Comprehensive analysis of differences in N6‐methyladenosine RNA methylomes in the rat adenohypophysis after GnRH treatment

Wang, Hao-Qi; Zhang, Jiabao; Zheng, Yi; Zhang, Weidi; Guo, Haixiang; Cong, Shuang; Ding, Yulong; Yuan, Bao

doi:10.1096/fj.202101608r

Cited by 6 publications

(5 citation statements)

References 46 publications

(94 reference statements)

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“…GnRH is involved in the regulation of the entire hypothalamic–pituitary–gonadal axis and plays an important role in reproductive regulation [ 44 ]. Our previous research revealed significant differences in methylation levels in the adenohypophyses of rats after GnRH treatment [ 24 ]. In addition, 14 circRNAs were found to be significantly differentially expressed in the rat adenohypophysis [ 22 ].…”

Section: Discussionmentioning

confidence: 99%

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Sequencing of the Pituitary Transcriptome after GnRH Treatment Uncovers the Involvement of lncRNA-m23b/miR-23b-3p/CAMK2D in FSH Synthesis and Secretion

Zhao

Song

Zheng

et al. 2023

Genes

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The pituitary gland is a key participant in the hypothalamic–pituitary–gonadal axis, as it secretes a variety of hormones and plays an important role in mammalian reproduction. Gonadotrophin-releasing hormone(GnRH) signaling molecules can bind to GnRH receptors on the surfaces of adenohypophysis gonadotropin cells and regulate the expression of follicle-stimulating hormone(FSH) and luteinizing hormone(LH) through various pathways. An increasing number of studies have shown that noncoding RNAs mediate the regulation of GnRH signaling molecules in the adenohypophysis. However, the expression changes and underlying mechanisms of genes and noncoding RNAs in the adenohypophysis under the action of GnRH remain unclear. In the present study, we performed RNA sequencing (RNA-seq) of the rat adenohypophysis before and after GnRH treatment to identify differentially expressed mRNAs, lncRNAs, and miRNAs. We found 385 mRNAs, 704 lncRNAs, and 20 miRNAs that were significantly differentially expressed in the rat adenohypophysis. Then, we used a software to predict the regulatory roles of lncRNAs as molecular sponges that compete with mRNAs to bind miRNAs, and construct a GnRH-mediated ceRNA regulatory network. Finally, we enriched the differentially expressed mRNAs, lncRNA target genes, and ceRNA regulatory networks to analyze their potential roles. Based on the sequencing results, we verified that GnRH could affect FSH synthesis and secretion by promoting the competitive binding of lncRNA-m23b to miR-23b-3p to regulate the expression of Calcium/Calmodulin Dependent Protein Kinase II Delta(CAMK2D). Our findings provide strong data to support exploration of the physiological processes in the rat adenohypophysis under the action of GnRH. Furthermore, our profile of lncRNA expression in the rat adenohypophysis provides a theoretical basis for research on the roles of lncRNAs in the adenohypophysis.

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Section: Discussionmentioning

confidence: 99%

“…The rat is a common experimental animal model for research on the effect of GnRH on the pituitary gland. Various studies have used rat experimental animal models to explore the expression changes of gonadotropins in the adenohypophysis after a GnRH treatment [ 22 , 23 , 24 ].…”

Section: Introductionmentioning

confidence: 99%

Sequencing of the Pituitary Transcriptome after GnRH Treatment Uncovers the Involvement of lncRNA-m23b/miR-23b-3p/CAMK2D in FSH Synthesis and Secretion

Zhao

Song

Zheng

et al. 2023

Genes

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“…Impaired steroid production and release in D. melanogaster prothoracic glands leads to developmental delay and precocity [ 46 ]. In mammals, the potential role of m6A modification in the regulation of reproductive hormone secretion was found to be linked with steroid biosynthetic processes [ 47 ]. On the other hand, the mobilization of energy is tightly coupled to a variety of metabolic pathways, in which the fat body coordinates insect growth with metamorphosis or reproduction by storing or releasing key elements associated with these events [ 48 ].…”

Section: Discussionmentioning

confidence: 99%

Functional Characterization of Two RNA Methyltransferase Genes METTL3 and METTL14 Uncovers the Roles of m6A in Mediating Adaptation of Plutella xylostella to Host Plants

Wang

Lai

et al. 2022

IJMS

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N6-methyladenosine (m6A) is one of the major epigenetic modifications in eukaryotes. Although increasing functions of m6A have been identified in insects, its role in Plutella xylostella L. for host plant adaptation remains unclear. In the current study, we show that the m6A content of P. xylostella was relatively low in different developmental stages and tissues, with no significant differences. Two RNA methyltransferase genes, PxMETTL3 (methyltransferase-like 3) and PxMETTL14 (methyltransferase-like 14), were identified and characterized. PxMETTL3 could be transcribed into two transcripts, and PxMETTL14 had only one transcript; both of these genes were highly expressed in egg and adult stages and reproductive tissues. The CRISPR/Cas9-mediated knockout of PxMETTL3 (ΔPxMETTL3-2) or PxMETTL14 (ΔPxMETTL14-14) confirmed their function in m6A installation into RNA. Furthermore, upon transfer from an artificial diet to the host plant, the mutant strains were affected in terms of larval and pupal weight or adult emergence rate, while the wildtype (WT) strain did not exhibit any difference. In addition, the fecundity and egg hatching rate of the WT strain decreased significantly, whereas only the ΔPxMETTL14-14 mutant strain displayed significantly decreased fecundity. There seemed to be a tradeoff between the stress adaptation and reproduction in P. xylostella mediated by m6A modification. During host transfer, the expression of PxMETTL14 was consistent with the change in m6A content, which implied that PxMETTL14 could respond to host plant defense effectively, and may regulate m6A content. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis of the differentially expressed transcripts with changes in m6A levels revealed that the potential functions of m6A-related genes may be involved in steroid biosynthesis for larval performance and metabolic pathways for adult reproduction. Overall, our work reveals an epigenetic regulation mechanism for the rapid adaptation of P. xylostella to variations in the host environment.

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“…Adenohypophysis tissue and blood were collected 10 min after the second treatment for subsequent experiments. The specific protocol was described in detail in our previous research [ 32 , 50 ].…”

Section: Methodsmentioning

confidence: 99%

Integrative Proteomics and Phosphoproteomics Analysis of the Rat Adenohypophysis after GnRH Treatment

Wang

Yuan

Zhao

et al. 2023

IJMS

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The regulation of mammalian reproductive activity is tightly dependent on the HPG axis crosstalk, in which several reproductive hormones play important roles. Among them, the physiological functions of gonadotropins are gradually being uncovered. However, the mechanisms by which GnRH regulates FSH synthesis and secretion still need to be more extensively and deeply explored. With the gradual completion of the human genome project, proteomes have become extremely important in the fields of human disease and biological process research. To explore the changes of protein and protein phosphorylation modifications in the adenohypophysis after GnRH stimulation, proteomics and phosphoproteomics analyses of rat adenohypophysis after GnRH treatment were performed by using TMT markers, HPLC classification, LC/MS, and bioinformatics analysis in this study. A total of 6762 proteins and 15,379 phosphorylation sites contained quantitative information. Twenty-eight upregulated proteins and fifty-three downregulated proteins were obtained in the rat adenohypophysis after GnRH treatment. The 323 upregulated phosphorylation sites and 677 downregulated phosphorylation sites found in the phosphoproteomics implied that a large number of phosphorylation modifications were regulated by GnRH and were involved in FSH synthesis and secretion. These data constitute a protein–protein phosphorylation map in the regulatory mechanism of “GnRH-FSH,” which provides a basis for future studies on the complex molecular mechanisms of FSH synthesis and secretion. The results will be helpful for understanding the role of GnRH in the development and reproduction regulated by the pituitary proteome in mammals.

show abstract

Comprehensive analysis of differences in N6‐methyladenosine RNA methylomes in the rat adenohypophysis after GnRH treatment

Cited by 6 publications

References 46 publications

Sequencing of the Pituitary Transcriptome after GnRH Treatment Uncovers the Involvement of lncRNA-m23b/miR-23b-3p/CAMK2D in FSH Synthesis and Secretion

Sequencing of the Pituitary Transcriptome after GnRH Treatment Uncovers the Involvement of lncRNA-m23b/miR-23b-3p/CAMK2D in FSH Synthesis and Secretion

Functional Characterization of Two RNA Methyltransferase Genes METTL3 and METTL14 Uncovers the Roles of m6A in Mediating Adaptation of Plutella xylostella to Host Plants

Integrative Proteomics and Phosphoproteomics Analysis of the Rat Adenohypophysis after GnRH Treatment

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