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Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis.

ABSTRACT: Folliculogenesis is a complex biological process involving a central oocyte and its surrounding somatic cells. Three-dimensional chromatin architecture is an important transcription regulator; however, little is known about its dynamics and role in transcriptional regulation of granulosa cells during chicken folliculogenesis. We investigate the transcriptomic dynamics of chicken granulosa cells over ten follicular stages and assess the chromatin architecture dynamics and how it influences gene expression in granulosa cells at three key stages: the prehierarchical small white follicles, the first largest preovulatory follicles, and the postovulatory follicles. Our results demonstrate the consistency between the global reprogramming of chromatin architecture and the transcriptomic divergence during folliculogenesis, providing ample evidence for compartmentalization rearrangement, variable organization of topologically associating domains, and rewiring of the long-range interaction between promoter and enhancers. These results provide key insights into avian reproductive biology and provide a foundational dataset for the future in-depth functional characterization of granulosa cells.

SUBMITTER: Li D

PROVIDER: S-EPMC8748434 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis.

Li Diyan D Ning Chunyou C Zhang Jiaman J Wang Yujie Y Tang Qianzi Q Kui Hua H Wang Tao T He Mengnan M Jin Long L Li Jing J Lin Yu Y Zeng Bo B Yin Huadong H Zhao Xiaoling X Zhang Yao Y Xu Huailiang H Zhu Qing Q Li Mingzhou M

Nature communications 20220110 1

Folliculogenesis is a complex biological process involving a central oocyte and its surrounding somatic cells. Three-dimensional chromatin architecture is an important transcription regulator; however, little is known about its dynamics and role in transcriptional regulation of granulosa cells during chicken folliculogenesis. We investigate the transcriptomic dynamics of chicken granulosa cells over ten follicular stages and assess the chromatin architecture dynamics and how it influences gene e ...[more]

PMID: 35013308

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Project description:In this study, we aimed to better understand the difference between the functions of the two types of granulosa cells and sought to discover more key genes involved in follicle development and follicle selection. Herein, we separately collected pre-hierarchical follicle granulosa cells (PHGCs) and preovulatory follicle granulosa cells (POGCs) for RNA extraction; the transcriptomes of the two groups were compared via RNA-seq. A total of 5273 differentially expressed genes (DEGs) were identified between the PHGCs and POGCs; 2797 genes were up-regulated and 2476 were down-regulated in the PHGCs compared with the POGCs. A qPCR analysis confirmed that the expression patterns of 16 randomly selected DEGs were highly consistent with the RNA-seq results. In the POGCs, many of the genes with the most significant increase in expression were related to steroid hormone synthesis. In addition, the genes with the most significant decline in expression, including AMH and WT1, were related to the inhibition of steroid hormone synthesis. These results suggest that steroid hormones play a key role in follicle development. Furthermore, a Gene Ontology (GO) analysis revealed that these DEGs were mainly involved in the primary metabolic process, the carbohydrate metabolic process, the cellular process, ribosomes, the cytoplasm, and intracellular processes. A Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that the DEGs were mainly enriched in steroid biosynthesis, the cell cycle, ribosomes, the TGF-beta signaling pathway, focal adhesion, and so on. We also observed the morphology of the follicles at different developmental stages, and the results showed that the thickness of the granular layer of the small yellow follicles (SYFs) decreased significantly with further development. In addition, we also found that the thickness of the granulosa layer of hens over 300 days old was significantly lower than that of 200-day-old hens. In short, these data indicate that the tissue morphology and function of granulosa cells change throughout follicle development.

Project description:BackgroundThe major function of the ovary is to produce oocytes for fertilisation. Oocytes mature in follicles surrounded by nurturing granulosa cells and all are enclosed by a basal lamina. During growth, granulosa cells replicate and a large fluid-filled cavity (the antrum) develops in the centre. Only follicles that have enlarged to over 10 mm can ovulate in cows. In mammals, the number of primordial follicles far exceeds the numbers that ever ovulate and atresia or regression of follicles is a mechanism to regulate the number of oocytes ovulated and to contribute to the timing of ovulation. To better understand the molecular basis of follicular atresia, we undertook transcriptome profiling of granulosa cells from healthy (n = 10) and atretic (n = 5) bovine follicles at early antral stages (< 5 mm).ResultsPrincipal Component Analysis (PCA) and hierarchical classification of the signal intensity plots for the arrays showed primary clustering into two groups, healthy and atretic. These analyses and size-frequency plots of coefficients of variation of signal intensities revealed that the healthy follicles were more heterogeneous. Examining the differentially-expressed genes the most significantly affected functions in atretic follicles were cell death, organ development, tissue development and embryonic development. The overall processes influenced by transcription factor gene TP53 were predicted to be activated, whereas those of MYC were inhibited on the basis of known interactions with the genes in our dataset. The top ranked canonical pathway contained signalling molecules common to various inflammatory/fibrotic pathways such as the transforming growth factor-β and tumour necrosis factor-α pathways. The two most significant networks also reflect this pattern of tissue remodelling/fibrosis gene expression. These networks also contain molecules which are present in the canonical pathways of hepatic fibrosis/hepatic stellate cell activation and transforming growth factor-β signalling and were up regulated.ConclusionsSmall healthy antral follicles, which have a number of growth outcomes, exhibit greater variability in gene expression, particularly in genes associated with cell division and other growth-related functions. Atresia, on the other hand, not only involves cell death but clearly is an active process similar to wound healing.

Dataset Information

Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis.

Publications

Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis.

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