Abstract
BackgroundDuring 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.Methodology/Principal FindingsThe 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.Conclusions/SignificanceSince 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.
Highlights
IntroductionDuring their journey through the female genital tract, mammalian sperm are exposed to a wide range of compounds of different origins and chemical properties [1]: From the anterior vagina towards the mature oocyte in the fallopian tube of the oviduct, ejaculated sperm have to sense slight variations in the composition of diverse environmental chemical cues in the different fluids of the female genital tract, like changes in the concentrations of carbohydrates [2], different levels of single amino acids [3,4], or variations in ion composition and pH [5,6].For the essential proper chemical communication with the egg’s environment, and with the oocyte itself, sperm are functionally reprogrammed or capacitated within the female’s genital tract [7,8,9]
Conclusions/Significance: 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
PCR-reactions with L8 primers and those with a b-actin primer pair set (Fig. 1; right panel, [actin]) resulted in amplification fragments of the predicted size without any additional amplification products, ensuring that genomic cDNA would not lead to erroneously positive reverse transcriptionpolymerase chain reaction (RT-PCR)-results
Summary
During their journey through the female genital tract, mammalian sperm are exposed to a wide range of compounds of different origins and chemical properties [1]: From the anterior vagina towards the mature oocyte in the fallopian tube of the oviduct, ejaculated sperm have to sense slight variations in the composition of diverse environmental chemical cues in the different fluids of the female genital tract, like changes in the concentrations of carbohydrates [2], different levels of single amino acids [3,4], or variations in ion composition and pH [5,6].For the essential proper chemical communication with the egg’s environment, and with the oocyte itself, sperm are functionally reprogrammed or capacitated within the female’s genital tract [7,8,9]. Chemical orientation within the female tract entirely occurs in an aqueous environment, whereas olfactory receptors usually detect volatile, lipophilic substances [25], which are unlikely to be dissolved in appropriate concentrations in this aqueous milieu During their transit through the female genital tract, sperm have to recognize and discriminate numerous chemical compounds. 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
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