A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression

Abstract Background Endometriosis is an estrogen-dependent chronic inflammatory disease, however the mechanisms underlying inflammation remain unclear. Non-hormonal drugs that can prevent endometriosis progression and resolve endometriotic infertility are urgently required. We thus focused on cellul...

Full description

Saved in:
Bibliographic Details
Main Authors: Reina Sonehara, Tomoko Nakamura, Takehiko Takeda, Satoshi Kaseki, Tomomi Seki, Hideaki Tanaka, Atsushi Yabuki, Natsuki Miyake, Ayako Muraoka, Satoko Osuka, Akira Iwase, Hiroaki Kajiyama
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Reproductive Biology and Endocrinology
Subjects:
Online Access:https://doi.org/10.1186/s12958-025-01381-4
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849391023338291200
author Reina Sonehara
Tomoko Nakamura
Takehiko Takeda
Satoshi Kaseki
Tomomi Seki
Hideaki Tanaka
Atsushi Yabuki
Natsuki Miyake
Ayako Muraoka
Satoko Osuka
Akira Iwase
Hiroaki Kajiyama
author_facet Reina Sonehara
Tomoko Nakamura
Takehiko Takeda
Satoshi Kaseki
Tomomi Seki
Hideaki Tanaka
Atsushi Yabuki
Natsuki Miyake
Ayako Muraoka
Satoko Osuka
Akira Iwase
Hiroaki Kajiyama
author_sort Reina Sonehara
collection DOAJ
description Abstract Background Endometriosis is an estrogen-dependent chronic inflammatory disease, however the mechanisms underlying inflammation remain unclear. Non-hormonal drugs that can prevent endometriosis progression and resolve endometriotic infertility are urgently required. We thus focused on cellular senescence as a novel feature of endometriosis. Senescent cells cause chronic inflammation via the senescence-associated secretory phenotype (SASP) factor. It has been reported the effects of senolysis for various diseases in recent years. The aim of this study was to validate the involvement of cellular senescence in endometriosis and as the effects of senolytic drug to develop a novel non-hormonal therapeutic strategy for endometriosis. Methods The senescence markers were assessed by morphological features and semiquantitative immunofluorescence staining (senescence-associated b-galactosidase [SA-b-Gal], the cyclin-dependent kinase inhibitor 2 A locus [p16INK4a], and laminB1) to compare among cell types (normal endometrial stromal cells [nESCs], endometrial stromal cells with endometriosis [eESCs], and ovarian endometriosis [OE] cyst-derived stromal cells [CSCs]). Expression of SASP markers was examined in cell culture supernatants using a cytokine array. In addition, the effects of senolytic drugs (azithromycin [AZM] and navitoclax [ABT263]) on endometriosis were evaluated in vitro and in vivo. The in vivo study used the endometriosis mice model. Results CSCs exhibited stronger senescence markers. Semi-quantitative SA-β-Gal and p16INK4a staining intensities were significantly increased, and that of LaminB1 was decreased in CSCs compared to those in nESCs and eESCs (SA-b-Gal, P < 0.001; p16INK4a, P < 0.05; LaminB1, P < 0.05). Cytokine array analysis revealed elevated SASP-related cytokine levels, including interleukin-6 (IL-6), in CSC supernatants compared to those in nESCs. AZM and ABT263 reduced the viable fraction in CSCs (AZM: P < 0.001, ABT263: P < 0.01). Furthermore, AZM suppressed IL-6 expression in CSC culture supernatants (P < 0.05). In murine model, AZM administration reduced endometriotic lesion volume compared to that in vehicle (P < 0.05). Proliferative activity, IL-6 expression levels, and fibrosis within endometriotic lesions also decreased (Ki67, P < 0.01; IL-6, P < 0.001; fibrosis, P < 0.001). Conclusions Our findings show that cellular senescence is involved in the pathogenesis of endometriosis and that AZM may be useful for preventing endometriosis progression by suppressing the secretion of IL-6 as a SASP.
format Article
id doaj-art-5e5ac3cc98fb4aa3b30e9cb85c38c4e8
institution Kabale University
issn 1477-7827
language English
publishDate 2025-03-01
publisher BMC
record_format Article
series Reproductive Biology and Endocrinology
spelling doaj-art-5e5ac3cc98fb4aa3b30e9cb85c38c4e82025-08-20T03:41:14ZengBMCReproductive Biology and Endocrinology1477-78272025-03-0123111110.1186/s12958-025-01381-4A novel senotherapeutic strategy with azithromycin for preventing endometriosis progressionReina Sonehara0Tomoko Nakamura1Takehiko Takeda2Satoshi Kaseki3Tomomi Seki4Hideaki Tanaka5Atsushi Yabuki6Natsuki Miyake7Ayako Muraoka8Satoko Osuka9Akira Iwase10Hiroaki Kajiyama11Department of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Maternal and Perinatal Medicine, Nagoya University HospitalDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Maternal and Perinatal Medicine, Nagoya University HospitalDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Maternal and Perinatal Medicine, Nagoya University HospitalDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineDepartment of Obstetrics and Gynecology, Gunma University Graduate School of MedicineDepartment of Obstetrics and Gynecology, Nagoya University Graduate School of MedicineAbstract Background Endometriosis is an estrogen-dependent chronic inflammatory disease, however the mechanisms underlying inflammation remain unclear. Non-hormonal drugs that can prevent endometriosis progression and resolve endometriotic infertility are urgently required. We thus focused on cellular senescence as a novel feature of endometriosis. Senescent cells cause chronic inflammation via the senescence-associated secretory phenotype (SASP) factor. It has been reported the effects of senolysis for various diseases in recent years. The aim of this study was to validate the involvement of cellular senescence in endometriosis and as the effects of senolytic drug to develop a novel non-hormonal therapeutic strategy for endometriosis. Methods The senescence markers were assessed by morphological features and semiquantitative immunofluorescence staining (senescence-associated b-galactosidase [SA-b-Gal], the cyclin-dependent kinase inhibitor 2 A locus [p16INK4a], and laminB1) to compare among cell types (normal endometrial stromal cells [nESCs], endometrial stromal cells with endometriosis [eESCs], and ovarian endometriosis [OE] cyst-derived stromal cells [CSCs]). Expression of SASP markers was examined in cell culture supernatants using a cytokine array. In addition, the effects of senolytic drugs (azithromycin [AZM] and navitoclax [ABT263]) on endometriosis were evaluated in vitro and in vivo. The in vivo study used the endometriosis mice model. Results CSCs exhibited stronger senescence markers. Semi-quantitative SA-β-Gal and p16INK4a staining intensities were significantly increased, and that of LaminB1 was decreased in CSCs compared to those in nESCs and eESCs (SA-b-Gal, P < 0.001; p16INK4a, P < 0.05; LaminB1, P < 0.05). Cytokine array analysis revealed elevated SASP-related cytokine levels, including interleukin-6 (IL-6), in CSC supernatants compared to those in nESCs. AZM and ABT263 reduced the viable fraction in CSCs (AZM: P < 0.001, ABT263: P < 0.01). Furthermore, AZM suppressed IL-6 expression in CSC culture supernatants (P < 0.05). In murine model, AZM administration reduced endometriotic lesion volume compared to that in vehicle (P < 0.05). Proliferative activity, IL-6 expression levels, and fibrosis within endometriotic lesions also decreased (Ki67, P < 0.01; IL-6, P < 0.001; fibrosis, P < 0.001). Conclusions Our findings show that cellular senescence is involved in the pathogenesis of endometriosis and that AZM may be useful for preventing endometriosis progression by suppressing the secretion of IL-6 as a SASP.https://doi.org/10.1186/s12958-025-01381-4EndometriosisCellular senescenceSASPIL-6SenotherapyAzithromycin
spellingShingle Reina Sonehara
Tomoko Nakamura
Takehiko Takeda
Satoshi Kaseki
Tomomi Seki
Hideaki Tanaka
Atsushi Yabuki
Natsuki Miyake
Ayako Muraoka
Satoko Osuka
Akira Iwase
Hiroaki Kajiyama
A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
Reproductive Biology and Endocrinology
Endometriosis
Cellular senescence
SASP
IL-6
Senotherapy
Azithromycin
title A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
title_full A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
title_fullStr A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
title_full_unstemmed A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
title_short A novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
title_sort novel senotherapeutic strategy with azithromycin for preventing endometriosis progression
topic Endometriosis
Cellular senescence
SASP
IL-6
Senotherapy
Azithromycin
url https://doi.org/10.1186/s12958-025-01381-4
work_keys_str_mv AT reinasonehara anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT tomokonakamura anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT takehikotakeda anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT satoshikaseki anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT tomomiseki anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT hideakitanaka anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT atsushiyabuki anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT natsukimiyake anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT ayakomuraoka anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT satokoosuka anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT akiraiwase anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT hiroakikajiyama anovelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT reinasonehara novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT tomokonakamura novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT takehikotakeda novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT satoshikaseki novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT tomomiseki novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT hideakitanaka novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT atsushiyabuki novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT natsukimiyake novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT ayakomuraoka novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT satokoosuka novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT akiraiwase novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression
AT hiroakikajiyama novelsenotherapeuticstrategywithazithromycinforpreventingendometriosisprogression