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L. Zhang, L. F. Schütz, C. L. Robinson, M. L. Totty, L. J. Spicer, Evidence that gene expression of ovarian follicular tight junction proteins is regulated in vivo and in vitro in cattle, Journal of Animal Science, Volume 95, Issue 3, March 2017, Pages 1313–1324, https://doi.org/10.2527/jas.2016.0892
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Abstract
Tight junctions (TJ) are common paracellular sealing structures that control the transport of water, ions, and macromolecules across cell layers. Because the role of TJ in bovine follicular development is unknown, we investigated the developmental and hormonal regulation of the transmembrane TJ protein, occludin (OCLN), and the cytoplasmic TJ proteins, TJ protein 1 (TJP1) and cingulin (CGN) in bovine granulosa cells (GC) and theca cells (TC). For this purpose, bovine GC and TC were isolated from large (>8 mm) and/or small (1 to 5 mm) follicles and either extracted for real-time PCR (qPCR) or cultured in vitro. The abundances of both OCLN and TJP1 mRNA were greater (P < 0.05) in TC than GC, whereas the CGN mRNA abundance was greater (P < 0.05) in GC than TC. The abundance of OCLN mRNA in both GC and TC was greater (P < 0.05) in small follicles compared with large follicles, whereas the GC of large follicles had less (P < 0.05) TJP1 mRNA abundance than the GC of small follicles. The abundance of CGN mRNA in GC or TC did not differ (P > 0.10) among follicle sizes. In vitro treatment with various growth factors known to affect ovarian folliculogenesis indicated that CGN, OCLN, and TJP1 were hormonally regulated. Fibroblast growth factor 9 (FGF9) decreased (P < 0.05) the OCLN and CGN mRNA abundances. Tumor necrosis factor α (TNFα) and vascular endothelial growth factor A (VEGFA) increased (P < 0.05) the OCLN mRNA abundance but decreased (P < 0.05) the CGN mRNA abundance. Dexamethasone (DEX) increased (P < 0.05) TJP1 and CGN mRNA abundances. Epidermal growth factor (EGF) decreased (P < 0.05) and dihydrotestosterone (DHT) increased (P < 0.05) the abundances of OCLN, TJP1, and CGN mRNA. We propose that the downregulation of OCLN and other TJ proteins during follicular development could reduce barrier function, thereby participating in increasing follicle size by allowing for an increase in the volume of follicular fluid as well as by allowing additional serum factors into the follicular fluid that potentially may directly impact GC functions. The results of the current study indicate the following in cattle: 1) gene expression of TJ proteins (i.e., OCLN, TJP1, and CGN) differs between GC and TC and changes with follicle size, and 2) autocrine, paracrine, and endocrine regulators, such as FGF9, EGF, DHT, TNFα, and glucocorticoids, modulate OCLN, TJP1, and CGN mRNA abundance in TC in vitro.
