NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development

Abstract Testicular fetal Leydig cells produce androgens essential for male reproductive development. Impaired fetal Leydig cell differentiation leads to differences of sex development including hypospadias, cryptorchidism, and infertility. Despite fetal Leydig cells are thought to originate from pr...

Full description

Saved in:
Bibliographic Details
Main Authors: Martín Andrés Estermann, Sara A. Grimm, Abigail S. Kitakule, Karina F. Rodriguez, Paula R. Brown, Kathryn McClelland, Ciro M. Amato, Humphrey Hung-Chang Yao
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59183-6
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850206413955006464
author Martín Andrés Estermann
Sara A. Grimm
Abigail S. Kitakule
Karina F. Rodriguez
Paula R. Brown
Kathryn McClelland
Ciro M. Amato
Humphrey Hung-Chang Yao
author_facet Martín Andrés Estermann
Sara A. Grimm
Abigail S. Kitakule
Karina F. Rodriguez
Paula R. Brown
Kathryn McClelland
Ciro M. Amato
Humphrey Hung-Chang Yao
author_sort Martín Andrés Estermann
collection DOAJ
description Abstract Testicular fetal Leydig cells produce androgens essential for male reproductive development. Impaired fetal Leydig cell differentiation leads to differences of sex development including hypospadias, cryptorchidism, and infertility. Despite fetal Leydig cells are thought to originate from proliferating progenitor cells in the testis interstitium, the precise mechanisms governing the interstitial cells to fetal Leydig cell transition remain elusive. Using mouse models and single-nucleus multiomics, we find that fetal Leydig cells arise from a Nr2f2-positive interstitial population. Embryonic deletion of Nr2f2 in mouse testes results in differences of sex development, including dysgenic testes, Leydig cell hypoplasia, cryptorchidism, and hypospadias. By combining single-nucleus multiomics and NR2F2 ChIP-seq we find that NR2F2 promotes the progenitor fate while suppresses Leydig cell differentiation by modulating key transcription factors and downstream genes. Our findings establish Nr2f2 as a crucial regulator of fetal Leydig cell differentiation and provide molecular insights into differences of sex development linked to Nr2f2 mutations.
format Article
id doaj-art-1c2e8ae92cfa440b97c9afa859dda545
institution OA Journals
issn 2041-1723
language English
publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-1c2e8ae92cfa440b97c9afa859dda5452025-08-20T02:10:50ZengNature PortfolioNature Communications2041-17232025-04-0116111910.1038/s41467-025-59183-6NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex developmentMartín Andrés Estermann0Sara A. Grimm1Abigail S. Kitakule2Karina F. Rodriguez3Paula R. Brown4Kathryn McClelland5Ciro M. Amato6Humphrey Hung-Chang Yao7Reproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkIntegrative Bioinformatics, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkReproductive Developmental Biology Group, National Institute of Environmental Health Sciences, Research Triangle ParkAbstract Testicular fetal Leydig cells produce androgens essential for male reproductive development. Impaired fetal Leydig cell differentiation leads to differences of sex development including hypospadias, cryptorchidism, and infertility. Despite fetal Leydig cells are thought to originate from proliferating progenitor cells in the testis interstitium, the precise mechanisms governing the interstitial cells to fetal Leydig cell transition remain elusive. Using mouse models and single-nucleus multiomics, we find that fetal Leydig cells arise from a Nr2f2-positive interstitial population. Embryonic deletion of Nr2f2 in mouse testes results in differences of sex development, including dysgenic testes, Leydig cell hypoplasia, cryptorchidism, and hypospadias. By combining single-nucleus multiomics and NR2F2 ChIP-seq we find that NR2F2 promotes the progenitor fate while suppresses Leydig cell differentiation by modulating key transcription factors and downstream genes. Our findings establish Nr2f2 as a crucial regulator of fetal Leydig cell differentiation and provide molecular insights into differences of sex development linked to Nr2f2 mutations.https://doi.org/10.1038/s41467-025-59183-6
spellingShingle Martín Andrés Estermann
Sara A. Grimm
Abigail S. Kitakule
Karina F. Rodriguez
Paula R. Brown
Kathryn McClelland
Ciro M. Amato
Humphrey Hung-Chang Yao
NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
Nature Communications
title NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
title_full NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
title_fullStr NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
title_full_unstemmed NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
title_short NR2F2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
title_sort nr2f2 regulation of interstitial cell fate in the embryonic mouse testis and its impact on differences of sex development
url https://doi.org/10.1038/s41467-025-59183-6
work_keys_str_mv AT martinandresestermann nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT saraagrimm nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT abigailskitakule nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT karinafrodriguez nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT paularbrown nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT kathrynmcclelland nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT ciromamato nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment
AT humphreyhungchangyao nr2f2regulationofinterstitialcellfateintheembryonicmousetestisanditsimpactondifferencesofsexdevelopment