Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells

Bisphenol-A (BPA) exposure in an adult male can affect the reproductive system, which may also adversely affect the next generation. However, there is a lack of comprehensive data on the BPA-induced disruption of the association and functional characteristics of the testicular germ cells, which the...

Full description

Bibliographic Details
Main Authors: Polash Chandra Karmakar, Jin Seop Ahn, Yong-Hee Kim, Sang-Eun Jung, Bang-Jin Kim, Hee-Seok Lee, Sun-Uk Kim, Md Saidur Rahman, Myung-Geol Pang, Buom-Yong Ryu
Format: Article
Language:English
Published: MDPI AG 2020-07-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/15/5408
_version_ 1797560944406036480
author Polash Chandra Karmakar
Jin Seop Ahn
Yong-Hee Kim
Sang-Eun Jung
Bang-Jin Kim
Hee-Seok Lee
Sun-Uk Kim
Md Saidur Rahman
Myung-Geol Pang
Buom-Yong Ryu
author_facet Polash Chandra Karmakar
Jin Seop Ahn
Yong-Hee Kim
Sang-Eun Jung
Bang-Jin Kim
Hee-Seok Lee
Sun-Uk Kim
Md Saidur Rahman
Myung-Geol Pang
Buom-Yong Ryu
author_sort Polash Chandra Karmakar
collection DOAJ
description Bisphenol-A (BPA) exposure in an adult male can affect the reproductive system, which may also adversely affect the next generation. However, there is a lack of comprehensive data on the BPA-induced disruption of the association and functional characteristics of the testicular germ cells, which the present study sought to investigate. Adult male mice were administered BPA doses by gavage for six consecutive weeks and allowed to breed, producing generations F1–F4. Testis samples from each generation were evaluated for several parameters, including abnormal structure, alterations in germ cell proportions, apoptosis, and loss of functional properties of spermatogonial stem cells (SSCs). We observed that at the lowest-observed-adverse-effect level (LOAEL) dose, the testicular abnormalities and alterations in seminiferous epithelium staging persisted in F0–F2 generations, although a reduced total spermatogonia count was found only in F0. However, abnormalities in the proportions of germ cells were observed until F2. Exposure of the male mice (F0) to BPA alters the morphology of the testis along with the association of germ cells and stemness properties of SSCs, with the effects persisting up to F2. Therefore, we conclude that BPA induces physiological and functional disruption in male germ cells, which may lead to reproductive health issues in the next generation.
first_indexed 2024-03-10T18:07:07Z
format Article
id doaj.art-c0fb9fa7d9b3493d9e1f1cd8fde2eaa8
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-10T18:07:07Z
publishDate 2020-07-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-c0fb9fa7d9b3493d9e1f1cd8fde2eaa82023-11-20T08:25:27ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-07-012115540810.3390/ijms21155408Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem CellsPolash Chandra Karmakar0Jin Seop Ahn1Yong-Hee Kim2Sang-Eun Jung3Bang-Jin Kim4Hee-Seok Lee5Sun-Uk Kim6Md Saidur Rahman7Myung-Geol Pang8Buom-Yong Ryu9Department of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Cancer Biology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USADepartment of Food Science & Technology, Chung-Ang University, Anseong 17546, KoreaNational Primate Research Center and Futuristic Animal Resource & Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Ochang 28116, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaDepartment of Animal Science and Technology and BET Research Institute, Chung-Ang University, Anseong 17546, KoreaBisphenol-A (BPA) exposure in an adult male can affect the reproductive system, which may also adversely affect the next generation. However, there is a lack of comprehensive data on the BPA-induced disruption of the association and functional characteristics of the testicular germ cells, which the present study sought to investigate. Adult male mice were administered BPA doses by gavage for six consecutive weeks and allowed to breed, producing generations F1–F4. Testis samples from each generation were evaluated for several parameters, including abnormal structure, alterations in germ cell proportions, apoptosis, and loss of functional properties of spermatogonial stem cells (SSCs). We observed that at the lowest-observed-adverse-effect level (LOAEL) dose, the testicular abnormalities and alterations in seminiferous epithelium staging persisted in F0–F2 generations, although a reduced total spermatogonia count was found only in F0. However, abnormalities in the proportions of germ cells were observed until F2. Exposure of the male mice (F0) to BPA alters the morphology of the testis along with the association of germ cells and stemness properties of SSCs, with the effects persisting up to F2. Therefore, we conclude that BPA induces physiological and functional disruption in male germ cells, which may lead to reproductive health issues in the next generation.https://www.mdpi.com/1422-0067/21/15/5408bisphenol Atestis morphologygerm cell associationsapoptosis
spellingShingle Polash Chandra Karmakar
Jin Seop Ahn
Yong-Hee Kim
Sang-Eun Jung
Bang-Jin Kim
Hee-Seok Lee
Sun-Uk Kim
Md Saidur Rahman
Myung-Geol Pang
Buom-Yong Ryu
Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
International Journal of Molecular Sciences
bisphenol A
testis morphology
germ cell associations
apoptosis
title Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
title_full Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
title_fullStr Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
title_full_unstemmed Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
title_short Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
title_sort paternal exposure to bisphenol a transgenerationally impairs testis morphology germ cell associations and stemness properties of mouse spermatogonial stem cells
topic bisphenol A
testis morphology
germ cell associations
apoptosis
url https://www.mdpi.com/1422-0067/21/15/5408
work_keys_str_mv AT polashchandrakarmakar paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT jinseopahn paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT yongheekim paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT sangeunjung paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT bangjinkim paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT heeseoklee paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT sunukkim paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT mdsaidurrahman paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT myunggeolpang paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells
AT buomyongryu paternalexposuretobisphenolatransgenerationallyimpairstestismorphologygermcellassociationsandstemnesspropertiesofmousespermatogonialstemcells