Gene expression networks underlying ovarian development in wild largemouth bass (Micropterus salmoides)

Oocyte maturation in fish involves numerous cell signaling cascades that are activated or inhibited during specific stages of oocyte development. The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild fe...

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Veröffentlicht in:PloS one 2013-03, Vol.8 (3), p.e59093
Hauptverfasser: Martyniuk, Christopher J, Prucha, Melinda S, Doperalski, Nicholas J, Antczak, Philipp, Kroll, Kevin J, Falciani, Francesco, Barber, David S, Denslow, Nancy D
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container_start_page e59093
container_title PloS one
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creator Martyniuk, Christopher J
Prucha, Melinda S
Doperalski, Nicholas J
Antczak, Philipp
Kroll, Kevin J
Falciani, Francesco
Barber, David S
Denslow, Nancy D
description Oocyte maturation in fish involves numerous cell signaling cascades that are activated or inhibited during specific stages of oocyte development. The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation. Transcriptomic analysis was performed on eight morphologically diverse stages of the ovary, including primary and secondary stages of oocyte growth, ovulation, and atresia. Ovary histology, plasma vitellogenin, 17β-estradiol, and testosterone were also measured to correlate with gene networks. Global expression patterns revealed dramatic differences across ovarian development, with 552 and 2070 genes being differentially expressed during both ovulation and atresia respectively. Gene set enrichment analysis (GSEA) revealed that early primary stages of oocyte growth involved increases in expression of genes involved in pathways of B-cell and T-cell receptor-mediated signaling cascades and fibronectin regulation. These pathways as well as pathways that included adrenergic receptor signaling, sphingolipid metabolism and natural killer cell activation were down-regulated at ovulation. At atresia, down-regulated pathways included gap junction and actin cytoskeleton regulation, gonadotrope and mast cell activation, and vasopressin receptor signaling and up-regulated pathways included oxidative phosphorylation and reactive oxygen species metabolism. Expression targets for luteinizing hormone signaling were low during vitellogenesis but increased 150% at ovulation. Other networks found to play a significant role in oocyte maturation included those with genes regulated by members of the TGF-beta superfamily (activins, inhibins, bone morphogenic protein 7 and growth differentiation factor 9), neuregulin 1, retinoid X receptor, and nerve growth factor family. This study offers novel insight into the gene networks underlying vitellogenesis, ovulation and atresia and generates new hypotheses about the cellular pathways regulating oocyte maturation.
doi_str_mv 10.1371/journal.pone.0059093
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The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation. Transcriptomic analysis was performed on eight morphologically diverse stages of the ovary, including primary and secondary stages of oocyte growth, ovulation, and atresia. Ovary histology, plasma vitellogenin, 17β-estradiol, and testosterone were also measured to correlate with gene networks. Global expression patterns revealed dramatic differences across ovarian development, with 552 and 2070 genes being differentially expressed during both ovulation and atresia respectively. Gene set enrichment analysis (GSEA) revealed that early primary stages of oocyte growth involved increases in expression of genes involved in pathways of B-cell and T-cell receptor-mediated signaling cascades and fibronectin regulation. These pathways as well as pathways that included adrenergic receptor signaling, sphingolipid metabolism and natural killer cell activation were down-regulated at ovulation. At atresia, down-regulated pathways included gap junction and actin cytoskeleton regulation, gonadotrope and mast cell activation, and vasopressin receptor signaling and up-regulated pathways included oxidative phosphorylation and reactive oxygen species metabolism. Expression targets for luteinizing hormone signaling were low during vitellogenesis but increased 150% at ovulation. Other networks found to play a significant role in oocyte maturation included those with genes regulated by members of the TGF-beta superfamily (activins, inhibins, bone morphogenic protein 7 and growth differentiation factor 9), neuregulin 1, retinoid X receptor, and nerve growth factor family. 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This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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The objectives of this study were to characterize molecular pathways and temporal gene expression patterns throughout a complete breeding cycle in wild female largemouth bass to improve understanding of the molecular sequence of events underlying oocyte maturation. Transcriptomic analysis was performed on eight morphologically diverse stages of the ovary, including primary and secondary stages of oocyte growth, ovulation, and atresia. Ovary histology, plasma vitellogenin, 17β-estradiol, and testosterone were also measured to correlate with gene networks. Global expression patterns revealed dramatic differences across ovarian development, with 552 and 2070 genes being differentially expressed during both ovulation and atresia respectively. Gene set enrichment analysis (GSEA) revealed that early primary stages of oocyte growth involved increases in expression of genes involved in pathways of B-cell and T-cell receptor-mediated signaling cascades and fibronectin regulation. These pathways as well as pathways that included adrenergic receptor signaling, sphingolipid metabolism and natural killer cell activation were down-regulated at ovulation. At atresia, down-regulated pathways included gap junction and actin cytoskeleton regulation, gonadotrope and mast cell activation, and vasopressin receptor signaling and up-regulated pathways included oxidative phosphorylation and reactive oxygen species metabolism. Expression targets for luteinizing hormone signaling were low during vitellogenesis but increased 150% at ovulation. Other networks found to play a significant role in oocyte maturation included those with genes regulated by members of the TGF-beta superfamily (activins, inhibins, bone morphogenic protein 7 and growth differentiation factor 9), neuregulin 1, retinoid X receptor, and nerve growth factor family. This study offers novel insight into the gene networks underlying vitellogenesis, ovulation and atresia and generates new hypotheses about the cellular pathways regulating oocyte maturation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23527095</pmid><doi>10.1371/journal.pone.0059093</doi><tpages>e59093</tpages><oa>free_for_read</oa></addata></record>
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1932-6203
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subjects 17β-Estradiol
Actin
Activation
Adrenergic receptors
Analysis
Animal breeding
Animals
Bass
Bass - genetics
Bass - metabolism
beta Catenin - metabolism
Biology
Breeding
Cascades
Catfish
Cell activation
Cloning
Cluster Analysis
Computational Biology
Correlation analysis
Cytoskeleton
Developmental stages
Eggs
Estradiol
Estrogens - metabolism
Female
Females
Fibronectin
Fish
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Developmental
Gene Regulatory Networks
Gene set enrichment analysis
Genes
Growth differentiation factor 9
Histology
Ictalurus punctatus
Insulin-like growth factors
Integrin alpha5beta1 - metabolism
Lipid metabolism
Luteinizing hormone
Lymphocytes B
Lymphocytes T
Male
Maturation
Metabolism
Micropterus salmoides
Morphology
Natural killer cells
Nerve growth factor
Networks
Neuregulin
Neuregulin 1
Oncorhynchus mykiss
Oocytes
Oogenesis - genetics
Oreochromis niloticus
Ovary - anatomy & histology
Ovary - cytology
Ovary - metabolism
Ovulation
Oxidative phosphorylation
Oxygen
Pathways
Phosphorylation
Physiology
Pituitary (anterior)
Reactive oxygen species
Reproduction - genetics
Salvelinus fontinalis
Sex hormones
Signal Transduction
Signaling
T cell receptors
T-cell receptor
Testosterone
Toxicology
Transforming growth factor-b
Trout
Vasopressin
Vitellogenins - metabolism
Zebrafish
title Gene expression networks underlying ovarian development in wild largemouth bass (Micropterus salmoides)
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