Expression of Tas1 taste receptors in mammalian spermatozoa: functional role of Tas1r1 in regulating basal Ca²⁺ and cAMP concentrations in spermatozoa

During their transit through the female genital tract, sperm have to recognize and discriminate numerous chemical compounds. However, our current knowledge of the molecular identity of appropriate chemosensory receptor proteins in sperm is still rudimentary. Considering that members of the Tas1r fam...

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Veröffentlicht in:PloS one 2012-02, Vol.7 (2), p.e32354
Hauptverfasser: Meyer, Dorke, Voigt, Anja, Widmayer, Patricia, Borth, Heike, Huebner, Sandra, Breit, Andreas, Marschall, Susan, de Angelis, Martin Hrabé, Boehm, Ulrich, Meyerhof, Wolfgang, Gudermann, Thomas, Boekhoff, Ingrid
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container_title PloS one
container_volume 7
creator Meyer, Dorke
Voigt, Anja
Widmayer, Patricia
Borth, Heike
Huebner, Sandra
Breit, Andreas
Marschall, Susan
de Angelis, Martin Hrabé
Boehm, Ulrich
Meyerhof, Wolfgang
Gudermann, Thomas
Boekhoff, Ingrid
description During their transit through the female genital tract, sperm have to recognize and discriminate numerous chemical compounds. However, our current knowledge of the molecular identity of appropriate chemosensory receptor proteins in sperm is still rudimentary. Considering that members of the Tas1r family of taste receptors are able to discriminate between a broad diversity of hydrophilic chemosensory substances, the expression of taste receptors in mammalian spermatozoa was examined. The present manuscript documents that Tas1r1 and Tas1r3, which form the functional receptor for monosodium glutamate (umami) in taste buds on the tongue, are expressed in murine and human spermatozoa, where their localization is restricted to distinct segments of the flagellum and the acrosomal cap of the sperm head. Employing a Tas1r1-deficient mCherry reporter mouse strain, we found that Tas1r1 gene deletion resulted in spermatogenic abnormalities. In addition, a significant increase in spontaneous acrosomal reaction was observed in Tas1r1 null mutant sperm whereas acrosomal secretion triggered by isolated zona pellucida or the Ca²⁺ ionophore A23187 was not different from wild-type spermatozoa. Remarkably, cytosolic Ca²⁺ levels in freshly isolated Tas1r1-deficient sperm were significantly higher compared to wild-type cells. Moreover, a significantly higher basal cAMP concentration was detected in freshly isolated Tas1r1-deficient epididymal spermatozoa, whereas upon inhibition of phosphodiesterase or sperm capacitation, the amount of cAMP was not different between both genotypes. Since Ca²⁺ and cAMP control fundamental processes during the sequential process of fertilization, we propose that the identified taste receptors and coupled signaling cascades keep sperm in a chronically quiescent state until they arrive in the vicinity of the egg - either by constitutive receptor activity and/or by tonic receptor activation by gradients of diverse chemical compounds in different compartments of the female reproductive tract.
doi_str_mv 10.1371/journal.pone.0032354
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However, our current knowledge of the molecular identity of appropriate chemosensory receptor proteins in sperm is still rudimentary. Considering that members of the Tas1r family of taste receptors are able to discriminate between a broad diversity of hydrophilic chemosensory substances, the expression of taste receptors in mammalian spermatozoa was examined. The present manuscript documents that Tas1r1 and Tas1r3, which form the functional receptor for monosodium glutamate (umami) in taste buds on the tongue, are expressed in murine and human spermatozoa, where their localization is restricted to distinct segments of the flagellum and the acrosomal cap of the sperm head. Employing a Tas1r1-deficient mCherry reporter mouse strain, we found that Tas1r1 gene deletion resulted in spermatogenic abnormalities. In addition, a significant increase in spontaneous acrosomal reaction was observed in Tas1r1 null mutant sperm whereas acrosomal secretion triggered by isolated zona pellucida or the Ca²⁺ ionophore A23187 was not different from wild-type spermatozoa. Remarkably, cytosolic Ca²⁺ levels in freshly isolated Tas1r1-deficient sperm were significantly higher compared to wild-type cells. Moreover, a significantly higher basal cAMP concentration was detected in freshly isolated Tas1r1-deficient epididymal spermatozoa, whereas upon inhibition of phosphodiesterase or sperm capacitation, the amount of cAMP was not different between both genotypes. Since Ca²⁺ and cAMP control fundamental processes during the sequential process of fertilization, we propose that the identified taste receptors and coupled signaling cascades keep sperm in a chronically quiescent state until they arrive in the vicinity of the egg - either by constitutive receptor activity and/or by tonic receptor activation by gradients of diverse chemical compounds in different compartments of the female reproductive tract.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0032354</identifier><identifier>PMID: 22427794</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abnormalities ; Amino acids ; Animals ; Apoptosis ; Aquaporins ; Biology ; Blotting, Western ; Calcimycin ; Calcium ; Calcium - metabolism ; Capacitation ; Cascades ; Chemical compounds ; Chemoreception ; Clonal deletion ; Compartments ; Cyclic AMP ; Cyclic AMP - metabolism ; Deoxyribonucleic acid ; DNA ; Female ; Fertilization ; Flagella ; Gene deletion ; Gene Expression ; Genital tract ; Genotypes ; Humans ; In vitro fertilization ; Infertility ; Kidney diseases ; Ligands ; Localization ; Luminescent Proteins - genetics ; Luminescent Proteins - metabolism ; Male ; Mammals ; Mice ; Mice, 129 Strain ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Transgenic ; Microscopy, Confocal ; Models, Biological ; Monosodium glutamate ; Neurobiology ; Neurosciences ; Nutrition ; Pharmacology ; Phosphodiesterase ; Proteins ; Rats ; Rats, Wistar ; Receptor mechanisms ; Receptors ; Receptors, G-Protein-Coupled - genetics ; Receptors, G-Protein-Coupled - metabolism ; Receptors, G-Protein-Coupled - physiology ; Red Fluorescent Protein ; Reproductive system ; Reverse Transcriptase Polymerase Chain Reaction ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Rodents ; Secretion ; Signal transduction ; Sperm ; Sperm Head - metabolism ; Spermatozoa ; Spermatozoa - metabolism ; Taste ; Taste buds ; Taste receptors ; Testis - cytology ; Testis - metabolism ; Tongue ; Toxicology ; Umami ; Zona pellucida</subject><ispartof>PloS one, 2012-02, Vol.7 (2), p.e32354</ispartof><rights>2012 Meyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meyer, Dorke</au><au>Voigt, Anja</au><au>Widmayer, Patricia</au><au>Borth, Heike</au><au>Huebner, Sandra</au><au>Breit, Andreas</au><au>Marschall, Susan</au><au>de Angelis, Martin Hrabé</au><au>Boehm, Ulrich</au><au>Meyerhof, Wolfgang</au><au>Gudermann, Thomas</au><au>Boekhoff, Ingrid</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expression of Tas1 taste receptors in mammalian spermatozoa: functional role of Tas1r1 in regulating basal Ca²⁺ and cAMP concentrations in spermatozoa</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-02-29</date><risdate>2012</risdate><volume>7</volume><issue>2</issue><spage>e32354</spage><pages>e32354-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>During their transit through the female genital tract, sperm have to recognize and discriminate numerous chemical compounds. However, our current knowledge of the molecular identity of appropriate chemosensory receptor proteins in sperm is still rudimentary. Considering that members of the Tas1r family of taste receptors are able to discriminate between a broad diversity of hydrophilic chemosensory substances, the expression of taste receptors in mammalian spermatozoa was examined. The present manuscript documents that Tas1r1 and Tas1r3, which form the functional receptor for monosodium glutamate (umami) in taste buds on the tongue, are expressed in murine and human spermatozoa, where their localization is restricted to distinct segments of the flagellum and the acrosomal cap of the sperm head. Employing a Tas1r1-deficient mCherry reporter mouse strain, we found that Tas1r1 gene deletion resulted in spermatogenic abnormalities. In addition, a significant increase in spontaneous acrosomal reaction was observed in Tas1r1 null mutant sperm whereas acrosomal secretion triggered by isolated zona pellucida or the Ca²⁺ ionophore A23187 was not different from wild-type spermatozoa. Remarkably, cytosolic Ca²⁺ levels in freshly isolated Tas1r1-deficient sperm were significantly higher compared to wild-type cells. Moreover, a significantly higher basal cAMP concentration was detected in freshly isolated Tas1r1-deficient epididymal spermatozoa, whereas upon inhibition of phosphodiesterase or sperm capacitation, the amount of cAMP was not different between both genotypes. Since Ca²⁺ and cAMP control fundamental processes during the sequential process of fertilization, we propose that the identified taste receptors and coupled signaling cascades keep sperm in a chronically quiescent state until they arrive in the vicinity of the egg - either by constitutive receptor activity and/or by tonic receptor activation by gradients of diverse chemical compounds in different compartments of the female reproductive tract.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22427794</pmid><doi>10.1371/journal.pone.0032354</doi><oa>free_for_read</oa></addata></record>
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subjects Abnormalities
Amino acids
Animals
Apoptosis
Aquaporins
Biology
Blotting, Western
Calcimycin
Calcium
Calcium - metabolism
Capacitation
Cascades
Chemical compounds
Chemoreception
Clonal deletion
Compartments
Cyclic AMP
Cyclic AMP - metabolism
Deoxyribonucleic acid
DNA
Female
Fertilization
Flagella
Gene deletion
Gene Expression
Genital tract
Genotypes
Humans
In vitro fertilization
Infertility
Kidney diseases
Ligands
Localization
Luminescent Proteins - genetics
Luminescent Proteins - metabolism
Male
Mammals
Mice
Mice, 129 Strain
Mice, Inbred BALB C
Mice, Inbred C57BL
Mice, Knockout
Mice, Transgenic
Microscopy, Confocal
Models, Biological
Monosodium glutamate
Neurobiology
Neurosciences
Nutrition
Pharmacology
Phosphodiesterase
Proteins
Rats
Rats, Wistar
Receptor mechanisms
Receptors
Receptors, G-Protein-Coupled - genetics
Receptors, G-Protein-Coupled - metabolism
Receptors, G-Protein-Coupled - physiology
Red Fluorescent Protein
Reproductive system
Reverse Transcriptase Polymerase Chain Reaction
RNA, Messenger - genetics
RNA, Messenger - metabolism
Rodents
Secretion
Signal transduction
Sperm
Sperm Head - metabolism
Spermatozoa
Spermatozoa - metabolism
Taste
Taste buds
Taste receptors
Testis - cytology
Testis - metabolism
Tongue
Toxicology
Umami
Zona pellucida
title Expression of Tas1 taste receptors in mammalian spermatozoa: functional role of Tas1r1 in regulating basal Ca²⁺ and cAMP concentrations in spermatozoa
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