Exercise-induced irisin improves follicular dysfunction by inhibiting IRE1α-TXNIP/ROS-NLRP3 pathway in PCOS.


Journal

Journal of ovarian research
ISSN: 1757-2215
Titre abrégé: J Ovarian Res
Pays: England
ID NLM: 101474849

Informations de publication

Date de publication:
31 Jul 2023
Historique:
received: 31 10 2022
accepted: 17 07 2023
medline: 2 8 2023
pubmed: 1 8 2023
entrez: 31 7 2023
Statut: epublish

Résumé

Excessive production of androgen drives oxidative stress (OS) and inflammasome activation in ovarian granulosa cells (GCs). Therefore, the induced follicular developmental disorder is the major cause of infertility in women with polycystic ovary syndrome (PCOS). Exercise-induced upregulation of irisin is capable of regulating metabolism by reducing OS and inflammation. Exercise has been shown to alleviate a range of PCOS symptoms, including maintaining a normal menstrual cycle, in several clinical trials. Female Sprague-Dawley (SD) rats and primary ovarian cells were treated with two different androgens, dehydroepiandrosterone (DHEA) and dihydrotestosterone (DHT), to simulate a hyperandrogenic environment, followed by eight weeks of exercise training and irisin intervention. The levels of reactive oxygen species (ROS), tissue inflammation and fibrosis were examined using hematoxylin and eosin (H&E) staining, western blot, quantitative real-time PCR (qRT-PCR), dichlorofluorescein diacetate (DCF-DA) probe detection, immunofluorescence staining, immunohistochemistry, and Sirius red staining. Exercise for eight weeks improved polycystic ovarian morphology and decreased the levels of inflammation, OS, and fibrosis in PCOS rats. Hyperandrogen increased ROS production in ovarian cells by inducing endoplasmic reticulum stress (ERS) and activating the inositol-requiring enzyme 1α (IRE1α)-thioredoxin-interacting protein (TXNIP)/ROS-NOD-like receptor family pyrin domain containing 3 (NLRP3) signaling pathway, further enhancing the levels of inflammation. Irisin suppressed the expression of IRE1α and its downstream targets, thus improving the ovarian dysfunction of PCOS rats induced by hyperandrogen. Exercise can alleviate various phenotypes of PCOS rats induced by DHEA, and its therapeutic effect may be mediated by secreting beneficial myokines. IRE1α may be an important target of irisin for reducing OS and inflammation, thereby improving ovarian fibrosis.

Sections du résumé

BACKGROUND BACKGROUND
Excessive production of androgen drives oxidative stress (OS) and inflammasome activation in ovarian granulosa cells (GCs). Therefore, the induced follicular developmental disorder is the major cause of infertility in women with polycystic ovary syndrome (PCOS). Exercise-induced upregulation of irisin is capable of regulating metabolism by reducing OS and inflammation. Exercise has been shown to alleviate a range of PCOS symptoms, including maintaining a normal menstrual cycle, in several clinical trials.
METHODS METHODS
Female Sprague-Dawley (SD) rats and primary ovarian cells were treated with two different androgens, dehydroepiandrosterone (DHEA) and dihydrotestosterone (DHT), to simulate a hyperandrogenic environment, followed by eight weeks of exercise training and irisin intervention. The levels of reactive oxygen species (ROS), tissue inflammation and fibrosis were examined using hematoxylin and eosin (H&E) staining, western blot, quantitative real-time PCR (qRT-PCR), dichlorofluorescein diacetate (DCF-DA) probe detection, immunofluorescence staining, immunohistochemistry, and Sirius red staining.
RESULTS RESULTS
Exercise for eight weeks improved polycystic ovarian morphology and decreased the levels of inflammation, OS, and fibrosis in PCOS rats. Hyperandrogen increased ROS production in ovarian cells by inducing endoplasmic reticulum stress (ERS) and activating the inositol-requiring enzyme 1α (IRE1α)-thioredoxin-interacting protein (TXNIP)/ROS-NOD-like receptor family pyrin domain containing 3 (NLRP3) signaling pathway, further enhancing the levels of inflammation. Irisin suppressed the expression of IRE1α and its downstream targets, thus improving the ovarian dysfunction of PCOS rats induced by hyperandrogen.
CONCLUSION CONCLUSIONS
Exercise can alleviate various phenotypes of PCOS rats induced by DHEA, and its therapeutic effect may be mediated by secreting beneficial myokines. IRE1α may be an important target of irisin for reducing OS and inflammation, thereby improving ovarian fibrosis.

Identifiants

pubmed: 37525261
doi: 10.1186/s13048-023-01242-x
pii: 10.1186/s13048-023-01242-x
pmc: PMC10388501
doi:

Substances chimiques

Reactive Oxygen Species 0
NLR Family, Pyrin Domain-Containing 3 Protein 0
Endoribonucleases EC 3.1.-
Fibronectins 0
Protein Serine-Threonine Kinases EC 2.7.11.1
Dehydroepiandrosterone 459AG36T1B
TXNIP protein, human 0
Carrier Proteins 0
TXNIP protein, rat 0
Cell Cycle Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

151

Subventions

Organisme : National Natural Science Foundation of China
ID : 81971346
Organisme : Jiangsu Provincial Department of Science and Technology
ID : BE2022755

Informations de copyright

© 2023. The Author(s).

Références

J Endocrinol. 2014 Jul;222(1):R25-38
pubmed: 24781257
J Transl Med. 2020 Feb 17;18(1):84
pubmed: 32066482
Int J Womens Health. 2011 Feb 08;3:25-35
pubmed: 21339935
Chem Biol Interact. 2019 Apr 1;302:11-21
pubmed: 30703374
Cochrane Database Syst Rev. 2011 Feb 16;(2):CD007506
pubmed: 21328294
Cell Death Discov. 2021 Mar 15;7(1):50
pubmed: 33723236
Hum Reprod. 2013 Nov;28(11):3074-85
pubmed: 23980058
Int J Obes (Lond). 2007 Nov;31 Suppl 2:S8-13; discussion S31-2
pubmed: 17968437
J Gynecol Obstet Hum Reprod. 2021 Jun;50(6):101894
pubmed: 32814159
Bonekey Rep. 2016 Jul 20;5:826
pubmed: 27579164
J Cardiovasc Pharmacol. 2018 Dec;72(6):259-269
pubmed: 29979350
Clin Endocrinol (Oxf). 2018 Sep;89(3):251-268
pubmed: 30024653
Nature. 2012 Jan 11;481(7382):463-8
pubmed: 22237023
Int J Mol Sci. 2012 Dec 24;14(1):434-56
pubmed: 23263672
J Ovarian Res. 2018 Jan 10;11(1):6
pubmed: 29321035
J Cell Physiol. 2017 Dec;232(12):3775-3785
pubmed: 28181692
Fertil Steril. 2011 Dec;96(6):1508-13
pubmed: 21962963
J Ovarian Res. 2014 Apr 08;7:37
pubmed: 24708600
J Am Osteopath Assoc. 2020 Apr 14;:
pubmed: 32285088
Nat Rev Endocrinol. 2012 Apr 03;8(8):457-65
pubmed: 22473333
Biol Chem. 2021 Jan 20;402(6):703-715
pubmed: 33951764
Hormones (Athens). 2021 Jun;20(2):339-345
pubmed: 32725588
Fertil Steril. 2011 Jun 30;95(8):2696-9
pubmed: 21324452
Biomolecules. 2019 Jul 31;9(8):
pubmed: 31370285
Endocrine. 2013 Dec;44(3):583-90
pubmed: 23625194
Health Sci Rep. 2020 Dec 04;3(4):e212
pubmed: 33305014
J Phys Ther Sci. 2015 Jul;27(7):2293-7
pubmed: 26311969
Obes Rev. 2011 May;12(5):e202-10
pubmed: 20546140
Exerc Immunol Rev. 2004;10:42-55
pubmed: 15633585
Sci Transl Med. 2017 Nov 29;9(418):
pubmed: 29187642
Sci Total Environ. 2020 Nov 25;745:141049
pubmed: 32758727
Diabetes. 2020 Nov;69(11):2267-2280
pubmed: 32873590
Cell. 2019 Jul 11;178(2):507-508
pubmed: 31299203
J Clin Endocrinol Metab. 2013 Dec;98(12):4565-92
pubmed: 24151290
Hum Reprod. 2008 Sep;23(9):2113-21
pubmed: 18556679
J Clin Endocrinol Metab. 2011 Jan;96(1):E48-56
pubmed: 20926534
Adipocyte. 2013 Oct 1;2(4):289-93
pubmed: 24052909
Dis Model Mech. 2012 May;5(3):293-5
pubmed: 22566556
Appl Microbiol Biotechnol. 2020 Jul;104(14):6129-6140
pubmed: 32447438
Biochim Biophys Acta. 2013 Dec;1833(12):3460-3470
pubmed: 23850759
BMC Endocr Disord. 2020 May 19;20(1):71
pubmed: 32429890

Auteurs

Yajing Weng (Y)

State Key Laboratory of Analytical Chemistry for Life Science & Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, China.

Yaling Zhang (Y)

School of Medicine, Jiaxing University, Jiaxing, 314001, China.

Daojuan Wang (D)

Department of Pain, Medical School, The Affiliated Drum Tower Hospital, Nanjing University, Nanjing, 210008, China.

Rong Wang (R)

State Key Laboratory of Analytical Chemistry for Life Science & Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, China.

Zou Xiang (Z)

Department of Health Technology and Informatics, Hong Kong Polytechnic University, Hong Kong, 999077, China.

Shanmei Shen (S)

Department of Endocrinology, Medical School, The Affiliated Drum Tower Hospital, Nanjing University, Nanjing, 210093, China.

Hongwei Wang (H)

State Key Laboratory of Analytical Chemistry for Life Science & Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, China.

Xiaoke Wu (X)

Department of Obstetrics and Gynecology, First Affiliated Hospital, Heilongjiang University of Chinese Medicine, Harbin, 150040, China. xiaokewu2002@vip.sina.com.

Yanting Wen (Y)

State Key Laboratory of Analytical Chemistry for Life Science & Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, China. wenyanting@nju.edu.cn.

Yong Wang (Y)

State Key Laboratory of Analytical Chemistry for Life Science & Jiangsu Key Laboratory of Molecular Medicine, Medical School, Nanjing University, Nanjing, 210093, China. yongwang@nju.edu.cn.
Nanjing University (Suzhou) High-Tech Institute, Suzhou, 215123, China. yongwang@nju.edu.cn.

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Classifications MeSH