Epidermal growth factor differentially regulates activin subunits in the zebrafish ovarian follicle cells via diverse signaling pathways

Chung, Chi-kin; Ge, Wei

doi:10.1016/j.mce.2012.03.022

Cited by 19 publications

(25 citation statements)

References 62 publications

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“…Although our results suggest an early activation of PKCδ by δ receptors upstream of the metalloproteinase‐dependent EGFR transactivation, our findings do not exclude the involvement of PKCδ activity in ERK1/2 activation downstream of EGFR transactivation, because EGFRs have also been shown to regulate PKC activity (Yarden and Sliwkowski, ; Woods and Johnson, ; Chung and Ge, ). Thus, we next determined whether PKCδ contributed to the activation of ERK1/2 only by acting upstream of the transactivation of EGFR and not by acting downstream of EGFR.…”

Section: Resultscontrasting

confidence: 72%

Role for engagement of β‐arrestin2 by the transactivated EGFR in agonist‐specific regulation of δ receptor activation of ERK1/2

Zhang

Wang

et al. 2015

British J Pharmacology

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BACKGROUND AND PURPOSEβ-Arrestins function as signal transducers linking GPCRs to ERK1/2 signalling either by scaffolding members of ERK1/2s cascades or by transactivating receptor tyrosine kinases through Src-mediated release of transactivating factor. Recruitment of β-arrestins to the activated GPCRs is required for ERK1/2 activation. Our previous studies showed that δ receptors activate ERK1/2 through a β-arrestin-dependent mechanism without inducing β-arrestin binding to the δ receptors. However, the precise mechanisms involved remain to be established. EXPERIMENTAL APPROACHERK1/2 activation by δ receptor ligands was assessed using HEK293 cells in vitro and male Sprague Dawley rats in vivo. Immunoprecipitation, immunoblotting, siRNA transfection, intracerebroventricular injection and immunohistochemistry were used to elucidate the underlying mechanism. KEY RESULTSWe identified a new signalling pathway in which recruitment of β-arrestin2 to the EGFR rather than δ receptor was required for its role in δ receptor-mediated ERK1/2 activation in response to H-Tyr-Tic-Phe-Phe-OH (TIPP) or morphine stimulation. Stimulation of the δ receptor with ligands leads to the phosphorylation of PKCδ, which acts upstream of EGFR transactivation and is needed for the release of the EGFR-activating factor, whereas β-arrestin2 was found to act downstream of the EGFR transactivation. Moreover, we demonstrated that coupling of the PKCδ/EGFR/β-arrestin2 transactivation pathway to δ receptor-mediated ERK1/2 activation was ligand-specific and the Ser 363 of δ receptors was crucial for ligand-specific implementation of this ERK1/2 activation pathway. CONCLUSIONS AND IMPLICATIONSThe δ receptor-mediated activation of ERK1/2 is via ligand-specific transactivation of EGFR. This study adds new insights into the mechanism by which δ receptors activate ERK1/2.Abbreviations DPDPE, [D-Pen2, D-Pen5] enkephalin; HB-EGF, heparin-binding EGF-like growth factor; IGFR, insulin-like growth factor receptor; NG108-15, cell mouse neuroblastoma x rat glioma hybrid cell; RTK, receptor tyrosine kinase; TIPP, H-Tyr-Tic-PhePhe-OH

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Section: Resultscontrasting

confidence: 72%

Role for engagement of β‐arrestin2 by the transactivated EGFR in agonist‐specific regulation of δ receptor activation of ERK1/2

Zhang

Wang

et al. 2015

British J Pharmacology

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“…This happened when the body weight reached 100 mg or standard body length above 1.8 cm, suggesting a role for the somatotrophic or growth axis in activating the reproductive axis ( 7 ), similar to the situation in salmons ( 10 ) and mammals ( 21 ). By using candidate gene approach, a variety of genes especially growth factors and their receptors have been shown to display differential expression patterns during the PG-PV transition in zebrafish, including activin-inhibin-follistatin family ( 22 , 23 ), transforming growth factor β (TGF-β) family ( 24 ), bone morphogenetic protein (BMP) family ( 25 – 28 ), epidermal growth factor (EGF) family ( 29 – 31 ), insulin-like growth factor (IGF) family ( 32 – 34 ), Kit family ( 35 ), and anti-Müllerian hormone (AMH) ( 36 ). The candidate gene approach has recently been boosted by the emergence of powerful genome editing technologies such as TALEN and CRISPR/Cas9.…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic Analysis for Differentially Expressed Genes in Ovarian Follicle Activation in the Zebrafish

et al. 2018

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In teleosts, the onset of puberty in females is marked by the appearance of the first wave of pre-vitellogenic (PV) follicles from the pool of primary growth (PG) follicles (follicle activation) in the ovary during sexual maturation. To understand the mechanisms underlying follicle activation and therefore puberty onset, we undertook this transcriptomic study to investigate gene expression profiles in the event. Our analysis revealed a total of 2,027 up-regulated and 859 down-regulated genes during the PG-PV transition. Gene Ontology (GO) analysis showed that in addition to basic cellular functions such as gene transcription, cell differentiation, and cell migration, other biological processes such as steroidogenesis, cell signaling and angiogenesis were also enriched in up-regulated genes; by comparison, some processes were down-regulated including piRNA metabolism, gene silencing and proteolysis. Further Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis identified a variety of signaling pathways that might play pivotal roles in PG-PV transition, including MAPK, TGF-β, Hedgehog, FoxO, VEGF, Jak-STAT, and phosphatidylinositol signaling pathways. Other pathways of particular interest included endocytosis and glycosaminoglycan biosynthesis. We also analyzed expression changes of genes expressed in different compartments viz. oocytes and follicle cells. Interestingly, most oocyte-specific genes remained unchanged in expression during follicle activation whereas a great number of genes specifically expressed in the follicle cells showed significant changes in expression. Overall, this study reported a comprehensive analysis for genes, biological processes and pathways involved in follicle activation, which also marks female puberty onset in the zebrafish when occurring for the first time in sexual maturation.

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“…This pathway has been well studied in vertebrates and shown to regulate follicle development and oocyte maturation (63–67). In fish, the MAPK pathway has been suggested to mediate the actions of various hormones and growth factors in the ovary, such as regulation of steroid production (68, 69) and activin/inhibin subunit expression (70), as well as oocyte maturation (53, 71). Interestingly, analyses of zebrafish ovarian transcriptomes revealed that the MAPK pathway was also strongly regulated when follicles transitioned from stage I to stage II (72) and most strongly affected by β-diketone antibiotics, which have toxic effects in the reproductive system (73).…”

Section: Discussionmentioning

confidence: 99%

“…Many studies have shown that ligands, receptors, and downstream signaling molecules of the TGF-β superfamily are expressed in the zebrafish ovary (76, 77) and that this pathway is involved in early follicle development, follicle growth, and oocyte maturation in zebrafish (10, 70, 78–80). Among the TGF-β family members, activin has potent effects on promoting maturational competency and oocyte maturation (8, 10) while TGF-β1 inhibits oocyte maturation (43, 78, 81).…”

Section: Discussionmentioning

confidence: 99%

Identification of Novel MicroRNAs and Characterization of MicroRNA Expression Profiles in Zebrafish Ovarian Follicular Cells

Zayed

Peng

2019

Front. Endocrinol.

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MicroRNAs (miRNAs) are small non-coding RNAs that regulate gene expression primarily at the post-transcriptional levels and thereby play important roles in regulating many physiological and developmental processes. Oocyte maturation in fish is induced by hormones produced from the hypothalamus, pituitary, and ovary. Gonadotropin-releasing hormone (GnRH) stimulates the secretion of luteinizing hormone (LH), which in turn, induces the secretion of maturation-inducing hormone (MIH) from the ovary. It is documented that small early vitellogenic (or stage IIIa) follicles are unable to undergo oocyte maturation whereas oocytes in mid- to late vitellogenic (stage IIIb) follicles can be induced by LH and MIH to become mature. To determine whether miRNAs may be involved in the growth and acquisition of maturational competency of ovarian follicles, we determined the miRNA expression profiles in follicular cells collected from stage IIIa and IIIb follicles using next-generation sequencing. It was found that miRNAs are abundantly expressed in the follicular cells from both stages IIIa and IIIb follicles. Furthermore, bioinformatics analysis revealed the presence of 214 known, 31 conserved novel and 44 novel miRNAs in zebrafish vitellogenic ovarian follicular cells. Most mature miRNAs in follicular cells were found to be in the length of 22 nucleotides. Differential expression analysis revealed that 11 miRNAs were significantly up-regulated, and 13 miRNAs were significantly down-regulated in the stage IIIb follicular cells as compared with stage IIIa follicular cells. The expression of four of the significantly regulated miRNAs, dre-miR-22a-3p, dre-miR-16a, dre-miR-181a-3p, and dre-miR-29a, was validated by real-time PCR. Finally, gene enrichment and pathway analyses of the predicted targets of the significantly regulated miRNAs supported the involvement of several key signaling pathways in regulating ovarian function, including oocyte maturation. Taken together, this study identifies novel zebrafish miRNAs and characterizes miRNA expression profiles in somatic cells within the zebrafish ovarian follicles. The differential expression of miRNAs between stage IIIa and IIIb follicular cells suggests that these miRNAs are important regulators of zebrafish ovarian follicle development and/or oocyte maturation.

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Epidermal growth factor differentially regulates activin subunits in the zebrafish ovarian follicle cells via diverse signaling pathways

Cited by 19 publications

References 62 publications

Role for engagement of β‐arrestin2 by the transactivated EGFR in agonist‐specific regulation of δ receptor activation of ERK1/2

Role for engagement of β‐arrestin2 by the transactivated EGFR in agonist‐specific regulation of δ receptor activation of ERK1/2

Transcriptomic Analysis for Differentially Expressed Genes in Ovarian Follicle Activation in the Zebrafish

Identification of Novel MicroRNAs and Characterization of MicroRNA Expression Profiles in Zebrafish Ovarian Follicular Cells

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