MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans

Abstract Non-obstructive azoospermia (NOA) represents the most severe form of male infertility; however, its genetic etiology remains largely elusive. MCM9 is crucial for DNA damage repair in mammalian somatic cells, playing a key role in regulating both homologous recombination (HR) and mismatch re...

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Main Authors: Xuan Sha, Xin Zhang, Hao Geng, Yuqian Li, Xun Xia, Guotong Li, Rong Hua, Kuokuo Li, Yang Gao, Qunshan Shen, Rui Guo, Yuping Xu, Xiaojin He, Yunxia Cao, Mingxi Liu, Huan Wu
Format: Article
Language:English
Published: Nature Publishing Group 2025-07-01
Series:Cell Death Discovery
Online Access:https://doi.org/10.1038/s41420-025-02581-y
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author Xuan Sha
Xin Zhang
Hao Geng
Yuqian Li
Xun Xia
Guotong Li
Rong Hua
Kuokuo Li
Yang Gao
Qunshan Shen
Rui Guo
Yuping Xu
Xiaojin He
Yunxia Cao
Mingxi Liu
Huan Wu
author_facet Xuan Sha
Xin Zhang
Hao Geng
Yuqian Li
Xun Xia
Guotong Li
Rong Hua
Kuokuo Li
Yang Gao
Qunshan Shen
Rui Guo
Yuping Xu
Xiaojin He
Yunxia Cao
Mingxi Liu
Huan Wu
author_sort Xuan Sha
collection DOAJ
description Abstract Non-obstructive azoospermia (NOA) represents the most severe form of male infertility; however, its genetic etiology remains largely elusive. MCM9 is crucial for DNA damage repair in mammalian somatic cells, playing a key role in regulating both homologous recombination (HR) and mismatch repair (MMR) pathways. In mice, MCM9 deficiency leads to spermatogenic failure characterized by progressive germ cell depletion and impaired HR repair. However, the underlying mechanism remains unclear in humans. Our study identified two novel homozygous loss-of-function (LoF) mutations in MCM9 in two unrelated NOA patients presenting with Sertoli cell-only syndrome (SCOS). The absence of testicular MCM9 confirmed the pathogenicity of these LoF mutations. Furthermore, diminished HR-mediated DNA repair capacity observed in HEK293T cells, either lacking MCM9 or overexpressing mutant MCM9 plasmids, highlighted the deleterious impact of these LoF mutations on HR repair. Additionally, the confirmed interaction between human testicular MCM9 and both MSH2 and MLH1, alongside findings that human MCM9 is predominantly expressed in spermatogonial stem cells and spermatogonia, provides compelling evidence for the involvement of the MCM9-mediated MMR pathway in maintaining genomic integrity and supporting the viability and proliferation of spermatogonia in humans. Given the poor outcomes of microdissection testicular sperm extraction (micro-TESE) observed in both probands, we propose that biallelic LoF mutations in MCM9 may serve as non-invasive molecular biomarkers for predicting micro-TESE failure. These findings enhance our understanding of the genetic basis of human NOA, particularly SCOS, and provide valuable insights for genetic counseling and fertility guidance tailored to these patients.
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spelling doaj-art-16b2a0b3a1d546c88e113e7e7deab5a02025-08-20T03:45:24ZengNature Publishing GroupCell Death Discovery2058-77162025-07-0111111110.1038/s41420-025-02581-yMCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humansXuan Sha0Xin Zhang1Hao Geng2Yuqian Li3Xun Xia4Guotong Li5Rong Hua6Kuokuo Li7Yang Gao8Qunshan Shen9Rui Guo10Yuping Xu11Xiaojin He12Yunxia Cao13Mingxi Liu14Huan Wu15Reproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityState Key Laboratory of Reproductive Medicine and Offspring Health, The Affiliated Taizhou People’s Hospital of Nanjing Medical University, Taizhou School of Clinical Medicine, Nanjing Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityNHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract (Anhui Medical University)Reproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityNHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract (Anhui Medical University)Reproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityState Key Laboratory of Reproductive Medicine and Offspring Health, The Affiliated Taizhou People’s Hospital of Nanjing Medical University, Taizhou School of Clinical Medicine, Nanjing Medical UniversityReproductive Medicine Center, Department of Obstetrics and Gynecology, the First Affiliated Hospital of Anhui Medical UniversityAbstract Non-obstructive azoospermia (NOA) represents the most severe form of male infertility; however, its genetic etiology remains largely elusive. MCM9 is crucial for DNA damage repair in mammalian somatic cells, playing a key role in regulating both homologous recombination (HR) and mismatch repair (MMR) pathways. In mice, MCM9 deficiency leads to spermatogenic failure characterized by progressive germ cell depletion and impaired HR repair. However, the underlying mechanism remains unclear in humans. Our study identified two novel homozygous loss-of-function (LoF) mutations in MCM9 in two unrelated NOA patients presenting with Sertoli cell-only syndrome (SCOS). The absence of testicular MCM9 confirmed the pathogenicity of these LoF mutations. Furthermore, diminished HR-mediated DNA repair capacity observed in HEK293T cells, either lacking MCM9 or overexpressing mutant MCM9 plasmids, highlighted the deleterious impact of these LoF mutations on HR repair. Additionally, the confirmed interaction between human testicular MCM9 and both MSH2 and MLH1, alongside findings that human MCM9 is predominantly expressed in spermatogonial stem cells and spermatogonia, provides compelling evidence for the involvement of the MCM9-mediated MMR pathway in maintaining genomic integrity and supporting the viability and proliferation of spermatogonia in humans. Given the poor outcomes of microdissection testicular sperm extraction (micro-TESE) observed in both probands, we propose that biallelic LoF mutations in MCM9 may serve as non-invasive molecular biomarkers for predicting micro-TESE failure. These findings enhance our understanding of the genetic basis of human NOA, particularly SCOS, and provide valuable insights for genetic counseling and fertility guidance tailored to these patients.https://doi.org/10.1038/s41420-025-02581-y
spellingShingle Xuan Sha
Xin Zhang
Hao Geng
Yuqian Li
Xun Xia
Guotong Li
Rong Hua
Kuokuo Li
Yang Gao
Qunshan Shen
Rui Guo
Yuping Xu
Xiaojin He
Yunxia Cao
Mingxi Liu
Huan Wu
MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
Cell Death Discovery
title MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
title_full MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
title_fullStr MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
title_full_unstemmed MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
title_short MCM9 deficiency impairs DNA damage repair during spermatogenesis, leading to Sertoli cell-only syndrome in humans
title_sort mcm9 deficiency impairs dna damage repair during spermatogenesis leading to sertoli cell only syndrome in humans
url https://doi.org/10.1038/s41420-025-02581-y
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