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Review
.2019 Feb 22;20(4):967.
doi: 10.3390/ijms20040967.

Taste Receptors: New Players in Sperm Biology

Affiliations
Review

Taste Receptors: New Players in Sperm Biology

Alice Luddi et al. Int J Mol Sci..

Abstract

Taste receptors were first described as sensory receptors located on the tongue, where they are expressed in small clusters of specialized epithelial cells. However, more studies were published in recent years pointing to an expression of these proteins not only in the oral cavity but throughout the body and thus to a physiological role beyond the tongue. The recent observation that taste receptors and components of the coupled taste transduction cascade are also expressed during the different phases of spermatogenesis as well as in mature spermatozoa from mouse to humans and the overlap between the ligand spectrum of taste receptors with compounds in the male and female reproductive organs makes it reasonable to assume that sperm "taste" these different cues in their natural microenvironments. This assumption is assisted by the recent observations of a reproductive phenotype of different mouse lines carrying a targeted deletion of a taste receptor gene as well as the finding of a significant correlation between human male infertility and some polymorphisms in taste receptors genes. In this review, we depict recent findings on the role of taste receptors in male fertility, especially focusing on their possible involvement in mechanisms underlying spermatogenesis and post testicular sperm maturation. We also highlight the impact of genetic deletions of taste receptors, as well as their polymorphisms on male reproduction.

Keywords: SNP; acrosome reaction; apoptosis; cAMP; calcium; epididymal sperm maturation; knockout mice; reproduction; sperm; spermatogenesis; spontaneous activity of GPCRs; taste receptor.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Transduction ofL-glutamate (umami), sweet and bitter stimuli in taste receptor cells on the tongue. Ligand-induced stimulation of the umami (Tas1r1+Tas1r3), sweet (Tas1r2+Tas1r3) or bitter receptors (Tas2rs) expressed at the apical membrane of type II taste cells within a taste bud (s. drawing in the left) activates in all cases a trimeric G protein composed of α-gustducin (Gαgus) and a complex consisting ofGβ3 andGγ13 (Gβ3/γ13). The released Gβγ-complex activates phospholipase C isoform β2 (PLCβ2) which then induces production of inositol 1,4,5-trisphosphate (IP3) and diacylglycerol (DAG); the second messenger IP3, in turn, activates the IP3 receptor (IP3R), an intracellular ion channel that allows Ca2+ release from the intracellular endoplasmic reticulum (ER) store (solid lines). Increase in intracellular Ca2+ then activates the transient receptor potential melastatin 5 (TRPM5), a plasma membrane localized sodium-selective channel which leads to depolarization and subsequent activation of voltage-gated sodium channels (Na+ channel) (dashed lines). The combined action of elevated Ca2+ and membrane depolarization opens the calcium homeostasis modulator (CALHM) channel, composed of CALHM1 and CALHM3 and pannexin1 channels, thus resulting in the release of the neurotransmitter ATP. At the same time, α-gustducin activates a phosphodiesterase (PDE) (solid lines), which catalyses the hydrolysis of the second messenger cyclic-AMP (cAMP) to AMP. For the sake of simplicity, regulatory effects of cAMP are omitted in the model.
Figure 2
Figure 2
Regulation of sperm production. (A) Hormonal control of spermatogenesis in the testis. Spermatogenesis in the testis is under endocrine and paracrine control, which is regulated by the hypothalamus and the pituitary gland also known as hypothalamic-pituitary-gonadal (HPG) axis. The hypothalamus regulates the hormonal activity of the anterior pituitary gland by secreting the tropic gonadotropin-releasing hormone (GnRH). Upon binding of GnRH to the anterior pituitary gland production of luteinizing hormone (LH) and follicle stimulating hormone (FSH) is elevated which upon blood stream transport stimulate testosterone secretion by intestinal Leydig cells and activation of Sertoli cells by FSH. Sertoli cells as cellular part of the tubular unit provide the optimal environment for the developing germ cells. A negative feedback of GnRH production in the hypothalamic neurons and LH/FSH secretion by the pituitary gland is exerted by high testosterone levels in the blood and secretion of the proteohormone inhibin-B by Sertoli cells. Arrow: positive (green) and negative (red) feedback. (B) Schematic drawing of a single seminiferous tubule with different stages of developing germ cells during spermatogenesis. The cross section shows that germ cells of a distinct developmental stage are organized in concentric layers within the tubule: In the most basal cell layer of the tubular unit, the immature spermatogonial stem cells are located, followed by spermatocytes, round spermatids and finally the most mature elongated spermatids which are concentrated in the lumen of the seminiferous tubule. The regulation of spermatogenesis is mainly mediated by surrounding interstitial Leydig cells which produce testosterone. The Sertoli cells within the seminiferous tubules have a nurturing role for the developing germ cell and transduce the action of FSH to the closely associated germ cells. (C) Schematic drawing showing a sagittal section through a whole testis and the overlying epididymis. The testis contains the tightly packed seminiferous tubules where spermatogenesis takes place. The elongated duct presenting the epididymis at the posterior margin of the testis is subdivided into three discrete segments (caput, corpus, cauda), where the luminal fluid of each region is characterized by a unique composition of different constituents, essential for post-testicular sperm maturation.
Figure 3
Figure 3
Schematic drawing showing the most critical steps during the sperm’s transit through the female genital tract before fertilizing the egg. The gamete interactions are a critical step on reproduction. Mammalian fertilization comprises: (i) sperm migration through the female reproductive tract (rheotaxis, thermotaxis and chemotaxis), (ii) biochemical and morphological changes to sperm (capacitation) and (iii) sperm-egg interaction in the oviduct (fertilization) (A). In the female reproductive tract, specifically in the isthmus of the uterus, the mammalian sperm must undergo a series of important modifications, such as tyrosine phosphorylation, cholesterol depletion, hyperpolarisation and finally hyperactivation. These complex priming processes, by which sperm become competent to fertilize an egg, are all together termed “capacitation” (B). Chemotaxis permit sperm to move into the ampulla and locate the egg,organized in a cell complex (C). The ovulated oocyte is covered by a multicellular cumulus oophorous. The fertilization takes place after specific steps: (i) binding ofzona pellucida, (ii) acrosome reaction, (iii) penetration of zona pellucida and (iv) final membrane fusion (D).
Figure 4
Figure 4
Experimental strategy to determine the impact of taste receptors for male reproduction. To gain a complete picture about a possible role of taste receptors for regulating male reproduction standard reproductive parameters (e.g., litter size, time to litter, sex ratio of pubs) were determined for breeding pairs of wild-type [WT] and taste receptor deficient animals [KO]. To evaluate whether genetic deletion of taste receptors affect spermatogenesis results of breeding experiments were supplemented by histopathological examinations of reproductive organs and isolated epididymal sperm cells; furthermore, reproductive-related hormones such as testosterone, LH, FSH and GnRH were quantified. To evaluate whether a loss of taste receptors modifies physiological sperm function, CASA (computer-assisted motility analysis) -based motility analyses were combined with experiments assessing the ability of sperm to respond to capacitation and acrosomal exocytosis stimuli.
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