Expression of Tas1 Taste Receptors in Mammalian Spermatozoa: Functional Role of Tas1r1 in Regulating Basal Ca and cAMP Concentrations in Spermatozoa

Walther-Straub Institute of Pharmacology and Toxicology, Ludwig-Maximilians-University, Munich, Germany.
PLoS ONE (Impact Factor: 3.23). 02/2012; 7(2):e32354. DOI: 10.1371/journal.pone.0032354
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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.

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Available from: Andreas Breit, Oct 08, 2015
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    • "The expression of T1R3 and α-gustducin, but not T1R2, was recently described in human spermatozoa [29] and male reproductive organs [30▪▪]. Mosinger et al.[30▪▪], using double-knockout mice for T1R3−/− and α-gustducin (Gnat−/−) expressing transgenic human T1R3, showed that when human T1R3 was blocked by a lactisole analogue (clofibrate), male mice exhibited sterility and pathological changes in their reproductive organs [30▪▪]. "
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    ABSTRACT: This review summarizes and discusses the current knowledge about the physiological roles of the sweet taste receptor in oral and extraoral tissues. The expression of a functional sweet taste receptor has been reported in numerous extragustatory tissues, including the gut, pancreas, bladder, brain and, more recently, bone and adipose tissues. In the gut, this receptor has been suggested to be involved in luminal glucose sensing, the release of some satiety hormones, the expression of glucose transporters, and the maintenance of glucose homeostasis. More recently, the sweet taste receptor was proposed to regulate adipogenesis and bone biology. The perception of sweet taste is mediated by the T1R2/T1R3 receptor, which is expressed in the oral cavity, wherein it provides input on the caloric and macronutrient contents of ingested food. This receptor recognizes all the chemically diverse compounds perceived as sweet by human beings, including natural sugars and sweeteners. Importantly, the expression of a functional sweet taste receptor has been reported in numerous extragustatory tissues, wherein it has been proposed to regulate metabolic processes. This newly recognized role of the sweet taste receptor makes this receptor a potential novel therapeutic target for the treatment of obesity and related metabolic dysfunctions, such as diabetes and hyperlipidemia.This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivitives 3.0 License, where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially.
    04/2014; 17(4). DOI:10.1097/MCO.0000000000000058
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    • "Taste receptors are also expressed by sperm. Most remarkably, in mice carrying a humanized T1R3 gene, infertility is induced by treatment with a human T1R3-specific blocker (Meyer et al., 2012). These studies point to the importance of developing chemicals that target taste receptors for treating conditions ranging from asthma to infer- tility. "
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    ABSTRACT: Five canonical tastes, bitter, sweet, umami (amino acid), salty, and sour (acid), are detected by animals as diverse as fruit flies and humans, consistent with a near-universal drive to consume fundamental nutrients and to avoid toxins or other harmful compounds. Surprisingly, despite this strong conservation of basic taste qualities between vertebrates and invertebrates, the receptors and signaling mechanisms that mediate taste in each are highly divergent. The identification over the last two decades of receptors and other molecules that mediate taste has led to stunning advances in our understanding of the basic mechanisms of transduction and coding of information by the gustatory systems of vertebrates and invertebrates. In this Review, we discuss recent advances in taste research, mainly from the fly and mammalian systems, and we highlight principles that are common across species, despite stark differences in receptor types.
    Neuron 03/2014; 81(5):984-1000. DOI:10.1016/j.neuron.2014.02.022 · 15.05 Impact Factor
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    • "Owing to the lack of anti-T1R2, the authors of the above study could not assess T1R2 expression in mature spermatozoa (Meyer et al., 2012). In one study, T1R1 knockout mice and wild-type controls showed similar reproductive characteristics, such as sperm concentration, testis histology, sperm morphology, sperm mobility and testosterone level (Meyer et al., 2012). In the tas1r1-null animals, treatment with zona pellucida induced significant acrosome reaction, indicating that tas1r1 deletion did not influence the ability of sperm to bind to the zona pellucida and activate coupled intracellular signalling cascades. "
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    ABSTRACT: In mammals, the sense of taste helps in the evaluation and consumption of nutrients, and in avoiding toxic substances and indigestible materials. Distinct cell types expressing unique receptors detect each of the five basic tastes: salty, sour, bitter, sweet and umami. The latter three tastes are detected by two distinct families of G protein-coupled receptors: T2Rs and T1Rs. Interestingly, these taste receptors have been found in tissues other than the tongue, such as the digestive system, respiratory system, brain, testis and spermatozoa. The functional implications of taste receptors distributed throughout the body are unknown. We therefore reviewed the remarkable advances in our understanding of the molecular basis of taste perception in 'taste' and 'non-taste' tissues. We also present our speculations on the direction of further research in the field of male reproduction.
    Molecular Human Reproduction 02/2013; 19(6). DOI:10.1093/molehr/gat009 · 3.75 Impact Factor
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