CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy

Cold-inducible RNA-binding protein (CIRBP) has been reported to be involved in various cellular functions by regulating programmed cell death (PCD). However, the specific mechanism and function of CIRBP in regulating mitochondrial autophagy are still unclear. In this study, we found that CIRBP induc...

Full description

Saved in:
Bibliographic Details
Main Authors: Rui Zhang, Yan Cui, Yangyang Pan, Meng Wang, Sijiu Yu, Ruihua Xu, Wenbin Ma, Junqian Wang, Donglan Zhong, Zhengxing Jiao
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Biomolecules
Subjects:
Online Access:https://www.mdpi.com/2218-273X/15/6/759
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849433218217934848
author Rui Zhang
Yan Cui
Yangyang Pan
Meng Wang
Sijiu Yu
Ruihua Xu
Wenbin Ma
Junqian Wang
Donglan Zhong
Zhengxing Jiao
author_facet Rui Zhang
Yan Cui
Yangyang Pan
Meng Wang
Sijiu Yu
Ruihua Xu
Wenbin Ma
Junqian Wang
Donglan Zhong
Zhengxing Jiao
author_sort Rui Zhang
collection DOAJ
description Cold-inducible RNA-binding protein (CIRBP) has been reported to be involved in various cellular functions by regulating programmed cell death (PCD). However, the specific mechanism and function of CIRBP in regulating mitochondrial autophagy are still unclear. In this study, we found that CIRBP induced mitophagy through the AMPK/mTOR pathway to improve the function of yak cumulus cells (YCCs). We observed that low temperatures (32 °C) activated autophagy, increased E2 and P4 secretion, and up-regulated CIRBP expression. CIRBP overexpression activated mitophagy in YCCs, promoted cumulus diffusion, enhanced E2 and P4 synthesis and secretion, and inhibited apoptosis. CIRBP overexpression significantly attenuated the dysfunction of YCCs induced by the inhibition of mitophagy, whereas the activation of mitophagy exerted the same effect as CIRBP overexpression. DOX HCL is an AMPK/mTOR pathway inhibitor. CIRBP overexpression can successfully alleviate the inhibition of mitophagy caused by DOX HCL inhibiting the AMPK/mTOR pathway and can significantly enhance the mitophagy induced by AMPK/mTOR pathway activation in YCCs. Furthermore, we found that the increased expression of CIRBP protein alleviated the apoptosis caused by AKT pathway activation. In summary, CIRBP promoted mitophagy by activating AMPK/mTOR pathway, thereby promoting the synthesis and secretion of steroid hormones and cumulus diffusion in YCCs and enhancing YCCs survival through activating autophagy and AKT signaling pathway, and then improve the function of YCCs. Our research provided new perspectives on CIRBP’s regulation of cell death and highlighted its potential role in female reproductive systems.
format Article
id doaj-art-46f99e4385ac41afac980823e2a0cb65
institution Kabale University
issn 2218-273X
language English
publishDate 2025-05-01
publisher MDPI AG
record_format Article
series Biomolecules
spelling doaj-art-46f99e4385ac41afac980823e2a0cb652025-08-20T03:27:09ZengMDPI AGBiomolecules2218-273X2025-05-0115675910.3390/biom15060759CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated MitophagyRui Zhang0Yan Cui1Yangyang Pan2Meng Wang3Sijiu Yu4Ruihua Xu5Wenbin Ma6Junqian Wang7Donglan Zhong8Zhengxing Jiao9College of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCollege of Veterinary Medicine, Gansu Agricultural University, Lanzhou 730000, ChinaCold-inducible RNA-binding protein (CIRBP) has been reported to be involved in various cellular functions by regulating programmed cell death (PCD). However, the specific mechanism and function of CIRBP in regulating mitochondrial autophagy are still unclear. In this study, we found that CIRBP induced mitophagy through the AMPK/mTOR pathway to improve the function of yak cumulus cells (YCCs). We observed that low temperatures (32 °C) activated autophagy, increased E2 and P4 secretion, and up-regulated CIRBP expression. CIRBP overexpression activated mitophagy in YCCs, promoted cumulus diffusion, enhanced E2 and P4 synthesis and secretion, and inhibited apoptosis. CIRBP overexpression significantly attenuated the dysfunction of YCCs induced by the inhibition of mitophagy, whereas the activation of mitophagy exerted the same effect as CIRBP overexpression. DOX HCL is an AMPK/mTOR pathway inhibitor. CIRBP overexpression can successfully alleviate the inhibition of mitophagy caused by DOX HCL inhibiting the AMPK/mTOR pathway and can significantly enhance the mitophagy induced by AMPK/mTOR pathway activation in YCCs. Furthermore, we found that the increased expression of CIRBP protein alleviated the apoptosis caused by AKT pathway activation. In summary, CIRBP promoted mitophagy by activating AMPK/mTOR pathway, thereby promoting the synthesis and secretion of steroid hormones and cumulus diffusion in YCCs and enhancing YCCs survival through activating autophagy and AKT signaling pathway, and then improve the function of YCCs. Our research provided new perspectives on CIRBP’s regulation of cell death and highlighted its potential role in female reproductive systems.https://www.mdpi.com/2218-273X/15/6/759CIRBPmitophagyapoptosiscumulus diffusionovarian steroid hormones
spellingShingle Rui Zhang
Yan Cui
Yangyang Pan
Meng Wang
Sijiu Yu
Ruihua Xu
Wenbin Ma
Junqian Wang
Donglan Zhong
Zhengxing Jiao
CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
Biomolecules
CIRBP
mitophagy
apoptosis
cumulus diffusion
ovarian steroid hormones
title CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
title_full CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
title_fullStr CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
title_full_unstemmed CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
title_short CIRBP Enhances the Function of Yak Cumulus Cells by Activating AMPK/mTOR-Mediated Mitophagy
title_sort cirbp enhances the function of yak cumulus cells by activating ampk mtor mediated mitophagy
topic CIRBP
mitophagy
apoptosis
cumulus diffusion
ovarian steroid hormones
url https://www.mdpi.com/2218-273X/15/6/759
work_keys_str_mv AT ruizhang cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT yancui cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT yangyangpan cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT mengwang cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT sijiuyu cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT ruihuaxu cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT wenbinma cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT junqianwang cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT donglanzhong cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy
AT zhengxingjiao cirbpenhancesthefunctionofyakcumuluscellsbyactivatingampkmtormediatedmitophagy