New Insight into Sperm Capacitation: A Novel Mechanism of 17β-Estradiol Signalling.

Tereza Bosakova,Natasa Sebkova,Tomas Albrecht,Jana Albrechtova,Zuzana Bosakova,Ondrej Simonik,Antonin Tockstein,Hana Adamusova,Katerina Dvorakova-Hortova

doi:10.3390/ijms19124011

Abstract

17β-estradiol (estradiol) is a natural estrogen regulating reproduction including sperm and egg development, sperm maturation—called capacitation—and sperm–egg communication. High doses can increase germ cell apoptosis and decrease sperm count. Our aim was to answer the biological relevance of estradiol in sperm capacitation and its effect on motility and acrosome reaction to quantify its interaction with estrogen receptors and propose a model of estradiol action during capacitation using kinetic analysis. Estradiol increased protein tyrosine phosphorylation, elevated rate of spontaneous acrosome reaction, and altered motility parameters measured Hamilton-Thorne Computer Assisted Semen Analyzer (CASA) in capacitating sperm. To monitor time and concentration dependent binding dynamics of extracellular estradiol, high-performance liquid chromatography with tandem mass spectrometry was used to measure sperm response and data was subjected to kinetic analysis. The kinetic model of estradiol action during sperm maturation shows that estradiol adsorption onto a plasma membrane surface is controlled by Langmuir isotherm. After, when estradiol passes into the cytoplasm, it forms an unstable adduct with cytoplasmic receptors, which display a signalling autocatalytic pattern. This autocatalytic reaction suggests crosstalk between receptor and non-receptor pathways utilized by sperm prior to fertilization.

Highlights

In order for mammalian sperm to fertilize, it must undergo a series of maturation events in the female reproductive tract, called capacitation [1]
Hamilton-Thorne Computer-Aided Sperm Analysis (CASA) is generally used for the monitoring of sperm motility and provides a set of standard kinematic parameters that aids with the identification of changes in trajectories and flagellar beating patterns connected with hyperactivation as an important part of sperm capacitation [6,7]
By applying kinetic analysis to our data obtained by HPLC-MS/MS, and measuring the estradiol dynamics during mouse sperm capacitation, we propose a unique type of autocatalytic estradiol signalling, which could unify all the estradiol actions into one complex event

Summary

Introduction

In order for mammalian sperm to fertilize, it must undergo a series of maturation events in the female reproductive tract, called capacitation [1]. It is important to evaluate the status of capacitation by other parameters, such as motility and sperm ability to undergo acrosome reaction (AR). Hamilton-Thorne Computer-Aided Sperm Analysis (CASA) is generally used for the monitoring of sperm motility and provides a set of standard kinematic parameters that aids with the identification of changes in trajectories and flagellar beating patterns connected with hyperactivation as an important part of sperm capacitation [6,7]. In vivo capacitation occurs mainly in the uterus and oviducts, facilitated by substances in the female genital tract including estrogen. Progesterone-induced AR [9,13], progesterone-enhanced sperm hyperactivation [14,15,16], and progesterone-increased TyrP [14,15] are all suppressed by estradiol

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