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      Transcriptomic Analyses of Sexual Dimorphism of the Zebrafish Liver and the Effect of Sex Hormones

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          Abstract

          The liver is one of the most sex-dimorphic organs in both oviparous and viviparous animals. In order to understand the molecular basis of the difference between male and female livers, high-throughput RNA-SAGE (serial analysis of gene expression) sequencing was performed for zebrafish livers of both sexes and their transcriptomes were compared. Both sexes had abundantly expressed genes involved in translation, coagulation and lipid metabolism, consistent with the general function of the liver. For sex-biased transcripts, from in addition to the high enrichment of vitellogenin transcripts in spawning female livers, which constituted nearly 80% of total mRNA, it is apparent that the female-biased genes were mostly involved in ribosome/translation, estrogen pathway, lipid transport, etc, while the male-biased genes were enriched for oxidation reduction, carbohydrate metabolism, coagulation, protein transport and localization, etc. Sexual dimorphism on xenobiotic metabolism and anti-oxidation was also noted and it is likely that retinol x receptor (RXR) and liver x receptor (LXR) play central roles in regulating the sexual differences of lipid and cholesterol metabolisms. Consistent with high ribosomal/translational activities in the female liver, female-biased genes were significantly regulated by two important transcription factors, Myc and Mycn. In contrast, Male livers showed activation of transcription factors Ppargc1b, Hnf4a, and Stat4, which regulate lipid and glucose metabolisms and various cellular activities. The transcriptomic responses to sex hormones, 17β-estradiol (E2) or 11-keto testosterone (KT11), were also investigated in both male and female livers and we found that female livers were relatively insensitive to sex hormone disturbance, while the male livers were readily affected. E2 feminized male liver by up-regulating female-biased transcripts and down-regulating male-biased transcripts. The information obtained in this study provides comprehensive insights into the sexual dimorphism of zebrafish liver transcriptome and will facilitate further development of the zebrafish as a human liver disease model.

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          Most cited references61

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          Small-sample estimation of negative binomial dispersion, with applications to SAGE data.

          We derive a quantile-adjusted conditional maximum likelihood estimator for the dispersion parameter of the negative binomial distribution and compare its performance, in terms of bias, to various other methods. Our estimation scheme outperforms all other methods in very small samples, typical of those from serial analysis of gene expression studies, the motivating data for this study. The impact of dispersion estimation on hypothesis testing is studied. We derive an "exact" test that outperforms the standard approximate asymptotic tests.
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            Moderated statistical tests for assessing differences in tag abundance.

            Digital gene expression (DGE) technologies measure gene expression by counting sequence tags. They are sensitive technologies for measuring gene expression on a genomic scale, without the need for prior knowledge of the genome sequence. As the cost of sequencing DNA decreases, the number of DGE datasets is expected to grow dramatically. Various tests of differential expression have been proposed for replicated DGE data using binomial, Poisson, negative binomial or pseudo-likelihood (PL) models for the counts, but none of the these are usable when the number of replicates is very small. We develop tests using the negative binomial distribution to model overdispersion relative to the Poisson, and use conditional weighted likelihood to moderate the level of overdispersion across genes. Not only is our strategy applicable even with the smallest number of libraries, but it also proves to be more powerful than previous strategies when more libraries are available. The methodology is equally applicable to other counting technologies, such as proteomic spectral counts. An R package can be accessed from http://bioinf.wehi.edu.au/resources/
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              MYC as a regulator of ribosome biogenesis and protein synthesis.

              MYC regulates the transcription of thousands of genes required to coordinate a range of cellular processes, including those essential for proliferation, growth, differentiation, apoptosis and self-renewal. Recently, MYC has also been shown to serve as a direct regulator of ribosome biogenesis. MYC coordinates protein synthesis through the transcriptional control of RNA and protein components of ribosomes, and of gene products required for the processing of ribosomal RNA, the nuclear export of ribosomal subunits and the initiation of mRNA translation. We discuss how the modulation of ribosome biogenesis by MYC may be essential to its physiological functions as well as its pathological role in tumorigenesis.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                17 January 2013
                : 8
                : 1
                : e53562
                Affiliations
                [1 ]Department of Biological Sciences, National University of Singapore, Singapore, Singapore
                [2 ]Computational and Systems Biology, Genome Institute of Singapore, Singapore, Singapore
                Auburn University, United States of America
                Author notes

                Competing Interests: Co-author Zhiyuan Gongis is a PLOS ONE Editorial Board member. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: HX SHL ZG. Performed the experiments: HX WZ. Analyzed the data: WZ SHL ZG. Contributed reagents/materials/analysis tools: HL RKMK. Wrote the paper: WZ ZG.

                Article
                PONE-D-12-27355
                10.1371/journal.pone.0053562
                3547925
                23349717
                4b89e1ed-0bd7-4abb-b9bb-cc57b670178f
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 September 2012
                : 29 November 2012
                Page count
                Pages: 12
                Funding
                This work was supported by the Singapore National Research Foundation under its Environmental & Water Technologies Strategic Research Programme and administered by the Environment & Water Industry Programme Office (EWI) of the PUB, grant number R-154-000-328-272. The funders had no role in study design, data collection and analysis, decision to publish, or reparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Aquaculture
                Biology
                Biotechnology
                Environmental Biotechnology
                Genetics
                Gene Expression
                DNA transcription
                Molecular Genetics
                Gene Classes
                Gene Identification and Analysis
                Gene Regulation
                Gene Function
                Gene Networks
                Genomics
                Genome Analysis Tools
                Genome-Wide Association Studies
                Transcriptomes
                Comparative Genomics
                Functional Genomics
                Genome Expression Analysis
                Model Organisms
                Animal Models
                Zebrafish
                Toxicology
                Genetic Toxicology

                Uncategorized
                Uncategorized

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