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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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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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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Meyer et al. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-79467e28d946fc8b4732f3f83a08e974be0b08983fca44abb5f398fdeb2e388b3</citedby><cites>FETCH-LOGICAL-c521t-79467e28d946fc8b4732f3f83a08e974be0b08983fca44abb5f398fdeb2e388b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3303551/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3303551/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22427794$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Meyer, Dorke</creatorcontrib><creatorcontrib>Voigt, Anja</creatorcontrib><creatorcontrib>Widmayer, Patricia</creatorcontrib><creatorcontrib>Borth, Heike</creatorcontrib><creatorcontrib>Huebner, Sandra</creatorcontrib><creatorcontrib>Breit, Andreas</creatorcontrib><creatorcontrib>Marschall, Susan</creatorcontrib><creatorcontrib>de Angelis, Martin Hrabé</creatorcontrib><creatorcontrib>Boehm, Ulrich</creatorcontrib><creatorcontrib>Meyerhof, Wolfgang</creatorcontrib><creatorcontrib>Gudermann, Thomas</creatorcontrib><creatorcontrib>Boekhoff, Ingrid</creatorcontrib><title>Expression of Tas1 taste receptors in mammalian spermatozoa: functional role of Tas1r1 in regulating basal Ca²⁺ and cAMP concentrations in spermatozoa</title><title>PloS one</title><addtitle>PLoS One</addtitle><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.</description><subject>Abnormalities</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Aquaporins</subject><subject>Biology</subject><subject>Blotting, Western</subject><subject>Calcimycin</subject><subject>Calcium</subject><subject>Calcium - metabolism</subject><subject>Capacitation</subject><subject>Cascades</subject><subject>Chemical compounds</subject><subject>Chemoreception</subject><subject>Clonal deletion</subject><subject>Compartments</subject><subject>Cyclic AMP</subject><subject>Cyclic AMP - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Female</subject><subject>Fertilization</subject><subject>Flagella</subject><subject>Gene deletion</subject><subject>Gene Expression</subject><subject>Genital tract</subject><subject>Genotypes</subject><subject>Humans</subject><subject>In vitro fertilization</subject><subject>Infertility</subject><subject>Kidney diseases</subject><subject>Ligands</subject><subject>Localization</subject><subject>Luminescent Proteins - genetics</subject><subject>Luminescent Proteins - metabolism</subject><subject>Male</subject><subject>Mammals</subject><subject>Mice</subject><subject>Mice, 129 Strain</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>Microscopy, Confocal</subject><subject>Models, Biological</subject><subject>Monosodium glutamate</subject><subject>Neurobiology</subject><subject>Neurosciences</subject><subject>Nutrition</subject><subject>Pharmacology</subject><subject>Phosphodiesterase</subject><subject>Proteins</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Receptor mechanisms</subject><subject>Receptors</subject><subject>Receptors, G-Protein-Coupled - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - 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> |
fulltext | fulltext |
identifier | ISSN: 1932-6203 |
ispartof | PloS one, 2012-02, Vol.7 (2), p.e32354 |
issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1333201423 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
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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