Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.

During gametogenesis in mammals, meiosis ensures the production of haploid gametes. The timing and length of meiosis to produce female and male gametes differ considerably. In contrast to males, meiotic prophase I in females initiates during development. Hence, the knowledge regarding progression th...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Xueying Fan, Ioannis Moustakas, Vanessa Torrens-Juaneda, Qijing Lei, Geert Hamer, Leoni A Louwe, Gonneke S K Pilgram, Karoly Szuhai, Roberto Matorras, Cristina Eguizabal, Lucette van der Westerlaken, Hailiang Mei, Susana M Chuva de Sousa Lopes
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
Materias:
Acceso en línea:https://doaj.org/article/cc6bb2ecaa424a22922367940bd877c2
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:cc6bb2ecaa424a22922367940bd877c2
record_format dspace
spelling oai:doaj.org-article:cc6bb2ecaa424a22922367940bd877c22021-12-02T20:03:20ZTranscriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.1553-73901553-740410.1371/journal.pgen.1009773https://doaj.org/article/cc6bb2ecaa424a22922367940bd877c22021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009773https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404During gametogenesis in mammals, meiosis ensures the production of haploid gametes. The timing and length of meiosis to produce female and male gametes differ considerably. In contrast to males, meiotic prophase I in females initiates during development. Hence, the knowledge regarding progression through meiotic prophase I is mainly focused on human male spermatogenesis and female oocyte maturation during adulthood. Therefore, it remains unclear how the different stages of meiotic prophase I between human oogenesis and spermatogenesis compare. Analysis of single-cell transcriptomics data from human fetal germ cells (FGC) allowed us to identify the molecular signatures of female meiotic prophase I stages leptotene, zygotene, pachytene and diplotene. We have compared those between male and female germ cells in similar stages of meiotic prophase I and revealed conserved and specific features between sexes. We identified not only key players involved in the process of meiosis, but also highlighted the molecular components that could be responsible for changes in cellular morphology that occur during this developmental period, when the female FGC acquire their typical (sex-specific) oocyte shape as well as sex-differences in the regulation of DNA methylation. Analysis of X-linked expression between sexes during meiotic prophase I suggested a transient X-linked enrichment during female pachytene, that contrasts with the meiotic sex chromosome inactivation in males. Our study of the events that take place during meiotic prophase I provide a better understanding not only of female meiosis during development, but also highlights biomarkers that can be used to study infertility and offers insights in germline sex dimorphism in humans.Xueying FanIoannis MoustakasVanessa Torrens-JuanedaQijing LeiGeert HamerLeoni A LouweGonneke S K PilgramKaroly SzuhaiRoberto MatorrasCristina EguizabalLucette van der WesterlakenHailiang MeiSusana M Chuva de Sousa LopesPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 9, p e1009773 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Xueying Fan
Ioannis Moustakas
Vanessa Torrens-Juaneda
Qijing Lei
Geert Hamer
Leoni A Louwe
Gonneke S K Pilgram
Karoly Szuhai
Roberto Matorras
Cristina Eguizabal
Lucette van der Westerlaken
Hailiang Mei
Susana M Chuva de Sousa Lopes
Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
description During gametogenesis in mammals, meiosis ensures the production of haploid gametes. The timing and length of meiosis to produce female and male gametes differ considerably. In contrast to males, meiotic prophase I in females initiates during development. Hence, the knowledge regarding progression through meiotic prophase I is mainly focused on human male spermatogenesis and female oocyte maturation during adulthood. Therefore, it remains unclear how the different stages of meiotic prophase I between human oogenesis and spermatogenesis compare. Analysis of single-cell transcriptomics data from human fetal germ cells (FGC) allowed us to identify the molecular signatures of female meiotic prophase I stages leptotene, zygotene, pachytene and diplotene. We have compared those between male and female germ cells in similar stages of meiotic prophase I and revealed conserved and specific features between sexes. We identified not only key players involved in the process of meiosis, but also highlighted the molecular components that could be responsible for changes in cellular morphology that occur during this developmental period, when the female FGC acquire their typical (sex-specific) oocyte shape as well as sex-differences in the regulation of DNA methylation. Analysis of X-linked expression between sexes during meiotic prophase I suggested a transient X-linked enrichment during female pachytene, that contrasts with the meiotic sex chromosome inactivation in males. Our study of the events that take place during meiotic prophase I provide a better understanding not only of female meiosis during development, but also highlights biomarkers that can be used to study infertility and offers insights in germline sex dimorphism in humans.
format article
author Xueying Fan
Ioannis Moustakas
Vanessa Torrens-Juaneda
Qijing Lei
Geert Hamer
Leoni A Louwe
Gonneke S K Pilgram
Karoly Szuhai
Roberto Matorras
Cristina Eguizabal
Lucette van der Westerlaken
Hailiang Mei
Susana M Chuva de Sousa Lopes
author_facet Xueying Fan
Ioannis Moustakas
Vanessa Torrens-Juaneda
Qijing Lei
Geert Hamer
Leoni A Louwe
Gonneke S K Pilgram
Karoly Szuhai
Roberto Matorras
Cristina Eguizabal
Lucette van der Westerlaken
Hailiang Mei
Susana M Chuva de Sousa Lopes
author_sort Xueying Fan
title Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
title_short Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
title_full Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
title_fullStr Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
title_full_unstemmed Transcriptional progression during meiotic prophase I reveals sex-specific features and X chromosome dynamics in human fetal female germline.
title_sort transcriptional progression during meiotic prophase i reveals sex-specific features and x chromosome dynamics in human fetal female germline.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/cc6bb2ecaa424a22922367940bd877c2
work_keys_str_mv AT xueyingfan transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT ioannismoustakas transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT vanessatorrensjuaneda transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT qijinglei transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT geerthamer transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT leonialouwe transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT gonnekeskpilgram transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT karolyszuhai transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT robertomatorras transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT cristinaeguizabal transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT lucettevanderwesterlaken transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT hailiangmei transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
AT susanamchuvadesousalopes transcriptionalprogressionduringmeioticprophaseirevealssexspecificfeaturesandxchromosomedynamicsinhumanfetalfemalegermline
_version_ 1718375686848118784