Regulation of miR-101/miR-199a-3p by the epithelial sodium channel during embryo implantation: involvement of CREB phosphorylation

Sun, Xiao; Ruan, Ye Chun; Guo, Jing; Chen, Hui; Tsang, Lai Ling; Zhang, Xiao Hu; Jiang, Xiaohua; Chan, Hsiao Chang

doi:10.1530/rep-14-0386

Cited by 35 publications

(34 citation statements)

References 52 publications

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“…Of note, we and others have also shown previously that PGE 2 exhibited similar role in mediating epithelial regulation of smooth muscles in other organ systems (Ruan et al, 2008(Ruan et al, , 2011. Interestingly, we have also shown previously that during embryo implantation, activation of ENaC can inhibit the COX-2 targeting microRNA, miR-199a-3p (Sun et al, 2014), which is reported to play important roles in labor as well (Renthal et al, 2013).…”

Section: Discussionsupporting

confidence: 76%

Activation of the epithelial sodium channel ( EN aC) leads to cytokine profile shift to pro‐inflammatory in labor

et al. 2018

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The shift of cytokine profile from anti- to pro-inflammatory is the most recognizable sign of labor, although the underlying mechanism remains elusive. Here, we report that the epithelial sodium channel (ENaC) is upregulated and activated in the uterus at labor in mice. Mechanical activation of ENaC results in phosphorylation of CREB and upregulation of pro-inflammatory cytokines as well as COX-2/PGE in uterine epithelial cells. ENaC expression is also upregulated in mice with RU486-induced preterm labor as well as in women with preterm labor. Interference with ENaC attenuates mechanically stimulated uterine contractions and significantly delays the RU486-induced preterm labor in mice. Analysis of a human transcriptome database for maternal-fetus tissue/blood collected at onset of human term and preterm births reveals significant and positive correlation of ENaC with labor-associated pro-inflammatory factors in labored birth groups (both term and preterm), but not in non-labored birth groups. Taken together, the present finding reveals a pro-inflammatory role of ENaC in labor at term and preterm, suggesting it as a potential target for the prevention and treatment of preterm labor.

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Section: Discussionsupporting

confidence: 76%

Activation of the epithelial sodium channel ( EN aC) leads to cytokine profile shift to pro‐inflammatory in labor

et al. 2018

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“…These studies suggest that miRs are capable of acting as intermediary components in the aldosterone signaling cascade (Edinger et al, ). Direct regulation of ENaC by miRs has been reported for miR‐16 (Tamarapu Parthasarathy et al, ) and miR‐7 (Qin et al, ) in alveolar epithelial cells and regulation of miR‐101 and ‐199 by ENaC in endometrial cells (Sun et al, ). Neither of these reports focused on miR regulation by hormones, and none of these ENaC‐targeting miRs were significantly altered in response to aldosterone in our microarray assays.…”

Section: Discussionmentioning

confidence: 97%

A MicroRNA Cluster miR‐23–24–27 Is Upregulated by Aldosterone in the Distal Kidney Nephron Where it Alters Sodium Transport

Liu

Edinger

Klemens

et al. 2017

Journal Cellular Physiology

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The epithelial sodium channel (ENaC) is expressed in the epithelial cells of the distal convoluted tubules, connecting tubules, and cortical collecting duct (CCD) in the kidney nephron. Under the regulation of the steroid hormone aldosterone, ENaC is a major determinant of sodium (Na+) and water balance. The ability of aldosterone to regulate microRNAs (miRs) in the kidney has recently been realized, but the role of miRs in Na+ regulation has not been well established. Here we demonstrate that expression of a miR cluster mmu-miR-23–24–27, is upregulated in the CCD by aldosterone stimulation both in vitro and in vivo. Increasing the expression of these miRs increased Na+ transport in the absence of aldosterone stimulation. Potential miR targets were evaluated and miR-27a/b was verified to bind to the 3′-untranslated region of intersectin-2, a multi-domain protein expressed in the distal kidney nephron and involved in the regulation of membrane trafficking. Expression of Itsn2 mRNA and protein was decreased after aldosterone stimulation. Depletion of Itsn2 expression, mimicking aldosterone regulation, increased ENaC-mediated Na+ transport, while Itsn2 overexpression reduced ENaC’s function. These findings reinforce a role for miRs in aldosterone regulation of Na+ transport, and implicate miR-27 in aldosterone’s action via a novel target.

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“…Because in vivo experiments in the pig are difficult to perform, we used an implantation failure mouse model based on other studies focusing on pig or human implantation that used this model (Jiang et al, ; X. Sun et al, ). The day when a vaginal plug was found was designated the first day after mating.…”

Section: Methodsmentioning

confidence: 99%

“…General anesthesia was performed on the mice on Day 3, and the intrauterine injection method used was described in the previous study (X. Sun et al, ). A dorsal midline skin incision was made, followed by two small incisions into the muscle wall near each ovary to expose the uterine‐oviduct connecting region.…”

Section: Methodsmentioning

confidence: 99%

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mRNA/lncRNA expression patterns and the function of fibrinogen‐like protein 2 in Meishan pig endometrium during the preimplantation phases

Wang

Hua

Xue

et al. 2019

Molecular Reproduction Devel

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Embryonic implantation involves a complex and well‐coordinated interaction between the developing conceptus and maternal uterus, and the preimplantation period has a major impact on litter size in pigs. The present study aimed to investigate the vital messenger RNAs (mRNAs) and long noncoding RNAs (lncRNAs) that regulate preimplantation in Meishan pigs. The enriched Gene Ontology terms were all related to “binding.” Furthermore, “ECM‐receptor interaction” was predicted as an important pathway that regulated the success of implantation. We speculated that the differentially expressed mRNAs S100A9, ANXA8, MUC16, and FGL2 and the differentially expressed lncRNAs TCONS_11206566, TCONS_09904861, and TCONS_1252933 may play vital roles in the process of implantation. Furthermore, this study verified that FGL2 was highly expressed on Day 12 of pregnancy, and we also investigated the function of FGL2 during preimplantation in vivo. In conclusion, this study provides useful information for further analyses of the molecular mechanisms of implantation in Chinese domestic pigs.

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Regulation of miR-101/miR-199a-3p by the epithelial sodium channel during embryo implantation: involvement of CREB phosphorylation

Cited by 35 publications

References 52 publications

Activation of the epithelial sodium channel ( EN aC) leads to cytokine profile shift to pro‐inflammatory in labor

Activation of the epithelial sodium channel ( EN aC) leads to cytokine profile shift to pro‐inflammatory in labor

A MicroRNA Cluster miR‐23–24–27 Is Upregulated by Aldosterone in the Distal Kidney Nephron Where it Alters Sodium Transport

mRNA/lncRNA expression patterns and the function of fibrinogen‐like protein 2 in Meishan pig endometrium during the preimplantation phases

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