Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study

BackgroundInfertility affects approximately 15% of couples worldwide, with male factors accounting for nearly 50% of cases. Intracytoplasmic sperm injection (ICSI) has become the standard treatment for male factor infertility, but outcomes vary significantly among couples. While conventional genetic...

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Main Authors: Ting Jiang, Yan Wang, Wandai Wu, Qianru Yang, Sixian Wu, Xueguang Zhang, Wenming Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Genetics
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Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2025.1610943/full
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author Ting Jiang
Yan Wang
Wandai Wu
Qianru Yang
Sixian Wu
Xueguang Zhang
Wenming Xu
author_facet Ting Jiang
Yan Wang
Wandai Wu
Qianru Yang
Sixian Wu
Xueguang Zhang
Wenming Xu
author_sort Ting Jiang
collection DOAJ
description BackgroundInfertility affects approximately 15% of couples worldwide, with male factors accounting for nearly 50% of cases. Intracytoplasmic sperm injection (ICSI) has become the standard treatment for male factor infertility, but outcomes vary significantly among couples. While conventional genetic testing using blood samples is common in reproductive medicine, the genetic composition of sperm may differ significantly from somatic cells due to mosaicism and de novo mutations during spermatogenesis.MethodsWe collected semen samples from 11 couples with varying ICSI outcomes: successful clinical pregnancy (n = 6), implantation failure (n = 3), and early pregnancy loss (n = 2). Sperm DNA was extracted using magnetic-activated cell separation and whole-exome sequencing was performed. The sequencing data were aligned to the GRCh37/hg19 reference genome and analyzed for potentially pathogenic mutations. Semen analysis and karyotype were also evaluated.ResultsSemen analysis showed no significant differences between groups except for sperm morphology. Whole-exome sequencing identified distinct mutation patterns between groups. Mutations in USP9X, SPAG6 and ADGRG2 were observed in the clinical pregnancy group. Implantation failure and pregnancy loss were associated with mutations in genes involved in embryo adhesion, immune regulation, and genomic stability, including MAGEC1, MUC4 and SERPINA2.ConclusionThis pilot study suggests that direct sperm exome sequencing may reveal genetic variants associated with different ICSI outcomes. While our findings require validation in larger cohorts, they generate hypotheses about sperm-specific factors that might influence post-fertilization developmental events and pregnancy outcomes.
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spelling doaj-art-3cfcfe0efbb64881bb25d753a3ce5e082025-08-20T01:53:08ZengFrontiers Media S.A.Frontiers in Genetics1664-80212025-05-011610.3389/fgene.2025.16109431610943Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot studyTing Jiang0Yan Wang1Wandai Wu2Qianru Yang3Sixian Wu4Xueguang Zhang5Wenming Xu6Department of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Center of Reproductive Medicine, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaDepartment of Obstetrics/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu, ChinaBackgroundInfertility affects approximately 15% of couples worldwide, with male factors accounting for nearly 50% of cases. Intracytoplasmic sperm injection (ICSI) has become the standard treatment for male factor infertility, but outcomes vary significantly among couples. While conventional genetic testing using blood samples is common in reproductive medicine, the genetic composition of sperm may differ significantly from somatic cells due to mosaicism and de novo mutations during spermatogenesis.MethodsWe collected semen samples from 11 couples with varying ICSI outcomes: successful clinical pregnancy (n = 6), implantation failure (n = 3), and early pregnancy loss (n = 2). Sperm DNA was extracted using magnetic-activated cell separation and whole-exome sequencing was performed. The sequencing data were aligned to the GRCh37/hg19 reference genome and analyzed for potentially pathogenic mutations. Semen analysis and karyotype were also evaluated.ResultsSemen analysis showed no significant differences between groups except for sperm morphology. Whole-exome sequencing identified distinct mutation patterns between groups. Mutations in USP9X, SPAG6 and ADGRG2 were observed in the clinical pregnancy group. Implantation failure and pregnancy loss were associated with mutations in genes involved in embryo adhesion, immune regulation, and genomic stability, including MAGEC1, MUC4 and SERPINA2.ConclusionThis pilot study suggests that direct sperm exome sequencing may reveal genetic variants associated with different ICSI outcomes. While our findings require validation in larger cohorts, they generate hypotheses about sperm-specific factors that might influence post-fertilization developmental events and pregnancy outcomes.https://www.frontiersin.org/articles/10.3389/fgene.2025.1610943/fullsperm whole-exome sequencingICSI outcomesgenetic variantsfertilization failureimplantation failurepregnancy loss
spellingShingle Ting Jiang
Yan Wang
Wandai Wu
Qianru Yang
Sixian Wu
Xueguang Zhang
Wenming Xu
Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
Frontiers in Genetics
sperm whole-exome sequencing
ICSI outcomes
genetic variants
fertilization failure
implantation failure
pregnancy loss
title Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
title_full Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
title_fullStr Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
title_full_unstemmed Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
title_short Distinct germ-line genetic mutation patterns correlate with reproductive outcomes in ICSI patients: a pilot study
title_sort distinct germ line genetic mutation patterns correlate with reproductive outcomes in icsi patients a pilot study
topic sperm whole-exome sequencing
ICSI outcomes
genetic variants
fertilization failure
implantation failure
pregnancy loss
url https://www.frontiersin.org/articles/10.3389/fgene.2025.1610943/full
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