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Whole-transcriptome analysis of atrophic ovaries in broody chickens reveals regulatory pathways associated with proliferation and apoptosis.

ABSTRACT: Broodiness in laying hens results in atrophy of the ovary and consequently decreases productivity. However, the regulatory mechanisms that drive ovary development remain elusive. Thus, we collected atrophic ovaries (AO) from 380-day-old broody chickens (BC) and normal ovaries (NO) from even-aged egg-laying hens (EH) for RNA sequencing. We identified 3,480 protein-coding transcripts that were differentially expressed (DE), including 1,719 that were down-regulated and 1,761 that were up-regulated in AO. There were 959 lncRNA transcripts that were DE, including 56 that were down-regulated and 903 that were up-regulated. Among the116 miRNAs that were DE, 79 were down-regulated and 37 were up-regulated in AO. Numerous DE protein-coding transcripts and target genes for miRNAs/lncRNAs were significantly enriched in reproductive processes, cell proliferation, and apoptosis pathways. A miRNA-intersection gene-pathway network was constructed by considering target relationships and correlation of the expression levels between ovary development-related genes and miRNAs. We also constructed a competing endogenous RNA (ceRNA) network by integrating competing relationships between protein-coding genes and lncRNA transcripts, and identified several lncRNA transcripts predicted to regulate the CASP6, CYP1B1, GADD45, MMP2, and SMAS2 genes. In conclusion, we discovered protein-coding genes, miRNAs, and lncRNA transcripts that are candidate regulators of ovary development in broody chickens.

SUBMITTER: Liu L

PROVIDER: S-EPMC5940789 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Whole-transcriptome analysis of atrophic ovaries in broody chickens reveals regulatory pathways associated with proliferation and apoptosis.

Liu Lingbin L Xiao Qihai Q Gilbert Elizabeth R ER Cui Zhifu Z Zhao Xiaoling X Wang Yan Y Yin Huadong H Li Diyan D Zhang Haihan H Zhu Qing Q

Scientific reports 20180508 1

Broodiness in laying hens results in atrophy of the ovary and consequently decreases productivity. However, the regulatory mechanisms that drive ovary development remain elusive. Thus, we collected atrophic ovaries (AO) from 380-day-old broody chickens (BC) and normal ovaries (NO) from even-aged egg-laying hens (EH) for RNA sequencing. We identified 3,480 protein-coding transcripts that were differentially expressed (DE), including 1,719 that were down-regulated and 1,761 that were up-regulated ...[more]

PMID: 29739971

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Project description:BackgroundThe yak (Bos grunniens) is an important livestock species that can survive the extremely cold, harsh, and oxygen-poor conditions of the Qinghai-Tibetan Plateau and provide meat, milk, and transportation for the Tibetans living there. However, the regulatory network that drive this hypoxic adaptation remain elusive.ResultsThe heart tissues from LeiRoqi (LWQY) yak and their related cattle (Bos Taurus) breeds, which are two native cattle breeds located in high altitude (HAC) and low altitude (LAC) regions, respectively, were collected for RNA sequencing. A total of 178 co-differentially expressed protein-coding transcripts (co-DETs) were discovered in each of the LAC-vs-LWQY and LAC-vs-HAC comparison groups, including NFATC2, NFATC1, ENPP2, ACSL4, BAD, and many other genes whose functions were reported to be associated with the immune-system, endocrine-system, and lipid metabolism. Two and 230 lncRNA transcripts were differentially expressed in the LAC-vs-LWQY and LAC-vs-HAC comparisons' respectively, but no lncRNA transcripts that were co-differentially expressed. Among the 58 miRNAs that were co-differentially expressed, 18 were up-regulated and 40 were down-regulated. In addition, 640 (501 up-regulated and 139 down-regulated) and 152 (152 up-regulated and one down-regulated) circRNAs showed differential expression in LAC-vs-LWQY and LAC-vs-HAC comparison groups, respectively, and 53 up-regulated co-differentially expressed circRNAs were shared. Multiple co-DETs, which are the targets of miRNAs/lncRNAs, are significantly enriched in high-altitude adaptation related processes, such as, T cell receptor signaling, VEGF signaling, and cAMP signaling. A competing endogenous RNA (ceRNA) network was constructed by integrating the competing relationships among co-differentially expressed mRNAs, miRNAs, lncRNAs and circRNAs. Furthermore, the hypoxic adaptation related ceRNA network was constructed, and the six mRNAs (MAPKAPK3, PXN, NFATC2, ATP7A, DIAPH1, and F2R), the eight miRNAs (including miR-195), and 15 circRNAs (including novel-circ-017096 and novel-circ-018073) are proposed as novel and promising candidates for regulation of hypoxic adaptation in the heart.ConclusionIn conclusion, the data recorded in the present study provides new insights into the molecular network of high-altitude adaptation along with more detailed information of protein-coding transcripts and non-coding transcripts involved in this physiological process, the detailed mechanisms behind how these transcripts "crosstalk" with each other during the plateau adaptation are worthy of future research efforts.

Project description:Chicken atrophic ovaries have decreased volume and are indicative of ovarian failure, presence of a tumor, or interrupted ovarian blood supply. Ovarian tumor is accompanied by an increase in follicular atresia, granulosa cell (GC) apoptosis, and autophagy. In a previous study, we found using high throughput sequencing that miR-204 is highly expressed in chicken atrophic ovaries. Thus, in the present study, we further investigated its function in GC apoptosis and autophagy. We found that overexpression of miR-204 reduced mRNA and protein levels of proliferation-related genes and increased apoptosis-related genes. Cell counting kit-8 (CCK-8), 5-ethynyl-2-deoxyuridine (EdU), and flow cytometry assays revealed that miR-204 inhibited GC proliferation and promoted apoptosis. Furthermore, we confirmed with reporter gene assays that Forkhead box K2 (FOXK2) was directly targeted by miR-204. FOXK2, as a downstream regulator of phosphoinositide 3-kinase (PI3K)/AKT/mammalian target of rapamycin (mTOR) signal pathways, promoted GC proliferation and inhibited apoptosis. Subsequently, we observed that miR-204 was involved in GC autophagy by targeting Transient Receptor Potential Melastatin 3 (TRPM3). The luciferase activities of the two binding sites of TRPM3 were decreased in response to treatment with a miR-204 mimic, and the autophagic flux was increased after miR-204 inhibition. However, overexpression of miR-204 had opposite results in autophagosomes and autolysosomes. miR-204 inhibits GC autophagy by suppressing the protein expression of TRPM3/AMP-activated protein kinase (AMPK)/ULK signaling pathway components. Inhibition of miR-204 enhanced autophagy by accumulating and degrading the protein levels of LC3-II (Microtubule Associated Protein Light Chain 3B) and p62 (Protein of 62 kDa), respectively, whereas miR-204 overexpression was associated with contrary results. Immunofluorescence staining showed that there was a significant reduction in the fluorescent intensity of LC3B, whereas p62 protein was increased after TRPM3 silencing. Collectively, our results indicate that miR-204 is highly expressed in chicken atrophic ovaries, which promotes GC apoptosis via repressing FOXK2 through the PI3K/AKT/mTOR pathway and inhibits autophagy by impeding the TRPM3/AMPK/ULK pathway.

Dataset Information

Whole-transcriptome analysis of atrophic ovaries in broody chickens reveals regulatory pathways associated with proliferation and apoptosis.

Publications

Whole-transcriptome analysis of atrophic ovaries in broody chickens reveals regulatory pathways associated with proliferation and apoptosis.

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