Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia

BackgroundOligoasthenoteratozoospermia (OAT) is a widespread cause of male infertility. One of the usual clinical manifestations of OAT is multiple morphological abnormalities of the sperm flagella (MMAF), which are frequently associated with mutations and defects in the dynein family. However, the...

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Main Authors: Shu Li, Zexin Zhang, Linna Xie, Yanqiu Zhao, Hongtai Chen, Shijia Zhang, Yixiang Cai, Bingjie Ren, Wensheng Liu, Songxi Tang, Yanwei Sha
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-10-01
Series:Frontiers in Endocrinology
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Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2024.1462509/full
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author Shu Li
Zexin Zhang
Linna Xie
Linna Xie
Yanqiu Zhao
Hongtai Chen
Shijia Zhang
Yixiang Cai
Bingjie Ren
Wensheng Liu
Songxi Tang
Yanwei Sha
Yanwei Sha
Yanwei Sha
author_facet Shu Li
Zexin Zhang
Linna Xie
Linna Xie
Yanqiu Zhao
Hongtai Chen
Shijia Zhang
Yixiang Cai
Bingjie Ren
Wensheng Liu
Songxi Tang
Yanwei Sha
Yanwei Sha
Yanwei Sha
author_sort Shu Li
collection DOAJ
description BackgroundOligoasthenoteratozoospermia (OAT) is a widespread cause of male infertility. One of the usual clinical manifestations of OAT is multiple morphological abnormalities of the sperm flagella (MMAF), which are frequently associated with mutations and defects in the dynein family. However, the relationship between the newly identified Dynein Axonemal Heavy Chain 3 (DNAH3) mutation and oligonasthenospermia in humans has not yet been established.MethodsWhole exome sequencing, pathogenicity analysis, and species conservation analysis of mutation sites were conducted on two patients from different unrelated families with DNAH3 mutations. We identified representative mutation sites and predicted the protein structure following these mutations. The sperm characteristics of the two patients with DNAH3 mutations were verified using Papanicolaou staining, scanning electron microscopy, and transmission electron microscopy. Additionally, mRNA and protein levels were assessed through RT-qPCR and Western blotting.ResultsThe biallelic mutations in the first progenitor included a heterozygous deletion and insertion, c.6535_6536 delinsAC (to infect mutation (p.Asp2179Thr), and stop codon premutation, c.3249G > A (p.Trp1083Ter). In Family II, the patient (P2) harbored a DNAH3 heterozygous missense mutation, c. 10439G> A(p.Arg3480Gln), along with a stop codon premutation, (c.10260G > A; p.Trp3420Ter). Patients with premature termination of transcription or translation due to DNAH3 mutations exhibit OAT phenotypes, including fibrous sheath dysplasia and multiple tail malformations. We identified the representative sites after mutation, predicted the protein structure, and assessed changes in the protein levels of DNAH3 and related genes following mutations. Notably,a significant reduction in DNAH3 protein expression was validated in these patients. We may explore in the future how DNAH3 affects sperm motility and quality through regulatory mechanisms involving protein structural changes.ConclusionNovel biallelic mutations in DNAH3, especially those resulting in a premature stop codon, may alter protein expression, structure, and active site, leading to spermatogenic failure and potentially inducing OAT. The discovery of new mutations in DNAH3 may be the key to the diagnosis and treatment of OAT.
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spelling doaj-art-8980aa46c8ec47d6ab74ec7a52712aa52024-11-11T08:39:26ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922024-10-011510.3389/fendo.2024.14625091462509Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermiaShu Li0Zexin Zhang1Linna Xie2Linna Xie3Yanqiu Zhao4Hongtai Chen5Shijia Zhang6Yixiang Cai7Bingjie Ren8Wensheng Liu9Songxi Tang10Yanwei Sha11Yanwei Sha12Yanwei Sha13Department of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaPeking Union Medical College, Chinese Academy of Medical Sciences, Beijing, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaState Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, School of Public Health, Xiamen University, Xiamen, Fujian, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaNational Health Commission (NHC) Key Laboratory of Male Reproduction and Genetics, Guangdong Provincial Reproductive Science Institute (Guangdong Provincial Fertility Hospital), Guangzhou, Guangdong, ChinaDepartment of Andrology and Sexual Medicine, First Affiliated Hospital of Fujian Medical University, Fuzhou, ChinaDepartment of Andrology, Women and Children’s Hospital, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaState Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, School of Public Health, Xiamen University, Xiamen, Fujian, ChinaFujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, ChinaBackgroundOligoasthenoteratozoospermia (OAT) is a widespread cause of male infertility. One of the usual clinical manifestations of OAT is multiple morphological abnormalities of the sperm flagella (MMAF), which are frequently associated with mutations and defects in the dynein family. However, the relationship between the newly identified Dynein Axonemal Heavy Chain 3 (DNAH3) mutation and oligonasthenospermia in humans has not yet been established.MethodsWhole exome sequencing, pathogenicity analysis, and species conservation analysis of mutation sites were conducted on two patients from different unrelated families with DNAH3 mutations. We identified representative mutation sites and predicted the protein structure following these mutations. The sperm characteristics of the two patients with DNAH3 mutations were verified using Papanicolaou staining, scanning electron microscopy, and transmission electron microscopy. Additionally, mRNA and protein levels were assessed through RT-qPCR and Western blotting.ResultsThe biallelic mutations in the first progenitor included a heterozygous deletion and insertion, c.6535_6536 delinsAC (to infect mutation (p.Asp2179Thr), and stop codon premutation, c.3249G > A (p.Trp1083Ter). In Family II, the patient (P2) harbored a DNAH3 heterozygous missense mutation, c. 10439G> A(p.Arg3480Gln), along with a stop codon premutation, (c.10260G > A; p.Trp3420Ter). Patients with premature termination of transcription or translation due to DNAH3 mutations exhibit OAT phenotypes, including fibrous sheath dysplasia and multiple tail malformations. We identified the representative sites after mutation, predicted the protein structure, and assessed changes in the protein levels of DNAH3 and related genes following mutations. Notably,a significant reduction in DNAH3 protein expression was validated in these patients. We may explore in the future how DNAH3 affects sperm motility and quality through regulatory mechanisms involving protein structural changes.ConclusionNovel biallelic mutations in DNAH3, especially those resulting in a premature stop codon, may alter protein expression, structure, and active site, leading to spermatogenic failure and potentially inducing OAT. The discovery of new mutations in DNAH3 may be the key to the diagnosis and treatment of OAT.https://www.frontiersin.org/articles/10.3389/fendo.2024.1462509/fulloligoasthenoteratozoospermiadyneinintracytoplasmic sperm injectionmale infertilityDNAH3
spellingShingle Shu Li
Zexin Zhang
Linna Xie
Linna Xie
Yanqiu Zhao
Hongtai Chen
Shijia Zhang
Yixiang Cai
Bingjie Ren
Wensheng Liu
Songxi Tang
Yanwei Sha
Yanwei Sha
Yanwei Sha
Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
Frontiers in Endocrinology
oligoasthenoteratozoospermia
dynein
intracytoplasmic sperm injection
male infertility
DNAH3
title Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
title_full Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
title_fullStr Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
title_full_unstemmed Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
title_short Novel bi-allelic DNAH3 variants cause oligoasthenoteratozoospermia
title_sort novel bi allelic dnah3 variants cause oligoasthenoteratozoospermia
topic oligoasthenoteratozoospermia
dynein
intracytoplasmic sperm injection
male infertility
DNAH3
url https://www.frontiersin.org/articles/10.3389/fendo.2024.1462509/full
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