fabp promoters to identify cis-elements responsible for transcriptional induction by FAs.
Diets and fish husbandry
Major fatty acids in the experimental diets1
One hundred and eighty wild-type inbred zebrafish siblings (mean wt. 0.26 g), bred from 2 males and 2 females (obtained from a local aquarium supply store) to control for genetic variance, were randomly assigned to 12 aquaria (35 l) with 15 fish per tank at approximately 20 weeks of age. Each dietary treatment had three tank replicates to control for environmental variance. Fishes were acclimatized for 15 days and fed Tetramin® (Tetrawerke, Melle, Germany) twice a day to satiation. The Tetramin diet was discontinued and then fish were fed one of the four diets twice a day at 0900 h and 1900 h to satiation for 10 weeks. A constant water temperature (28°C), a light/dark cycle (14/10 h) and other water parameters were maintained according to Westerfield . Feeding was stopped 24 h prior to sampling of tissue. Fish were individually euthanized by immersion in 0.2% MS-222, weighed and dissected to collect intestine, liver, muscle and brain tissues for RNA and FA analysis. Animal husbandry and protocols for this experiment were reviewed by the Animal Care Committee of Dalhousie University in accordance with the Canadian Council on Animal Care.
RNA isolation, cDNA synthesis and RT-qPCR
Primers used for the quantification of fabp mRNA and hnRNA
Entrez gene ID
The target sequence for each gene was quantified to generate a standard curve of known copy number. Amplification of cDNA samples and DNA standards was carried out using the SYBRGreen Quantitect PCR Kit (Qiagen, Mississauga, Ontario, Canada) following the manufacturer's instructions. For thermal cycling and fluorescence detection, a Rotor-Gene 3000 system (Corbett Research, Sydney, Australia) was used. PCR conditions were as follows: initial denaturation for 15 min at 95°C followed by 40 cycles of 15 s denaturation at 94°C, 20 s annealing of primers at different temperatures depending on the primer pairs (see Table 4), and 30 s of elongation at 72°C. Following the PCR cycles, the melting temperature of the PCR product was determined to assess its purity. Fluorescence was measured following each cycle. The copy numbers of mRNA and hnRNA for each fabp gene were determined using the standard curves as explained by Bustin et al. . As negative controls, the reverse transcriptase was omitted from cDNA synthesis reactions for each sample and these controls were subjected to RT-qPCR. To determine the relative steady-state level of fabp mRNA and hnRNA in each tissue, the absolute copy number of fabp mRNA and hnRNA transcripts was divided by the copy number of ef1α mRNA and hnRNA transcripts in each sample.
Lipid extraction, FAME preparation and gas chromatography
A modified Folch procedure  described by Budge et al.  was used to extract neutral lipid fractions from tissues. Briefly, the tissues were homogenized and sonicated for four minutes in 8:4:3 chloroform:methanol:water and the process was repeated four times. Following each extraction, the organic layer was removed, pooled and concentrated under a gentle stream of nitrogen. FA methyl esters (FAMEs) of tissue and dietary lipid were prepared with 7% boron trifluoride in methanol and heating to 100°C for 60 minutes . FAMEs were separated by a gas chromatograph equipped with a flame-ionization detector (Hewlett Packard 6890 GC system, Wilmington, Delaware, USA) on an Omegawax 320 capillary column (30 m × 0.32 mm × 0.25 μm; Supelco, Bellefonte, Pennsylvania, USA). FAMEs were identified by comparison of retention times with those of known standards (Supelco 37 and menhaden oil; Supelco, Bellefonte, Pennsylvania, USA).
Microsoft Excel® 2003 and SPSS® 14.0 (Chicago, USA) were used for statistical analysis. The relative abundance of mRNA and hnRNA encoded by each fabp gene is presented as means ± S.E.M. The significance level was set at P < 0.05. The effect of diet on FA composition and the relative abundance of mRNA and hnRNA encoded by each fabp gene in different tissues were analyzed by one-way ANOVA. Post hoc comparisons were conducted using the Tukey's HSD test.
List of Abbreviations
fatty acid-binding protein
intracellular lipid-binding protein
whole genome duplication
highly unsaturated FA-rich diet
linoleic acid-rich diet
linolenic acid-rich diet
low fat diet
standard error of means
reverse transcription, quantitative polymerase chain reaction.
The authors acknowledge Sean Tibbetts for advice during diet preparation, Joyce Milley for advice on lipid analysis, and the help of Daniel Sawler with RT-qPCR during this study. We gratefully appreciate the comments of Dr. Vanya Ewart on a draft of the manuscript. This work was supported by funds from the Natural Sciences and Engineering Research Council of Canada (to JMW), Canadian Institutes of Health Research (to ED-W), and National Research Council of Canada (to SPL). SK is recipient of a Faculty of Graduate Studies Scholarship from Dalhousie University.
- Ohno S: Evolution by gene duplication. 1970, Springer-Verlag. New York, New York, USAView ArticleGoogle Scholar
- Lynch M, Conery JS: The evolutionary fate and consequences of duplicate genes. Science. 2000, 290 (5494): 1151-1155. 10.1126/science.290.5494.1151.View ArticlePubMedGoogle Scholar
- Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999, 151 (4): 1531-1545.PubMed CentralPubMedGoogle Scholar
- Postlethwait JH, Woods IG, Ngo-Hazelett P, Yan YL, Kelly PD, Chu F, Huang H, Hill-Force A, Talbot WS: Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res. 2000, 10 (12): 1890-1902. 10.1101/gr.164800.View ArticlePubMedGoogle Scholar
- Mulley J, Holland P: Comparative genomics - small genome, big insights. Nature. 2004, 431 (7011): 916-917. 10.1038/431916a.View ArticlePubMedGoogle Scholar
- Woods IG, Wilson C, Friedlander B, Chang P, Reyes DK, Nix R, Kelly PD, Chu F, Postlethwait JH, Talbot WS: The zebrafish gene map defines ancestral vertebrate chromosomes. Genome Res. 2005, 15 (9): 1307-1314. 10.1101/gr.4134305.PubMed CentralView ArticlePubMedGoogle Scholar
- Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, Prince VE, Yang ZH, Thomas MG, Coates MI: A new time-scale for ray-finned fish evolution. P Roy Soc B-Biol Sci. 2007, 274 (1609): 489-498. 10.1098/rspb.2006.3749.View ArticleGoogle Scholar
- Haunerland NH, Spener F: Fatty acid-binding proteins - insights from genetic manipulations. Prog Lipid Res. 2004, 43 (4): 328-349. 10.1016/j.plipres.2004.05.001.View ArticlePubMedGoogle Scholar
- Li E, Norris AW: Structure/function of cytoplasmic vitamin A-binding proteins. Annual Review of Nutrition. 1996, 16: 205-234. 10.1146/annurev.nu.16.070196.001225.View ArticlePubMedGoogle Scholar
- Storch J, Corsico B: The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu Rev Nutr. 2008, 28: 73-95. 10.1146/annurev.nutr.27.061406.093710.View ArticlePubMedGoogle Scholar
- Schroeder F, Petrescu AD, Huang H, Atshaves BP, McIntosh AL, Martin GG, Hostetler HA, Vespa A, Landrock D, Landrock KK: Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 2008, 43 (1): 1-17. 10.1007/s11745-007-3111-z.View ArticlePubMedGoogle Scholar
- Furuhashi M, Hotamisligil GS: Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov. 2008, 7 (6): 489-503. 10.1038/nrd2589.PubMed CentralView ArticlePubMedGoogle Scholar
- Schaap FG, van der Vusse GJ, Glatz JF: Evolution of the family of intracellular lipid binding proteins in vertebrates. Mol Cell Biochem. 2002, 239 (1-2): 69-77. 10.1023/A:1020519011939.View ArticlePubMedGoogle Scholar
- Vogel Hertzel A, Bernlohr DA: The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrin Met. 2000, 11 (5): 175-180. 10.1016/S1043-2760(00)00257-5.View ArticleGoogle Scholar
- Ockner RK, Manning JA, Poppenhausen RB, Ho WK: A binding protein for fatty acids in cytosol of intestinal mucosa, liver, myocardium, and other tissues. Science. 1972, 177 (43): 56-58. 10.1126/science.177.4043.56.View ArticlePubMedGoogle Scholar
- Leaver MJ, Boukouvala E, Antonopoulou E, Diez A, Favre-Krey L, Ezaz MT, Bautista JM, Tocher DR, Krey G: Three peroxisome proliferator-activated receptor isotypes from each of two species of marine fish. Endocrinology. 2005, 146 (7): 3150-3162. 10.1210/en.2004-1638.View ArticlePubMedGoogle Scholar
- Liu RZ, Denovan-Wright EM, Wright JM: Structure, mRNA expression and linkage mapping of the brain-type fatty acid-binding protein gene (fabp7) from zebrafish (Danio rerio). Eur J Biochem. 2003, 270 (4): 715-725. 10.1046/j.1432-1033.2003.03432.x.View ArticlePubMedGoogle Scholar
- Liu RZ, Denovan-Wright EM, Degrave A, Thisse C, Thisse B, Wright JM: Differential expression of duplicated genes for brain-type fatty acid-binding proteins (fabp7a and fabp7b) during early development of the CNS in zebrafish (Danio rerio). Gene Expr Patterns. 2004, 4 (4): 379-387. 10.1016/j.modgep.2004.01.010.View ArticlePubMedGoogle Scholar
- Wu Q, Chang W, Rickers-Haunerland J, Higo T, Haunerland NH: Characterization of a new fatty acid response element that controls the expression of the locust muscle FABP gene. Mol Cell Biochem. 2002, 239 (1-2): 173-180. 10.1023/A:1020554824176.PubMedGoogle Scholar
- Carey M, Smale ST: Transcriptional regulation in eukaryotes: concepts, strategies and techniques. 1999, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USAGoogle Scholar
- Wu Q, Haunerland NH: A novel fatty acid response element controls the expression of the flight muscle FABP gene of the desert locust, Schistocerca gregaria. Eur J Biochem. 2001, 268 (22): 5894-5900. 10.1046/j.0014-2956.2001.02538.x.View ArticlePubMedGoogle Scholar
- Her GM, Chiang CC, Chen WY, Wu JL: In vivo studies of liver-type fatty acid binding protein (L-FABP) gene expression in liver of transgenic zebrafish (Danio rerio). FEBS Letters. 2003, 538 (1-3): 125-133. 10.1016/S0014-5793(03)00157-1.View ArticlePubMedGoogle Scholar
- Qu H, Cui L, Rickers-Haunerland J, Haunerland NH: Fatty acid-dependent expression of the muscle FABP gene - comparative analysis of gene control in functionally related, but evolutionary distant animal systems. Mol Cell Biochem. 2007, 299 (1-2): 45-53. 10.1007/s11010-005-9036-z.View ArticlePubMedGoogle Scholar
- Denovan-Wright EM, Pierce M, Sharma MK, Wright JM: cDNA sequence and tissue-specific expression of a basic liver-type fatty acid binding protein in adult zebrafish (Danio rerio). BBA-Gene Struct Expr. 2000, 1492 (1): 227-232.View ArticleGoogle Scholar
- Poirier H, Niot I, Monnot MC, Braissant O, Meunier-Durmort C, Costet P, Pineau T, Wahl W, Willson TM, Besnard P: Differential involvement of peroxisome proliferator-activated receptors alpha and delta in fibrate and fatty-acid-mediated inductions of the gene encoding liver fatty acid-binding protein in the liver and the small intestine. Biochem J. 2001, 355: 481-488. 10.1042/0264-6021:3550481.PubMed CentralView ArticlePubMedGoogle Scholar
- Meunier-Durmort C, Poirier H, Niot I, Forest C, Besnard P: Up-regulation of the expression of the gene for liver fatty acid-binding protein by long-chain fatty acids. Biochem J. 1996, 319: 483-487.PubMed CentralView ArticlePubMedGoogle Scholar
- Denovan-Wright EM, Pierce M, Wright JM: Nucleotide sequence of cDNA clones coding for a brain-type fatty acid binding protein and its tissue-specific expression in adult zebrafish (Danio rerio). BBA-Gene Struct Expr. 2000, 1492 (1): 221-226.View ArticleGoogle Scholar
- Liu RZ, Denovan-Wright EM, Wright JM: Structure, linkage mapping and expression of the heart-type fatty acid-binding protein gene (fabp3) from zebrafish (Danio rerio). Eur J Biochem. 2003, 270 (15): 3223-3234. 10.1046/j.1432-1033.2003.03705.x.View ArticlePubMedGoogle Scholar
- Liu RZ, Saxena V, Sharma MK, Thisse C, Thisse B, Denovan-Wright EM, Wright JM: The fabp4 gene of zebrafish (Danio rerio) - genomic homology with the mammalian FABP4 and divergence from the zebrafish fabp3 in developmental expression. FEBS J. 2007, 274 (6): 1621-1633. 10.1111/j.1742-4658.2007.05711.x.View ArticlePubMedGoogle Scholar
- Pierce M, Wang YM, Denovan-Wright EM, Wright JM: Nucleotide sequence of a cDNA clone coding for an intestinal-type fatty acid binding protein and its tissue-specific expression in zebrafish (Danio rerio). BBA-Gene Struct Expr. 2000, 1490 (1-2): 175-183.View ArticleGoogle Scholar
- Sharma MK, Denovan-Wright EM, Degrave A, Thisse C, Thisse B, Wright JM: Sequence, linkage mapping and early developmental expression of the intestinal-type fatty acid-binding protein gene (fabp2) from zebrafish (Danio rerio). Comp Biochem Phys B. 2004, 138 (4): 391-398. 10.1016/j.cbpc.2004.05.009.View ArticleGoogle Scholar
- Sharma MK, Liu RZ, Thisse C, Thisse B, Denovan-Wright EM, Wright JM: Hierarchical subfunctionalization of fabp1a, fabp1b and fabp10 tissue-specific expression may account for retention of these duplicated genes in the zebrafish (Danio rerio) genome. FEBS J. 2006, 273 (14): 3216-3229. 10.1111/j.1742-4658.2006.05330.x.View ArticlePubMedGoogle Scholar
- Karanth S, Denovan-Wright EM, Thisse C, Thisse B, Wright JM: The evolutionary relationship between the duplicated copies of the zebrafish fabp11 gene and the tetrapod FABP4, FABP5, FABP8 and FABP9 genes. FEBS J. 2008, 275 (12): 3031-3040. 10.1111/j.1742-4658.2008.06455.x.View ArticlePubMedGoogle Scholar
- Alves-Costa FA, Denovan-Wright EM, Thisse C, Thisse B, Wright JM: Spatio-temporal distribution of fatty acid-binding protein 6 (fabp6) gene transcripts in the developing and adult zebrafish (Danio rerio). FEBS J. 2008, 275 (13): 3325-3334. 10.1111/j.1742-4658.2008.06480.x.View ArticlePubMedGoogle Scholar
- Luxon BA, Weisiger RA: Sex-differences in intracellular fatty-acid transport - role of cytoplasmic-binding proteins. Am J Physiol. 1993, 265 (5): G831-G841.PubMedGoogle Scholar
- Bass NM, Manning JA, Ockner RK, Gordon JI, Seetharam S, Alpers DH: Regulation of the biosynthesis of 2 distinct fatty acid-binding proteins in rat-liver and intestine - influences of sex difference and of clofibrate. J Biol Chem. 1985, 260 (3): 1432-1436.PubMedGoogle Scholar
- Watson JD, Baker TA, Bell SP, Gann A, Levine M, Losick R: Molecular biology of the gene. 2008, Pearson Benjamin Cummings/Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 415-421.Google Scholar
- Tocher DR: Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci. 2003, 11 (2): 107-184. 10.1080/713610925.View ArticleGoogle Scholar
- Henderson RJ, Sargent JR: Chain-length specificities of mitochondrial and peroxisomal beta-oxidation of fatty-acids in livers of rainbow-trout (Salmo gairdneri). Comp Biochem Phys B. 1985, 82 (1): 79-85. 10.1016/0305-0491(85)90131-2.Google Scholar
- Torstensen BE, Lie O, Froyland L: Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.) - effects of capelin oil, palm oil, and oleic acid-enriched sunflower oil as dietary lipid sources. Lipids. 2000, 35 (6): 653-664. 10.1007/s11745-000-0570-6.View ArticlePubMedGoogle Scholar
- Bell JG, Henderson RJ, Tocher DR, McGhee F, Dick JR, Porter A, Smullen RP, Sargent JR: Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. J Nutr. 2002, 132 (2): 222-230.PubMedGoogle Scholar
- Bell JG, McEvoy J, Tocher DR, McGhee F, Campbell PJ, Sargent JR: Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr. 2001, 131 (5): 1535-1543.PubMedGoogle Scholar
- Meinelt T, Schulz C, Wirth M, Kuerzinger H, Steinberg C: Dietary fatty acid composition influences the fertilization rate of zebrafish (Danio rerio Hamilton-Buchanan). J Appl Ichthyol/Z Angew Ichthyol. 1999, 15 (1): 19-23. 10.1046/j.1439-0426.1999.00121.x.View ArticleGoogle Scholar
- Meinelt T, Schulz C, Wirth M, Kürzinger H, Steinberg C: Correlation of diets high in n-6 polyunsaturated fatty acids with high growth rate in zebrafish (Danio rerio). Comparative Med. 2000, 50 (1): 43-45.Google Scholar
- Tocher DR, Agaba M, Hastings N, Bell JG, Dick JR, Teale AJ: Nutritional regulation of hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition in zebrafish (Danio rerio) and tilapia (Oreochromis niloticus). Fish Physiol Biochem. 2001, 24 (4): 309-320. 10.1023/A:1015022406790.View ArticleGoogle Scholar
- Jaya-Ram A, Kuah MK, Lim PS, Kolkovski S, Shu-Chien AC: Influence of dietary HUFA levels on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs expression in female zebrafish Danio rerio. Aquaculture. 2008, 277 (3-4): 275-281. 10.1016/j.aquaculture.2008.02.027.View ArticleGoogle Scholar
- Jordal AEO, Hordvik I, Pelsers M, Bemlohr DA, Torstensen BE: FABP3 and FABP10 in Atlantic salmon (Salmo salar L.) - general effects of dietary fatty acid composition and life cycle variations. Comp Biochem Phys B. 2006, 145 (2): 147-158. 10.1016/j.cbpb.2006.05.007.View ArticleGoogle Scholar
- Zheng XZ, Tocher DR, Dickson CA, Bell JG, Teale AJ: Effects of diets containing vegetable oil on expression of genes involved in highly unsaturated fatty acid biosynthesis in liver of Atlantic salmon (Salmo salar). Aquaculture. 2004, 236 (1-4): 467-483. 10.1016/j.aquaculture.2004.02.003.View ArticleGoogle Scholar
- Ockner RK, Manning JA: Fatty acid-binding protein in small intestine. Identification, isolation, and evidence for its role in cellular fatty acid transport. J Clin Invest. 1974, 54 (2): 326-38. 10.1172/JCI107768.PubMed CentralView ArticlePubMedGoogle Scholar
- Mochizuki K, Mochizuki H, Kawai H, Ogura Y, Shmada M, Takase S, Goda T: Possible role of fatty acids in milk as the regulator of the expression of cytosolic binding proteins for fatty acids and vitamin A through PPAR alpha in developing rats. J Nutr Sci Vitaminol. 2007, 53 (6): 515-521. 10.3177/jnsv.53.515.View ArticlePubMedGoogle Scholar
- Drozdowski L, Clement L, Keelan M, Niot I, Clandinin MT, Agellon L, Wild G, Besnard P, Thomson ABR: Dietary lipids modify intestinal lipid-binding protein RNA abundance in diabetic and control rats. Digestion. 2004, 70 (3): 192-198. 10.1159/000082832.View ArticlePubMedGoogle Scholar
- Schroeder F, Petrescu AD, Huang H, Atshaves BP, McIntosh AL, Martin GG, Hostetler HA, Vespa A, Landrock D, Landrock KK, et al: Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 2008, 43 (1): 1-17. 10.1007/s11745-007-3111-z.View ArticlePubMedGoogle Scholar
- Huang H, Starodub O, McIntosh A, Atshaves BP, Woldegiorgis G, Kier AB, Schroeder F: Liver fatty acid-binding protein colocalizes with peroxisome proliferator activated receptor alpha and enhances ligand distribution to nuclei of living cells. Biochemistry. 2004, 43 (9): 2484-2500. 10.1021/bi0352318.View ArticlePubMedGoogle Scholar
- Schroeder F, Atshaves BP, Starodub O, Boedeker AL, Smith R, Roths JB, Foxworth WB, Kier AB: Expression of liver fatty acid binding protein alters growth and differentiation of embryonic stem cells. Mol Cell Biochem. 2001, 219: 127-138. 10.1023/A:1010851130136.View ArticlePubMedGoogle Scholar
- Tan NS, Shaw NS, Vinckenbosch N, Liu P, Yasmin R, Desvergne B, Wahli W, Noy N: Selective cooperation between fatty acid binding proteins and peroxisome proliferator activated receptors in regulating transcription. Mol Cell Biochem. 2002, 22: 5114-5127. 10.1128/MCB.22.14.5114-5127.2002.View ArticleGoogle Scholar
- Budhu AS, Noy N: Direct channeling of retinoic acid between cellular retinoic acid binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid induced growth arrest. Mol Cell Biochem. 2002, 22: 2632-2641. 10.1128/MCB.22.8.2632-2641.2002.View ArticleGoogle Scholar
- Delva L, Bastie JN, Rochette-Egly C, Kraiba R, Balitrand N, Despouy G, Chambon P, Chomienne C: Physical and functional interactions between cellular retinoic acid binding protein II and the retinoic acid-dependent nuclear complex. Mol Cell Biochem. 1999, 19: 7158-7167.View ArticleGoogle Scholar
- Gottlicher M, Widmark E, Li Q, Gustafsson JA: Fatty acids activate a chimera of the clofibric acid-activated receptor and the glucocorticoid receptor. Proc Natl Acad Sci USA. 1992, 89: 4653-4657. 10.1073/pnas.89.10.4653.PubMed CentralView ArticlePubMedGoogle Scholar
- Keller H, Dreyer C, Medin J, Mahfoudi A, Ozato K, Wahli W: Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator activated receptor retinoid X receptor heterodimers. Proc Natl Acad Sci USA. 1993, 90: 2160-2164. 10.1073/pnas.90.6.2160.PubMed CentralView ArticlePubMedGoogle Scholar
- Escher P, Wahli W: Peroxisome proliferator activated receptors: insights into multiple cellular functions. Mutat Res. 2000, 448: 121-138.View ArticlePubMedGoogle Scholar
- Lemberger T, Desvergne B, Wahli W: Peroxisome proliferator-activated receptors. Annu Rev Cell Dev Biol. 1996, 12: 335-363. 10.1146/annurev.cellbio.12.1.335.View ArticlePubMedGoogle Scholar
- Wolfrum C, Borrmann CM, Borchers T, Spener F: Fatty acids and hypolipidemic drugs regulate PPARα and PPARγ gene expression via L-FABP: a signaling path to the nucleus. Proc Natl Acad Sci USA. 2001, 98: 2323-2328. 10.1073/pnas.051619898.PubMed CentralView ArticlePubMedGoogle Scholar
- Desvergne B, Wahli W: Peroxisome proliferator-activated receptors: Nuclear control of metabolism. Endocr Rev. 1999, 20 (5): 649-688. 10.1210/er.20.5.649.PubMedGoogle Scholar
- Puskas LG, Bereczki E, Santha M, Vigh L, Csanadi G, Spener F, Ferdinandy P, Onochy A, Kitajka K: Cholesterol and cholesterol plus DHA diet-induced gene expression and fatty acid changes in mouse eye and brain. Biochimie. 2004, 86 (11): 817-824. 10.1016/j.biochi.2004.10.004.View ArticlePubMedGoogle Scholar
- Berger A, Roberts MA, Hoff B: How dietary arachidonic- and docosahexaenoic-acid rich oils differentially affect the murine hepatic transcriptome. Lipids in Health and Disease. 2006, 5: 10-10.1186/1476-511X-5-10. doi:10.1186/1476-511X-5-10,PubMed CentralView ArticlePubMedGoogle Scholar
- Liu JW, Almaguel FG, Bu LM, De Leon DD, De Leon M: Expression of E-FABP in PC12 cells increases neurite extension during differentiation: involvement of n-3 and n-6 fatty acids. J Neurochem. 2008, 106 (5): 2015-2029.PubMed CentralPubMedGoogle Scholar
- Fontaine RN, Gossett RE, Schroeder F, Otoole BA, Doetschman T, Kier AB: Liver and intestinal fatty acid binding proteins in control and TGF beta 1 gene targeted deficient mice. Mol Cell Biochem. 1996, 159 (2): 149-153. 10.1007/BF00420917.View ArticlePubMedGoogle Scholar
- Belaguli NS, Zhang M, Rigi M, Aftab M, Berger DH: Cooperation between GATA4 and TGF-beta signaling regulates intestinal epithelial gene expression. Am J Physiol-Gastr L. 2007, 292 (6): G1520-G1533. 10.1152/ajpgi.00236.2006.Google Scholar
- Nagasawa T, Inada Y, Nakano S, Tamura T, Takahashi T, Maruyama K, Yamazaki Y, Kuroda J, Shibata N: Effects of bezafibrate, PPAR pan-agonist, and GW501516, PPAR delta agonist, on development of steatohepatitis in mice fed a methionine- and choline-deficient diet. Eur J Pharmacol. 2006, 536 (1-2): 182-191. 10.1016/j.ejphar.2006.02.028.View ArticlePubMedGoogle Scholar
- Mochizuki K, Mochizuki H, Kawai H, Ogura Y, Shmada M, Takase S, Goda T: Possible role of fatty acids in milk as the regulator of the expression of cytosolic binding proteins for fatty acids and vitamin A through PPAR alpha in developing rats. J Nutr Sci Vitaminol. 2007, 53 (6): 515-521. 10.3177/jnsv.53.515.View ArticlePubMedGoogle Scholar
- Lin MCM, Arbeeny C, Bergquist K, Kienzle B, Gordon DA, Wetterau JR: Cloning and regulation of hamster microsomal triglyceride transfer protein - the regulation is independent from that of other hepatic and intestinal proteins which participate in the transport of fatty-acids and triglycerides. J Biol Chem. 1994, 269 (46): 29138-29145.PubMedGoogle Scholar
- Papp B, Pal C, Hurst LD: Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet. 2003, 19 (8): 417-422. 10.1016/S0168-9525(03)00174-4.View ArticlePubMedGoogle Scholar
- The AceView genes. [http://www.ncbi.nlm.nih.gov/IEB/Research/Acembly]
- Prince VE, Pickett FB: Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet. 2002, 3 (11): 827-837. 10.1038/nrg928.View ArticlePubMedGoogle Scholar
- Lister JA, Close J, Raible DW: Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev Biol. 2001, 237 (2): 333-344. 10.1006/dbio.2001.0379.View ArticlePubMedGoogle Scholar
- Altschmied J, Delfgaauw J, Wilde B, Duschl J, Bouneau L, Volff JN, Schartl M: Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. Genetics. 2002, 161 (1): 259-267.PubMed CentralPubMedGoogle Scholar
- De Martino S, Yan YL, Jowett T, Postlethwait JH, Varga ZM, Ashworth A, Austin CA: Expression of sox11 gene duplicates in zebrafish suggests the reciprocal loss of ancestral gene expression patterns in development. Dev Dynam. 2000, 217 (3): 279-292. 10.1002/(SICI)1097-0177(200003)217:3<279::AID-DVDY6>3.0.CO;2-S.View ArticleGoogle Scholar
- Agulleiro MJ, Andre M, Morais S, Cerda J, Babin PJ: High transcript level of fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Biol Reprod. 2007, 77 (3): 504-516. 10.1095/biolreprod.107.061598.View ArticlePubMedGoogle Scholar
- National research council: Nutrient Requirements of Fish. 1993, National Academic Press, Washington DC, USAGoogle Scholar
- Goolish EM, Okutake K, Lesure S: Growth and survivorship of larval zebrafish (Danio rerio) on processed diets. N Am J Aquacult. 1999, 61 (3): 189-198. 10.1577/1548-8454(1999)061<0189:GASOLZ>2.0.CO;2.View ArticleGoogle Scholar
- Mathew P, Sherief P: Effects of dietary protein source on growth and survival of angelfish and zebrafish. 1999, Asian Fisheries Society, Indian Branch, Mangalore (India)Google Scholar
- Westerfield M: The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). 2000, Eugene: University of Oregon Press, 4Google Scholar
- Pattyn F, Speleman F, De Paepe A, Vandesompele J: RTPrimerDB: The real-time PCR primer and probe database. Nucleic Acids Res. 2003, 31 (1): 122-123. 10.1093/nar/gkg011.PubMed CentralView ArticlePubMedGoogle Scholar
- Bustin SA, Benes V, Nolan T, Pfaffl MW: Quantitative real-time RT-PCR - a perspective. J Mol Endocrinol. 2005, 34 (3): 597-601. 10.1677/jme.1.01755.View ArticlePubMedGoogle Scholar
- Folch J, Lees M, Sloane Stanley GH: A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957, 226 (1): 497-509.PubMedGoogle Scholar
- Budge SM, Parrish CC, McKenzie CH: Fatty acid composition of phytoplankton, settling particulate matter and sediments at a sheltered bivalve aquaculture site. Mar Chem. 2001, 76 (4): 285-303. 10.1016/S0304-4203(01)00068-8.View ArticleGoogle Scholar
- Martins DA, Valente LMP, Lall SP: Effects of dietary lipid level on growth and lipid utilization by juvenile Atlantic halibut (Hippoglossus hippoglossus, L.). Aquaculture. 2007, 263 (1-4): 150-158. 10.1016/j.aquaculture.2006.10.017.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.