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      Suppression of Progesterone-enhanced Hyperactivation in Hamster Spermatozoa by γ-aminobutyric Acid

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          Abstract

          It has been recently shown that mammalian spermatozoa were hyperactivated by steroids, amines and amino acids. In the present study, we investigated whether hyperactivation of hamster sperm is regulated by progesterone (P) and γ-aminobutyric acid (GABA). Although sperm hyperactivation was enhanced by P, GABA significantly suppressed P-enhanced hyperactivation in a dose-dependent manner. Suppression of P-enhanced hyperactivation by GABA was significantly inhibited by an antagonist of the GABA A receptor (bicuculline). Moreover, P bound to the sperm head, and this binding was decreased by GABA. Because the concentrations of GABA and P change in association with the estrous cycle, these results suggest that GABA and P competitively regulate the enhancement of hyperactivation through the GABA A receptor.

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          Fertilizing capacity of spermatozoa deposited into the fallopian tubes.

          Chawnshang Chang (1951)
          Article 0 comments Cited 192 times – based on 0 reviews     Review now
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            Progesterone activates the principal Ca2+ channel of human sperm.

            Polina V. Lishko, Inna Botchkina, Yuriy Kirichok (2011)
            Steroid hormone progesterone released by cumulus cells surrounding the egg is a potent stimulator of human spermatozoa. It attracts spermatozoa towards the egg and helps them penetrate the egg's protective vestments. Progesterone induces Ca(2+) influx into spermatozoa and triggers multiple Ca(2+)-dependent physiological responses essential for successful fertilization, such as sperm hyperactivation, acrosome reaction and chemotaxis towards the egg. As an ovarian hormone, progesterone acts by regulating gene expression through a well-characterized progesterone nuclear receptor. However, the effect of progesterone upon transcriptionally silent spermatozoa remains unexplained and is believed to be mediated by a specialized, non-genomic membrane progesterone receptor. The identity of this non-genomic progesterone receptor and the mechanism by which it causes Ca(2+) entry remain fundamental unresolved questions in human reproduction. Here we elucidate the mechanism of the non-genomic action of progesterone on human spermatozoa by identifying the Ca(2+) channel activated by progesterone. By applying the patch-clamp technique to mature human spermatozoa, we found that nanomolar concentrations of progesterone dramatically potentiate CatSper, a pH-dependent Ca(2+) channel of the sperm flagellum. We demonstrate that human CatSper is synergistically activated by elevation of intracellular pH and extracellular progesterone. Interestingly, human CatSper can be further potentiated by prostaglandins, but apparently through a binding site other than that of progesterone. Because our experimental conditions did not support second messenger signalling, CatSper or a directly associated protein serves as the elusive non-genomic progesterone receptor of sperm. Given that the CatSper-associated progesterone receptor is sperm specific and structurally different from the genomic progesterone receptor, it represents a promising target for the development of a new class of non-hormonal contraceptives.
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              The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm.

              Timo Strünker, Normann Goodwin, Christoph Brenker … (2011)
              In the oviduct, cumulus cells that surround the oocyte release progesterone. In human sperm, progesterone stimulates a Ca(2+) increase by a non-genomic mechanism. The Ca(2+) signal has been proposed to control chemotaxis, hyperactivation and acrosomal exocytosis of sperm. However, the underlying signalling mechanism has remained mysterious. Here we show that progesterone activates the sperm-specific, pH-sensitive CatSper Ca(2+) channel. We found that both progesterone and alkaline pH stimulate a rapid Ca(2+) influx with almost no latency, incompatible with a signalling pathway involving metabotropic receptors and second messengers. The Ca(2+) signals evoked by alkaline pH and progesterone are inhibited by the Ca(v) channel blockers NNC 55-0396 and mibefradil. Patch-clamp recordings from sperm reveal an alkaline-activated current carried by mono- and divalent ions that exhibits all the hallmarks of sperm-specific CatSper Ca(2+) channels. Progesterone substantially enhances the CatSper current. The alkaline- and progesterone-activated CatSper current is inhibited by both drugs. Our results resolve a long-standing controversy over the non-genomic progesterone signalling. In human sperm, either the CatSper channel itself or an associated protein serves as the non-genomic progesterone receptor. The identification of CatSper channel blockers will greatly facilitate the study of Ca(2+) signalling in sperm and help to define further the physiological role of progesterone and CatSper.
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                Author and article information

                Journal
                Journal ID (nlm-ta): J Reprod Dev
                Journal ID (iso-abbrev): J. Reprod. Dev
                Journal ID (publisher-id): JRD
                Title: The Journal of Reproduction and Development
                Publisher: The Society for Reproduction and Development
                ISSN (Print): 0916-8818
                ISSN (Electronic): 1348-4400
                Publication date (Electronic): 10 March 2014
                Publication date (Print): June 2014
                Volume: 60
                Issue: 3
                Pages: 202-209
                Affiliations
                [1) ]Laboratory Animal Research Center, Dokkyo Medical University, Tochigi 321-0293, Japan
                [2) ]Department of Physiology, School of Medicine, Dokkyo Medical University, Tochigi 321-0293, Japan
                Author notes
                Correspondence : M Fujinoki (e-mail: fujinoki@ 123456dokkyomed.ac.jp )
                Article
                Publisher ID: 2013-076
                DOI: 10.1262/jrd.2013-076
                PMC ID: 4085384
                PubMed ID: 24614320
                SO-VID: c9790ddf-ddf7-45ca-81ca-fb6e73977320
                Copyright © ©2014 Society for Reproduction and Development
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License.

                History
                Date received : 08 July 2013
                Date accepted : 10 February 2014
                Categories
                Subject: Original Article

                Keywords: γ-aminobutyric acid (gaba),hyperactivation,progesterone,spermatozoa
                Data availability:
                Keywords: γ-aminobutyric acid (gaba), hyperactivation, progesterone, spermatozoa

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