Hydrogen Sulfide Impairs Meiosis Resumption in Xenopuslaevis Oocytes

Armance Gelaude; Sylvain Slaby; Katia Cailliau; Matthieu Marin; Arlette Lescuyer-Rousseau; Caroline Molinaro; Jan Nevoral; Veronica Kučerová-Chrpová; Marketa Sedmikova; Jaroslav Petr; Alain Martoriati; Jean-François Bodart

doi:10.3390/cells9010237

Hydrogen Sulfide Impairs Meiosis Resumption in Xenopuslaevis Oocytes

Cells. 2020 Jan 17;9(1):237. doi: 10.3390/cells9010237.

Affiliations

¹ CNRS, UMR 8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, Univ. Lille, F-59000 Lille, France.
² Department of Veterinary Sciences, Food and Natural Resources, Faculty of Agrobiology, Czech University of Life Sciences in Prague, Kamycka 129, 16521 Prague-Suchdol, Czech Republic.
³ Biomedical Center and Department of Histology and Embryology, Faculty of Medicine in Pilsen, Charles University, Alej Svobody 1655/76, 32300 Pilsen, Czech Republic.
⁴ Research Institute of Animal Production, Pratelstvi 815, 10400 Prague 10-Uhrineves, Czech Republic.

Abstract

The role of hydrogen sulfide (H₂S) is addressed in Xenopuslaevis oocytes. Three enzymes involved in H₂S metabolism, cystathionine β-synthase, cystathionine γ-lyase, and 3-mercaptopyruvate sulfurtransferase, were detected in prophase I and metaphase II-arrested oocytes and drove an acceleration of oocyte meiosis resumption when inhibited. Moreover, meiosis resumption is associated with a significant decrease in endogenous H₂S. On another hand, a dose-dependent inhibition was obtained using the H₂S donor, NaHS (1 and 5 mM). NaHS impaired translation. NaHS did not induce the dissociation of the components of the M-phase promoting factor (MPF), cyclin B and Cdk1, nor directly impacted the MPF activity. However, the M-phase entry induced by microinjection of metaphase II MPF-containing cytoplasm was diminished, suggesting upstream components of the MPF auto-amplification loop were sensitive to H₂S. Superoxide dismutase and catalase hindered the effects of NaHS, and this sensitivity was partially dependent on the production of reactive oxygen species (ROS). In contrast to other species, no apoptosis was promoted. These results suggest a contribution of H₂S signaling in the timing of amphibian oocytes meiosis resumption.

Keywords: Xenopus laevis; cell cycle; hydrogen sulfide; meiosis; oocyte.

Publication types

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

MeSH terms

Animals
Apoptosis / drug effects
Catalase / metabolism
Cell Cycle Proteins / metabolism
Cell Survival / drug effects
Cyclin B / metabolism
Cystathionine beta-Synthase / antagonists & inhibitors
Cystathionine beta-Synthase / metabolism
Cystathionine gamma-Lyase / antagonists & inhibitors
Cystathionine gamma-Lyase / metabolism
Cytoplasm / metabolism
Female
Hydrogen Sulfide / metabolism*
Maturation-Promoting Factor / metabolism*
Meiosis / drug effects*
Meiotic Prophase I / drug effects
Metaphase / drug effects
Oocytes / chemistry
Oocytes / enzymology
Oocytes / metabolism*
Protein Kinases / metabolism
Reactive Oxygen Species / metabolism
Signal Transduction / drug effects
Sulfides / metabolism
Sulfides / pharmacology*
Sulfurtransferases / antagonists & inhibitors
Sulfurtransferases / metabolism
Superoxide Dismutase / metabolism
Xenopus Proteins / metabolism
Xenopus laevis
cdc25 Phosphatases / metabolism

Substances

Cell Cycle Proteins
Cyclin B
Reactive Oxygen Species
Sulfides
Xenopus Proteins
Catalase
Superoxide Dismutase
Protein Kinases
CDK1 protein, Xenopus
Maturation-Promoting Factor
Sulfurtransferases
3-mercaptopyruvate sulphurtransferase
CDC25C protein, human
cdc25 Phosphatases
Cystathionine beta-Synthase
Cystathionine gamma-Lyase
sodium bisulfide
Hydrogen Sulfide