The Involvement of GSTs in Mammalian Chemoperception: Comparison
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Glutathione transferases (GSTs) are ubiquitous key enzymes with different activities as transferases or isomerases. As key detoxifying enzymes, GSTs are expressed in the chemosensory organs. They fulfill an essential protective role because the chemosensory organs are located in the main entry paths of exogenous compounds within the body. In addition to this protective function, they modulate the perception process by metabolizing exogenous molecules, including tastants and odorants.

  • insects
  • glutathione transferase
  • taste

1. Chemoperception in Mammals

Chemoperception in mammals involves three components: olfaction, taste, and trigeminal sensations [20,21][1][2]. Olfaction is a fundamental sense that enables animals to locate their food and their sexual partners and to warn of danger, which is also of great importance for their well-being through the hedonic tone of food. In mammals, olfaction is assured by the olfactory system located in the nasal cavity. Odorant compounds are small, volatile chemicals, generally of a hydrophobic nature, that enter the body through the nostrils and solubilize within the nasal mucus. Odorants bind to olfactory receptors (ORs) located on the olfactory receptor neurons (ORNs) present in the main olfactory epithelium. Indeed, in addition to the olfactory epithelium, mammals have several accessory olfactory organs, such as the vomeronasal organ, the septal organ of Masera, and the Grueneberg ganglion, which all contain ORNs. These organs exhibit overlapping functions with the main olfactory system, but their specificities are not fully characterized. Each olfactory receptor neuron expresses only one type of OR [22][3]. ORNs are connected to the olfactory bulb, where the olfactory signal is processed and further transmitted to higher brain regions. This organization transforms a chemical signal into an electrical signal thanks to an efficient combinatorial code of odors permitted by the high diversity of olfactory receptors (380 for humans) [23][4].
In contrast to olfaction, which is important for various functions such as food search and enjoyment, reproduction, and survival, the sense of taste in mammals is exclusively devoted to the evaluation of food quality and is closely related to feeding behavior [24][5]. Taste compounds are divided into five qualities, namely, sweet (sugars), bitter (various compounds of organic or inorganic nature), sour (acidic compounds), salty (ionic inorganic compounds such as Na+), and umami (amino acids). In mammals, taste sensations result from the activation of taste receptors by taste compounds. Taste receptor cells assemble at the surface of the tongue or palate into small structures called “taste buds”, composed of approximately 100 cells. These taste buds are found in epithelial structures called “papillae”, classified into different types and present different structures and locations at the tongue surface. Papillae include fungiform, circumvallate, and foliate papillae. Taste receptor cells are linked by afferent nerves to the geniculate and petrosal ganglions, which mediate taste signals to the brain stem. Taste receptors from the T1R and T2R families are part of the class C and class A GPCR families, respectively [25][6]. They assemble through different functional homo- or heterodimers for T1Rs that are able to detect sweet (T1R2 + T1R3) and umami (T1R1 + T1R3) compounds. Monomeric T2Rs enable the detection of bitter molecules. Two other families of receptors have been proposed for the detection of sourness (PKD2L1) and saltiness (ENaC) [24][5].
In addition to the five qualities of taste, a few studies have evidenced a sixth sensation, which is more of a modulation of some of the basic tastes, namely the kokumi taste [26][7]. Kokumi means “rich taste” in Japanese and is associated with the reinforcement of umami, sweetness, and saltiness due to the presence of kokumi compounds. Kokumi compounds include both nonpeptide compounds and peptide compounds such as gamma-glutamyl peptides such as glutathione [27][8]. Kokumi compounds have been proposed to activate the calcium-sensing receptor (CaSR) to elicit the kokumi sensation [28][9]. Kokumi is an increasingly studied topic of research with great potential for flavor enhancement and food product development [26][7].
In addition to olfaction and taste, a third chemosensory sensation is related to the trigeminal system and enables the detection of trigeminal compounds such as astringent plant polyphenols, compounds present in foods eliciting a sensation of cooling (menthol) or burning (capsaicin), or carbonated drinks containing CO2 that trigger a prickly sensation [21][2]. Trigeminal compounds mainly stimulate transient receptor potential (TRP) channels present in sensory neurons of the oral mucosa, which convert chemical signals into electric activity. The identification of astringent compounds may either involve mechanoreceptors detecting changes in the friction forces at the surface of the oral mucosae or the transmembrane mucin MUC1, as recently proposed by ourthe group [29][10].
Olfaction, taste, and trigeminal sensations can be modulated by the metabolic activities present in the vicinity of the chemosensory receptors [30][11]. This metabolism involves enzymes such as glutathione transferases (GSTs). These have shown to be linked to both olfaction and taste perception, as explained in the following section.

2. Roles of GSTs in Mammalian Chemoperception

Many drug-metabolizing enzymes are present in the nasal cavity, within the nasal epithelium and mucus [31[12][13],32], as well as in the oral cavity, within the saliva and the oral mucosa [33,34][14][15]. These enzymes assure the protection of the epithelia and, notably, the olfactory receptor neurons from damage provoked by xenobiotics entering the nasal (or oral) cavity. In addition to their role in detoxification, some of these enzymes handle flavor molecules, thus producing flavor metabolites in the oronasal sphere [35,36,37,38][16][17][18][19]. All these enzymes, in addition to proteins able to bind flavor compounds such as odorant-binding proteins (OBPs), have an impact on both the quality and quantity of flavor compounds that activate chemoreceptors [30][11]. These molecular mechanisms have been named “perireceptor events” because they occur in the environment surrounding the chemoreceptors. In the context of mammalian olfaction, a body of evidence indicates that glutathione transferase is an important perireceptor enzyme acting on odorant detection modulation. Additionally, pioneering studies have started to investigate the potential role of glutathione transferases in taste perception. Both of these aspects are treated in this part of the review. Among the seven canonical mammalian GSTs identified thus far (alpha, mu, theta, pi, omega, sigma, and zeta [15][20]), alpha, mu, and pi classes of GSTs are common [39][21] among mammals [40][22].
In 1992, Ben-Arie and coworkers showed that the olfactory epithelium is the extrahepatic tissue in a rat model that exhibits the highest glutathione transfer activity with the chemical substrate chlorodinitrobenzene (CDNB), thus showing the strong expression of GSTs and suggesting a potential role in olfaction [41][23]. All GST classes were shown to be expressed in chemosensory organs in different mammalian species (Table 1). Glutathione transferase of the mu class was demonstrated in the rat nasal mucus and olfactory epithelium [4][24], supporting a previous study already showing GST expression in rat chemosensory mucosae [42][25]. Additionally, in the same study, the ability of recombinant rat GSTM2 to catalyze the transfer of glutathione to various odorant compounds, including aldehydes, ketones, and epoxides, was shown. Using a competition assay, GSTM2 was also found to be able to bind a large variety of odorants, most likely due to its ligandin properties [4][24]. Similar results were obtained for human GSTA1 and GSTP1, which are two GSTs that play roles in glutathione and ligand transfer for many odorous molecules and are expressed in the human respiratory epithelium [43][26]. Immunohistochemistry experiments showed the localization of human GSTs in ciliated cells (at the surface of the epithelium from the human olfactory vicinity), thus facilitating the entry of odorants into the epithelium. Furthermore, the first X-ray structure of a GST bound to a metabolized odorant enabled a fine analysis of its active site and its capacity to specifically recognize odorant molecules [43][26]. The crystal structure of human GSTA1 bound to the metabolite glutathionyl-dihydrocinnamaldehyde was analyzed and revealed the ability of the hydrophobic site of GSTA1 to strongly adapt to small hydrophobic volatile compounds. This property facilitates the binding of cinnamaldehyde and promotes the formation of the glutathione conjugate through a nucleophilic substitution, suppressing the carbon double bond of cinnamaldehyde [43][26].
GST expression levels were also shown to be associated with olfactory dysfunction. Zinc deficiency is linked to olfactory and gustatory dysfunction in mammals [44,45][27][28]. Interestingly, in rats, zinc deficiency is associated with a reduction in GST mRNA in some cell types of the olfactory epithelium (supporting cells [46][29]).
The involvement of GSTs in odorant metabolism has become increasingly documented; however, less evidence is available concerning the significance of these molecular mechanisms in odorant perception. In this context, experiments with a rabbit model enabled uresearchers  to reveal some clues on the role of GSTs in odorant signal termination. It was shown that the mammary pheromone, corresponding to the compound 2-methylbut-2-enal (2MB2), triggers the grasping of the mother rabbit mammae. Newborn rabbits are blind, and suckling-related behavior allows them to survive despite the short time that allows the mother to feed them [47][30]. This chemically triggered behavior is critical for pups, which are constrained to finding nipples within the five minutes of daily nursing. It has been shown that the mammary pheromone is metabolized to a glutathione conjugate in the olfactory epithelium of newborn rabbits, in accordance with a high early expression of glutathione transferases in this tissue [48][31]. Furthermore, it has been shown that this metabolism is also present in the nasal mucus of newborn rabbits due to the presence of glutathione transferases in this biological fluid based on proteomic analysis [49][32]. Additionally, the deregulation of this metabolism by in vivo washing of the nasal mucus, thus diminishing the glutathione conjugation of 2MB2, led to increased sensitivity of the behavior response in newborns exposed to the mammary pheromone. Similar results were obtained when the 2MB2 metabolism was reduced due to competition with another odorant substrate catalyzed by the same enzyme [50][33]. Decreasing the glutathione conjugation of the mammary pheromone allowed uresearchers to record behavioral responses with concentrations of mammary pheromone that were usually inactive. Glutathione conjugation to the mammary pheromone modifies its structure and thus terminates the odorant signal. This metabolization thus enables the newborn rabbit to remain responsive to the mammary pheromone by reinitializing the chemical signal. Rabbit GSTs catalyze glutathione conjugation with 2MB2 but can ensure the role of odorant signal termination for a wide range of other odorant compounds in mammals, including humans.
In addition to the nasal cavity, GSTs are expressed in the oral cavity, particularly in taste bud cells [51][34]. In rats, GSTM and GSTP were found to be expressed in both circumvallate and foliate papillae. The expression seems to be GST member-dependent; GSTA is not found in these papillae. Moreover, the results obtained in human and rat olfactory epithelia show differences with regard to the type of GST expressed in this tissue depending on the species, highlighting differences in their expression in chemosensory tissue between mammalian species [4,43][24][26]. GST was also found to be expressed in mammalian saliva, including human saliva [52][35]. Glutathione is found at a concentration of approximately 1 g/L in human saliva [53][36], enabling the GSH saturation of GSTP, the main human salivary GST, and then allowing it to catalyze glutathione conjugation at the maximal rate. Additionally, this salivary expression was shown to be modulated in humans in association with food behavior. Indeed, increased GST expression in response to specific diets, such as those rich in broccoli or coffee, was observed [52,54][35][37]. Recently, a study explored a possible link between GST expression in saliva and bitter taste perception [55][38]. GSTA1 and GSTP1 were identified in a cohort of 104 people, all of whom expressed the 2 GSTs in saliva. Additionally, people exhibiting ageusia or dysgeusia, included in this  study, showed significantly lower salivary GSTA1 levels than those in the saliva of the control group, suggesting possible relationships between salivary GST levels and taste function. In the same study, GSTA1 and GSTP1 interacted with various bitter compounds, including flavonoids and isothiocyanates. This last family of compounds is metabolized within the saliva [55][38]. The X-ray structures obtained between GSTs and isothiocyanates showed that different binding sites exist, whether the interactions imply glutathione conjugation (binding in the active site) or covalent adduction to an exposed cysteine in the GSTA1 ligand site.
All these elements suggest the involvement of GSTs in mammalian taste perception, in addition to olfaction. In addition, the level of expression of GST is correlated with disorders related to both taste and smell.
Table 1. Location and classes of GSTs within the mammal’s chemosensory organs.
Mammal Species Location GST Classes Ref.
Canis lupus familiaris Saliva Alpha, Mu, and Omega [56][39]
Equus caballus Saliva Pi [57][40]
Homo sapiens Olfactory mucus Alpha and Pi [58,59][41][42]
Olfactory epithelium Alpha, Mu, and Pi [43][26]
Saliva Alpha, Kappa, Mu Omega, Theta, and Pi [60,61][43][44]
Mus musculus Sensory cilia Alpha, Kappa, Mu, Omega, Tau, and Zeta [62][45]
Saliva Omega [63][46]
Oryctolagus cuniculus Olfactory mucus Alpha, Mu, and Pi [49][32]
Ovis aries Saliva Alpha [57][40]
Rattus norvegicus Sensory cilia Alpha and Mu [64][47]
Olfactory epithelium Alpha, Mu, and Pi [4,41][23][24]
Olfactory mucus Alpha, Mu, and Pi [4][24]

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