Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications

Abstract Spermatogonial stem cells (SSCs) are the foundation of life-long spermatogenesis. While SSC research has advanced greatly over the past two decades, characterization of SSCs during postnatal development has not been well documented. Using the mouse as a model, in this study, we defined the...

Full description

Bibliographic Details
Main Authors: Youngmin Song, Xiangfan Zhang, Joëlle A. Desmarais, Makoto Nagano
Format: Article
Language:English
Published: Nature Portfolio 2024-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-52824-8
_version_ 1797276638454480896
author Youngmin Song
Xiangfan Zhang
Joëlle A. Desmarais
Makoto Nagano
author_facet Youngmin Song
Xiangfan Zhang
Joëlle A. Desmarais
Makoto Nagano
author_sort Youngmin Song
collection DOAJ
description Abstract Spermatogonial stem cells (SSCs) are the foundation of life-long spermatogenesis. While SSC research has advanced greatly over the past two decades, characterization of SSCs during postnatal development has not been well documented. Using the mouse as a model, in this study, we defined the immunophenotypic profiles of testis cells during the course of postnatal development using multi-parameter flow cytometry with up to five cell-surface antigens. We found that the profiles progress over time in a manner specific to developmental stages. We then isolated multiple cell fractions at different developmental stages using fluorescent-activated cell sorting (FACS) and identified specific cell populations with prominent capacities to regenerate spermatogenesis upon transplantation and to initiate long-term SSC culture. The data indicated that the cell fraction with the highest level of regeneration capacity exhibited the most prominent potential to initiate SSC culture, regardless of age. Interestingly, refinement of cell fractionation using GFRA1 and KIT did not lead to further enrichment of regenerative and culture-initiating stem cells, suggesting that when a high degree of SSC enrichment is achieved, standard markers of SSC self-renewal or commitment may lose their effectiveness to distinguish cells at the stem cell state from committed progenitors. This study provides a significant information resource for future studies and practical applications of mammalian SSCs.
first_indexed 2024-03-07T15:31:06Z
format Article
id doaj.art-d0e77a58303b4c0083f0507e34c689dc
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-03-07T15:31:06Z
publishDate 2024-01-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-d0e77a58303b4c0083f0507e34c689dc2024-03-05T16:27:46ZengNature PortfolioScientific Reports2045-23222024-01-0114111510.1038/s41598-024-52824-8Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applicationsYoungmin Song0Xiangfan Zhang1Joëlle A. Desmarais2Makoto Nagano3Department of Obstetrics and Gynecology, McGill University, and the Child Health and Human Development Program, The Research Institute of the McGill University Health CentreDepartment of Obstetrics and Gynecology, McGill University, and the Child Health and Human Development Program, The Research Institute of the McGill University Health CentreDepartment of Obstetrics and Gynecology, McGill University, and the Child Health and Human Development Program, The Research Institute of the McGill University Health CentreDepartment of Obstetrics and Gynecology, McGill University, and the Child Health and Human Development Program, The Research Institute of the McGill University Health CentreAbstract Spermatogonial stem cells (SSCs) are the foundation of life-long spermatogenesis. While SSC research has advanced greatly over the past two decades, characterization of SSCs during postnatal development has not been well documented. Using the mouse as a model, in this study, we defined the immunophenotypic profiles of testis cells during the course of postnatal development using multi-parameter flow cytometry with up to five cell-surface antigens. We found that the profiles progress over time in a manner specific to developmental stages. We then isolated multiple cell fractions at different developmental stages using fluorescent-activated cell sorting (FACS) and identified specific cell populations with prominent capacities to regenerate spermatogenesis upon transplantation and to initiate long-term SSC culture. The data indicated that the cell fraction with the highest level of regeneration capacity exhibited the most prominent potential to initiate SSC culture, regardless of age. Interestingly, refinement of cell fractionation using GFRA1 and KIT did not lead to further enrichment of regenerative and culture-initiating stem cells, suggesting that when a high degree of SSC enrichment is achieved, standard markers of SSC self-renewal or commitment may lose their effectiveness to distinguish cells at the stem cell state from committed progenitors. This study provides a significant information resource for future studies and practical applications of mammalian SSCs.https://doi.org/10.1038/s41598-024-52824-8
spellingShingle Youngmin Song
Xiangfan Zhang
Joëlle A. Desmarais
Makoto Nagano
Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
Scientific Reports
title Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
title_full Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
title_fullStr Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
title_full_unstemmed Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
title_short Postnatal development of mouse spermatogonial stem cells as determined by immunophenotype, regenerative capacity, and long-term culture-initiating ability: a model for practical applications
title_sort postnatal development of mouse spermatogonial stem cells as determined by immunophenotype regenerative capacity and long term culture initiating ability a model for practical applications
url https://doi.org/10.1038/s41598-024-52824-8
work_keys_str_mv AT youngminsong postnataldevelopmentofmousespermatogonialstemcellsasdeterminedbyimmunophenotyperegenerativecapacityandlongtermcultureinitiatingabilityamodelforpracticalapplications
AT xiangfanzhang postnataldevelopmentofmousespermatogonialstemcellsasdeterminedbyimmunophenotyperegenerativecapacityandlongtermcultureinitiatingabilityamodelforpracticalapplications
AT joelleadesmarais postnataldevelopmentofmousespermatogonialstemcellsasdeterminedbyimmunophenotyperegenerativecapacityandlongtermcultureinitiatingabilityamodelforpracticalapplications
AT makotonagano postnataldevelopmentofmousespermatogonialstemcellsasdeterminedbyimmunophenotyperegenerativecapacityandlongtermcultureinitiatingabilityamodelforpracticalapplications