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


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
09 2021
Historique:
received: 23 08 2020
accepted: 10 08 2021
entrez: 9 9 2021
pubmed: 10 9 2021
medline: 15 12 2021
Statut: epublish

Résumé

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.

Identifiants

pubmed: 34499650
doi: 10.1371/journal.pgen.1009773
pii: PGENETICS-D-20-01314
pmc: PMC8428764
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1009773

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Xueying Fan (X)

Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands.

Ioannis Moustakas (I)

Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands.
Sequencing Analysis Support Core, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, The Netherlands.

Vanessa Torrens-Juaneda (V)

Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands.

Qijing Lei (Q)

Center for Reproductive Medicine, Reproductive Biology Laboratory, Amsterdam Reproduction and Development Research Institute, Amsterdam University Medical Centers, Location AMC, Amsterdam, the Netherlands.

Geert Hamer (G)

Center for Reproductive Medicine, Reproductive Biology Laboratory, Amsterdam Reproduction and Development Research Institute, Amsterdam University Medical Centers, Location AMC, Amsterdam, the Netherlands.

Leoni A Louwe (LA)

Department of Gynaecology, Leiden University Medical Center, Leiden, The Netherlands.

Gonneke S K Pilgram (GSK)

Department of Gynaecology, Leiden University Medical Center, Leiden, The Netherlands.

Karoly Szuhai (K)

Department of Cell and Chemical Biology, Leiden University Medical Center, Leiden, The Netherlands.

Roberto Matorras (R)

IVIRMA, IVI Bilbao, Bilbao, Spain; Human Reproduction Unit, Cruces University Hospital, Bilbao, Spain; Department of Obstetrics and Gynecology, Basque Country University, Spain; Biocruces Bizkaia Health Research Institute, Bilbao, Spain.

Cristina Eguizabal (C)

Cell Therapy, Stem Cells and Tissues Group, Basque Centre for Blood Transfusion and Human Tissues, Galdakao, Spain.
Biocruces Bizkaia Health Research Institute, Cell Therapy, Stem Cells and Tissues Group, Barakaldo, Spain.

Lucette van der Westerlaken (LV)

Department of Gynaecology, Leiden University Medical Center, Leiden, The Netherlands.

Hailiang Mei (H)

Sequencing Analysis Support Core, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, The Netherlands.

Susana M Chuva de Sousa Lopes (SM)

Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands.
Department for Reproductive Medicine, Ghent University Hospital, Ghent, Belgium.

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