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
Source: PubMed


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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    • "It is perhaps relevant that in the airway, stimulation of the bitter taste receptor raises the level of calcium and induces the release of b-defensins, while stimulation of the sweet taste receptor suppresses these effects (Lee et al., 2014). Intriguingly, male knockout mice deficient in the sweet receptor, Tas1R, are infertile, have raised intracellular sperm calcium concentrations and increased spontaneous acrosome reactions (Meyer et al., 2012), consistent with the modulation of sperm calcium dynamics by the loss of defensins. "
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    ABSTRACT: Recent work in humans and mouse has confirmed the involvement of the host defence β-defensin peptides in male fertility. We discuss here the work that has implicated β-defensins in sperm function including the identification of the epididymis as the predominant site of expression of the peptides and the in vivo consequences of mutation and deletion. The potential dual role of these peptides in the regulation of infection and control of sperm maturation is compelling and may combine their antimicrobial activity with the ability of these molecules to interact with cell membrane receptors and modulate ion transport.
    Preview · Article · Jul 2014 · Molecular Human Reproduction
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    • "In addition to the previously mentioned expression of chemosensory receptors in digestive system, several studies have shown that bitter, sweet, and umami receptors are expressed in testis [19] [20] [21] [22] [23]. Moreover, Fehr, et al. [24] demonstrated the expression of a-gustducin during mouse spermatogenesis and a segmental distribution of this G protein along the flagellum of mouse, rat, bull, and human spermatozoa suggesting a functional role in processing intracellular signals controlling sperm motility. "
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    ABSTRACT: During the transit in the female genital tract, spermatozoa are exposed to an environment that varies in composition from the vagina to the oviduct. Since G proteins α-gustducin and α-transducin are accepted as markers of chemosensitive cells, this study was aimed at assessing whether these proteins are expressed in boar germ cells. Ejaculated sperm extracts were analyzed by western blot and indirect immunofluorescence was performed on testis sections, smears of epididimal and ejaculated sermatozoa, sperm cells after in vitro induction of capacitation (IVC) and acrosome reaction (IVAR), and in sperm cells bound to zona pellucida during IVF. Basing on immunoblot results, both G proteins are present in boar sperm. In the testicular tissue sections α-gustducin and α-transducin positivity was recorded in the germinal cells near the tubular lumen while no positive signal was evident in spermatogonia located in the outer region of the seminiferous tubules. α-gustducin expression in epididimal and ejaculated spermatozoa was mainly detectable in both the acrosome and the principal piece of the tail while α-transducin was confined to the acrosome and midpiece. No changes after IVC and IVAR were observed, except for the disappearance of acrosomal positivity in reacted spermatozoa. In sperm bound to zona pellucida the G protein signal was congruent with that observed in IVAR cells. To the best of our knowledge, this is the first description of α-transducin in mammalian sperm and the first description of α-gustducin in boar sperm. Further studies are needed in order to clarify the possible role of these G proteins in sperm physiology.
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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.
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