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      Temporal transcriptome analysis of the chicken embryo yolk sac

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          Abstract

          Background

          The yolk sac (YS) is an extra-embryonic tissue that surrounds the yolk and absorbs, digests and transports nutrients during incubation of the avian embryo as well as during early term mammalian embryonic development. Understanding YS functions and development may enhance the efficient transfer of nutrients and optimize embryo development. To identify temporal large-scale patterns of gene expression and gain insights into processes and mechanisms in the YS, we performed a transcriptome study of the YS of chick embryos on embryonic days (E) E13, E15, E17, E19, and E21 (hatch).

          Results

          3547 genes exhibited a significantly changed expression across days. Clustering and functional annotation of these genes as well as histological sectioning of the YS revealed that we monitored two cell types: the epithelial cells and the erythropoietic cells of the YS. We observed a significant up-regulation of epithelial genes involved in lipid transport and metabolism between E13 and E19. YS epithelial cells expressed a vast array of lipoprotein receptors and fatty acid transporters. Several lysosomal genes ( CTSA, PSAP, NPC2) and apolipoproteins genes ( apoA1, A2, B, C3) were among the highest expressed, reflecting the intensive digestion and re-synthesis of lipoproteins in YS epithelial cells. Genes associated with cytoskeletal structure were down-regulated between E17 and E21 supporting histological evidence of a degradation of YS epithelial cells towards hatch.

          Expression patterns of hemoglobin synthesis genes indicated a high erythropoietic capacity of the YS between E13 and E15, which decreased towards hatch. YS histological sections confirmed these results. We also observed that YS epithelial cells expressed high levels of genes coding for plasma carrier proteins ( ALB, AFP, LTF, TTR), normally produced by the liver.

          Conclusions

          Here we expand current knowledge on developmental, nutritional and molecular processes in the YS. We demonstrate that in the final week of chick embryonic development, the YS plays different roles to support or replace the functions of several organs that have not yet reached their full functional capacity. The YS has a similar functional role as the intestine in digestion and transport of nutrients, the liver in producing plasma carrier proteins and coagulation factors, and the bone marrow in synthesis of blood cells.

          Electronic supplementary material

          The online version of this article (doi:10.1186/1471-2164-15-690) contains supplementary material, which is available to authorized users.

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          Most cited references40

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

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            Studying and modelling dynamic biological processes using time-series gene expression data.

            Biological processes are often dynamic, thus researchers must monitor their activity at multiple time points. The most abundant source of information regarding such dynamic activity is time-series gene expression data. These data are used to identify the complete set of activated genes in a biological process, to infer their rates of change, their order and their causal effects and to model dynamic systems in the cell. In this Review we discuss the basic patterns that have been observed in time-series experiments, how these patterns are combined to form expression programs, and the computational analysis, visualization and integration of these data to infer models of dynamic biological systems.
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              Nutrition of the developing embryo and hatchling.

              E.T. Moran (2007)
              Nutrient needs central to satisfactory egg incubation well-being undergo several major changes from fertilization until the reliance of the chick on feed. Glucose is central, with the initiation of incubation until the chorioallantois accesses O(2) to use for fatty acid oxidation. Nutrient recovery from albumen and yolk is largely commensurate with body assembly through to completion of the embryo by 14 d. Remaining albumen mixes with the amniotic fluid and is orally consumed until initiation of emergence. A portion of the albumen is absorbed by the small intestine to expand body glycogen reserves. The residual not absorbed contains digestive enzyme contributions and enters the yolk sac through its stalk at the jejunum and ileum. Interaction of the albumen-amnion digestive enzyme mixture with yolk sac contents leads to diverse alterations that influence subsequent use of lipids. Rapid removal of very low-density lipoprotein ensues, until pipping with triglycerides, expanding body fat depots while cholesterol deposits in the liver. A concurrent translocation of Ca from shell mineralizes the skeletal system while also crossing yolk sac villi for deposition on phosvitin-based granules accruing in its lumen. Loss of chorioallantois with pipping and the start of pulmonary respiration predispose a dependence on glycolysis to support emergence. Small intestinal villi progressively reorient their enterocytes from macromolecule transfer to competence at digestion and absorption after hatching. Mobilization of body fat complements contributions from the yolk sac to provide fatty acids for generating energy, heat, and water while also combining with hepatic cholesterol for membrane expansion and continued development. Calcified granules evacuate the yolk sac to further skeletal mineralization in the absence of shell contributions. Egg mass, its interior quality, and turning during early incubation directly influence the ability of the embryo to access nutrients and provide resources to support emergence and the transition of the chick to self-sufficiency.
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                Author and article information

                Contributors
                liran.yadgary@mail.huji.ac.il
                ewong@vt.edu
                zehava.uni@mail.huji.ac.il
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                19 August 2014
                19 August 2014
                2014
                : 15
                : 1
                : 690
                Affiliations
                [ ]Department of Animal Science, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University, 76100 Rehovot, Israel
                [ ]Department of Animal and Poultry Sciences, Virginia Tech, 24061 Blacksburg, VA USA
                Article
                6680
                10.1186/1471-2164-15-690
                4246430
                25141977
                3395677c-6ce4-4acb-9f26-3972b4f7e3b4
                © Yadgary et al.; licensee BioMed Central Ltd. 2014

                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 credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 17 January 2014
                : 12 August 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                yolk sac,gene expression,transcriptome analysis,chicken embryo,epithelial cells,nutrient transport,lipoproteins,cytoskeleton,erythropoiesis

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