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      Gene Expression Profiling Reveals New Potential Players of Gonad Differentiation in the Chicken Embryo

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          Abstract

          Background

          In birds as in mammals, a genetic switch determines whether the undifferentiated gonad develops into an ovary or a testis. However, understanding of the molecular pathway(s) involved in gonad differentiation is still incomplete.

          Methodology/Principal Findings

          With the aim of improving characterization of the molecular pathway(s) involved in gonad differentiation in the chicken embryo, we developed a large scale real time reverse transcription polymerase chain reaction approach on 110 selected genes for evaluation of their expression profiles during chicken gonad differentiation between days 5.5 and 19 of incubation. Hierarchical clustering analysis of the resulting datasets discriminated gene clusters expressed preferentially in the ovary or the testis, and/or at early or later periods of embryonic gonad development. Fitting a linear model and testing the comparisons of interest allowed the identification of new potential actors of gonad differentiation, such as Z-linked ADAMTS12, LOC427192 (corresponding to NIM1 protein) and CFC1, that are upregulated in the developing testis, and BMP3 and Z-linked ADAMTSL1, that are preferentially expressed in the developing ovary. Interestingly, the expression patterns of several members of the transforming growth factor β family were sexually dimorphic, with inhibin subunits upregulated in the testis, and bone morphogenetic protein subfamily members including BMP2, BMP3, BMP4 and BMP7, upregulated in the ovary. This study also highlighted several genes displaying asymmetric expression profiles such as GREM1 and BMP3 that are potentially involved in different aspects of gonad left-right asymmetry.

          Conclusion/Significance

          This study supports the overall conservation of vertebrate sex differentiation pathways but also reveals some particular feature of gene expression patterns during gonad development in the chicken. In particular, our study revealed new candidate genes which may be potential actors of chicken gonad differentiation and provides evidence of the preferential expression of BMPs in the developing ovary and Inhibin/Activin subunits in the developing testis.

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          Most cited references72

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Cluster analysis and display of genome-wide expression patterns.

            A system of cluster analysis for genome-wide expression data from DNA microarray hybridization is described that uses standard statistical algorithms to arrange genes according to similarity in pattern of gene expression. The output is displayed graphically, conveying the clustering and the underlying expression data simultaneously in a form intuitive for biologists. We have found in the budding yeast Saccharomyces cerevisiae that clustering gene expression data groups together efficiently genes of known similar function, and we find a similar tendency in human data. Thus patterns seen in genome-wide expression experiments can be interpreted as indications of the status of cellular processes. Also, coexpression of genes of known function with poorly characterized or novel genes may provide a simple means of gaining leads to the functions of many genes for which information is not available currently.
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              A series of normal stages in the development of the chick embryo. 1951.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                9 September 2011
                : 6
                : 9
                : e23959
                Affiliations
                [1 ]Physiologie de la Reproduction et des Comportements UMR 6175, INRA- CNRS-Université F. Rabelais de Tours-Haras Nationaux, Nouzilly, France
                [2 ]Unité de Recherche Avicole, INRA, Nouzilly, France
                Centro Cardiologico Monzino, Italy
                Author notes

                Conceived and designed the experiments: MSG. Performed the experiments: GAC IC MSG. Analyzed the data: GAC MSG. Contributed reagents/materials/analysis tools: GAC MSG. Wrote the paper: GAC MSG. Statistical analysis of the data: CHA.

                Article
                PONE-D-10-01606
                10.1371/journal.pone.0023959
                3170287
                21931629
                97878601-fdb4-40ae-9a6d-3214b0b9790a
                Carré et al. 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
                : 10 September 2010
                : 2 August 2011
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Developmental Biology
                Molecular Development
                Morphogens
                Morphogenesis
                Sexual Differentiation
                Cell Differentiation
                Embryology
                Model Organisms
                Animal Models
                Chicken
                Molecular Cell Biology
                Cellular Types
                Germ Cells
                Nucleic Acids
                RNA
                Gene Expression
                Zoology
                Ornithology

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                Uncategorized

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