L–Tryptophan Derivatives as Essential Compounds for Serotonin Synthesis: Comparison
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L–Tryptophan (Trp) and its derivatives, such as 5-hydroxy–L–tryptophan (5-OH-L-Trp), and tryptamine, are related to biochemical reactions that lead to serotonin synthesis in the brain’s neurotransmitters, lower levels of which are observed in clinically depressed patients.

  • L–tryptophan
  • 5-OH-L-Tryptophan

1. Introduction

As defined by the World Health Organization (WHO), depression is a common mental illness that affects more than 322 million people worldwide [1]. The typical symptoms of depression are persistent sadness, as well as the inability to feel feelings of happiness (anhedonia), sleep problems, loss of appetite, general fatigue, and cognitive problems. Depression is one of the leading causes of mental and physical disability worldwide [2].
The etiology of depression is a complex interplay of psychological, social, and biological factors. People who have experienced adverse life events, such as the death of a loved one or prolonged unemployment, are at an increased risk of developing depression. The presence of physical diseases such as cardiovascular and neurogenerative diseases may increase the risk of depression [3,4][3][4].
Interestingly, the COVID-19 pandemic increased depressive symptoms by five percentage points, from 27.8 to 32.8% of adults in the United States in 2021 compared to the first months of 2020 [5]. The increased risk of depressive symptoms and the development of depression may be related to the so-called pandemic environment and the introduction of “lockdowns” that restrict social activities in many countries. There is also growing evidence of COVID-19 disease and an increased risk of depression in recovered adults [6]. The mechanism of the development of depressive symptoms in recovered adults is not well understood yet. One of the possible explanations for this phenomenon may be related to the so-called “cytokine storm”—abnormally high levels of pro-inflammatory cytokines such as IL–1β, IL–6, IL–12, and tumor necrosis factor-alpha (TNF–α) and interferon gamma (INF–γ). A cytokine storm can contribute to neurotoxicity, blood barrier disruption, or even acute necrotizing encephalopathy [7].
Clinical psychopharmacology is a branch of science that deals with the description of the use of pharmacological agents for the treatment of specific psychopathological symptoms. The beginning of this field of knowledge dates to the 1940s and 1950s [8]. The first antidepressant drug was iproniazid, introduced in the treatment of tuberculosis in 1952 [9]. In tuberculosis patients treated with this drug, a significant improvement in mood was observed, unprecedented in patients in this clinical state [10]. After a few years, the mechanism of action of iproniazid was described, as it turned out to be an irreversible inhibitor of the monoamine oxidase (MAO) enzyme, which in turn led to an increase in the concentration of biogenic amines in the brain [11]. Iproniazid became a precursor drug for the first antidepressants, MAO inhibitors, including trancylopromine and phenelzine. Currently, iproniazide is not registered for the treatment of depression due to side effects, including liver damage [11].
Treatment of depression is based on the theory of monoamines introduced in the 1960s, which states that this disease is caused by a decreased level of monoamines (serotonin, norepinephrine, and dopamine) in the brain [12]. The mechanism of action of drugs used in the first line of depression treatment is inhibition of neuronal reuptake of monoamines from synaptic clefts, as in the case of selective serotonin reuptake inhibitors (SSRIs), for example, fluoxetine, citalopram, or sertraline, which reduce the activity of serotonin transporters [13]. Although these drugs are potent antidepressants, the cause of depression is not simply insufficient monoamine levels. SSRIs cause an immediate increase in serotonin transmission, while it takes several weeks for mood-elevating activity to develop in treated patients, which is associated with changes in the expression of serotonin-dependent receptors. Recent data on the development of depression have extended the theory of monoamines to include neurotrophic and neurogenic hypotheses [14,15][14][15]. Decreased levels of brain-derived neurotrophic factor (BDNF) are involved in the pathogenesis of depression [16]. BDNF is required for neurogenesis and neuroplasticity in the hippocampus [17]. In people with depression, BDNF expression is decreased in the limbic area of the brain due to neuronal atrophy. Serotonin and its receptors are involved in the regulation of BDNF levels and neurogenesis in the adult hippocampus. Chronic treatment with an SSRI has been shown to increase BDNF levels in humans and rodents [18,19][18][19]. Altered levels of other neurotrophins, such as neurotrophin–3 (NT–3), neurotrophin–4 (NT–4), and nerve growth factor (NGF), are also observed in patients with depressive disorders [20].
Medicinal/edible mushrooms and their mycelia from in vitro cultures are receiving increasing scientific attention for their potential to promote health. They are considered functional foods because of their ability to synthesize and accumulate different types of metabolites, which enhance their health-promoting properties and can be used as a supplement to the human diet. Studies show the multidirectional activity of medicinal mushrooms and their mycelium, including antioxidant, anticancer, anti-inflammatory, and immunostimulatory effects. Increasingly, there is also evidence of antidepressant activity [21,22,23][21][22][23].
Researchers at Penn State University published a research paper describing the link between eating mushrooms and depression [24]. The main conclusion of this population-based study, which analyzed mushroom consumption among US residents from 2005 to 2016, was that mushroom consumers are less likely to suffer from depression [24]. The results are consistent with previous small clinical studies [25,26,27][25][26][27]. However, the studies presented above did not investigate the potential mechanisms of the antidepressant effect of edible mushrooms.

2. L–Tryptophan Derivatives—Essential Compounds for Serotonin Synthesis

L–Tryptophan (Trp) and its derivatives, such as 5-hydroxy–L–tryptophan (5-OH-L-Trp), and tryptamine, are related to biochemical reactions that lead to serotonin synthesis in the brain’s neurotransmitters, lower levels of which are observed in clinically depressed patients [28] These compounds have been shown to scavenge free radicals and protect cells against oxidative stress, potentially reducing the risk of certain diseases such as cancer, neurogenerative diseases, and depression [29]. Trp is an essential amino acid and is considered an exogenic amino acid for the human body. Although its importance is the synthesis of various proteins, Trp is a precursor of serotonin (5-hydroxytryptamine) in the brain and gut. The biosynthetic pathway of serotonin is presented in Figure 1.
Antioxidants 12 00623 g001
Figure 1.
Pathway of serotonin (5–hydroxytryptamine) synthesis.
The serotonin metabolic pathway starts with the hydroxylation of Trp to 5-OH-L-Trp, which is decarboxylated to 5-hydroxytryptamine (serotonin). The limiting stage of serotonin synthesis is Trp hydroxylation by the enzyme Trp hydroxylase (TPH) and is not saturated at physiological brain tryptophan concentrations; therefore, serotonin synthesis in the brain is assumed to be directly connected with tryptophan transport into the brain [30,31,32][30][31][32]. Trp can be transported to the brain through a nutrient amino acid transporter protein that is involved in the transport of large neutral amino acids (LNAAs) such as valine, leucine, isoleucine, tyrosine, phenylalanine, and methionine from the bloodstream to the brain through the blood-brain barrier (BBB) [33]. The content of Trp that crosses the BBB by the nutrient amino acid transporter depends on the ratio of Trp and other LNAAs in plasma [33]. After meal ingestion, the levels of Trp and other LNAAs in plasma increase. As a result of a relatively low increase in Trp in comparison to other essential amino acids in plasma concentration, the plasma Trp/LNAA ratio decreases, and consequently, a reduced Trp influx to the brain is observed [33]. There are several factors that can influence Trp influx to the brain by influencing LNAA concentration in plasma, such as the ingestion of carbohydrates, the intake of protein amounts, or exercise. Ingestion of dietary carbohydrates led to elevated insulin levels. Insulin promotes the uptake of LNAAs in skeletal muscle, which leads to an increase in the Trp/LNAA ratio and consequently to Trp influx into brain tissue [34]. L–Tryptophan is not transported to muscle tissue because it bonds with albumin, while other LNAAs are not. Trp obtained from food can be transformed into serotonin in a limited amount. In mammals, approximately 95% of Trp is metabolized through the kynurenic metabolic pathway, whose products exhibit biological activity [35]. Fruiting bodies of edible mushrooms are a good source of non-hallucinogenic indole compounds such as Trp, 5-OH-L-Trp, and tryptamine (Table 1) [36,37,38][36][37][38].
Table 1.
Content of L–tryptophan, 5–hydroxy–L–tryptophan and tryptamine in fruiting bodies of selected medicinal mushrooms.
Species Source L-Tryptophan (mg/100 g dw) Tryptamine

(mg/100 g dw)		 5-Hydroxy-L-tryptophan

(mg/100 g dw)		 Ref.
Pleurotus citrinopileatus Fruiting bodies form commercial cultivation 1.29 ± 0.08 1.29 ± 0.08 128.89 ± 10.67 [39]
Pleurotus djamor 24.84 ± 0.97 3.54 ± 0.18 193.95 ± 17.69
Pleurotus ostreatus 5.79 ± 0.06 1.04 ± 0.15 67.45 ± 7.94
Auricularia cornea 0.16 ± 0.050 2.77 ± 0.050 7.35 ± 0.200 [40]
[51] Armillaria mellea Fruiting bodies from natural habitats 4.47 ± 0.01 2.74 ± 0.01 - z [41
Sarcodon imbricatus 1.31 ± 0.6 4.11 ± 0.26]
n/a [52] Imleria badia 0.68 ± 0.047 0.18 ± 0.001 - z
Tricholoma equestre 1.036 ± 0.093 0.598 ± 0.048 0.344 ± 0.031 [44] Boletus edulis 0.39 ± 0.020
Imleria badia 0.827 ± 0.0491.17 ± 0.003 0.18 ± 0.001
0.409 ± 0.045 Lactarius deliciosus - z - z 0.25 ± 0.017
Hydnum repandum 0.37 ± 0.09 1.46 ± 1.05 n/a [42]
Cantharellus cibarius 0.01 ± 0.002 0.01 ± 0.002 0.02 ± 0.003 [43]
Agaricus bisporus 0.39 ± 0.020 0.06 ± 0.003 - z
Sarcodon imbricatus 13.01 ± 0.01 22.12 ± 0.03 n/a
Macrolepiota procera 3.47 ± 0.050 0.92 ± 0.040 22.94 ± 0.500 [40]
Suillus bovinus 25.90 ± 0.200 3.15 ± 0.050 15.83 ± 0.500
Tricholoma equestre 2.851 ± 0.242 2.011 ± 0.141 0.586 ± 0.041 [44]
Calocera viscosa 1.26 ± 0.04 n/a 11.88 ± 0.19
n/a—data not available, z concentration lower than 0.001 mg/100 g dw.
The highest content of Trp and its hydroxylated derivative was observed in Pleurotus djamor (respectively, 24.84 and 193.95 mg/100 g dw) and Suillus bovinus (respectively, 25.9 and 15.83 mg/100 g dw) [39]. According to scientific data, nonfungal sources that contain high levels of Trp include soy seeds (680 mg/100 g dw), pumpkin seeds (580 mg/100 g dw), and spirulina (930 mg/100 g dw) [45]. Other researchers described that transgenic soybean plants were found to accumulate Trp at levels as high as 380 to 480 mg/100 g dw of seed flour, up to a 12-fold increase compared to Trp levels in non-transgenic seeds [46]. Wheat—durum 169 mg/100 g dw, rye 125 mg/100 g dw, barley 165 mg/100 g dw, chickpea 220 mg/100 g dw, lentil—red 139 mg/100 g dw, and kidney beans 240 mg/100 g dw are also considered good natural sources of Trp [45]. In contrast, the seeds of the Griffonia simplicifolia plant are considered one of the best natural sources of 5-OH-L-Trp [47,48][47][48]. Its content can be as high as 156 mg/g dw (16% of the seed weight) [48]. However, Maffei points out that mushrooms can also be a good source of this substance [47]. When analyzing the plant sources of Trp, it turns out that tomatoes are a good source (14.71 mg/100 g dw), while smaller amounts were determined in strawberries (5.7 mg/100 g dw), lettuce (2.5 mg/100 g dw), spinach (0.65 mg/100 g dw) or chicory (0.08 mg/100 g dw) [49]. Thus, it appears that both mycelium and fruiting bodies can provide an alternative source of Trp and Trp derivatives. The content of biologically active substances in mushroom samples is mainly measured after extracting them with various solvents such as methanol and ethanol from raw, lyophilized fruiting bodies. To determine the usage of selected edible mushrooms as sources of indole compounds, the influence of various types of thermal preparation of edible mushrooms on the content of biological active substances was analyzed [40,41][40][41]. Thermal processing (dry material suspended in water and thermostated at 100 °C for 60 min in a Soxhlet apparatus) was shown to result in approximately 2 times lower indole compound content after thermal processing compared to the unprocessed. However, Trp content increases relatively in processed samples compared to that of unprocessed one. The increase in Trp content can be explained by the fact that 5-OH-L-Trp or serotonin degradation at higher temperatures [40]. The results were confirmed in another study [41]. In conclusion, the method of preparing meals with mushrooms can affect the content of indole compounds because of their sensitivity to elevated temperature. However, thermally processed mushrooms remain a good source of Trp and 5-OH-L-Trp [40,41][40][41]. Today, dietary supplements containing lyophilized fruiting bodies, extracts, or even mycelium from edible mushroom species are available in community pharmacies or in stores with so-called healthy food. Mycelium can be obtained through in vitro cultures initiated from specially prepared parts of the fruiting body, the hymenial area. One of the most important advantages of in vitro cultures is the fact that the content of biological active substances does not differ between batches because the condition of the in vitro culture is monitored and maintained at specific parameters depending on the mushroom species. Studies have shown that the content of indole compounds in biomass from in vitro cultures can be much higher than that in fruiting bodies [50]. The content of selected indole compounds in mycelia from in vitro cultures is presented in Table 2.
Table 2.
Content of selected non-hallucinogenic indole compounds in mycelia of selected edible mushroom.
Species L-Tryptophan (mg/100 g dw) Tryptamine

(mg/100 g dw)		 5-Hydroxy-L-tryptophan

(mg/100 g dw)		 Ref.
Pleurotus citrinopileatus 7.82 ± 0.31 3.71 ± 0.34 368.67 ± 23.53 [39]
Pleurotus djamor 24.34 ± 1.44 n/d 703.56 ± 37.79
Pleurotus ostreatus 1.89 ± 0.04 1.03 ± 0.15 120.11 ± 20.12
Agaricus bisporus 14.00 ± 0.300 0.48 ± 0.050 12.50 ± 0.671
-
z
Calocera viscosa 1.79 ± 0.05 n/a 11.42 ± 0.20 [53]
Cantharellus cibarius 0.64 ± 0.013 - z 12.52 ± 0.671 [54]
n/a—data not available, n/d—not detected, z concentration lower than 0.001 mg/100 g dw.
In most cases, the content of Trp is higher in mycelia than in the fruiting bodies of selected edible mushroom species, especially Pleurotus citrinopileatus and Pleurotus djamor. The most notable change can be observed in the content of 5-OH-L-Trp, which is almost four times higher in the mycelium compared to the fruiting bodies [39]. Another advantage of making mycelium from edible mushroom species a dietary supplement is that powdered mycelium or mycelial extract does not have to be thermally processed, so thermolabile substances will not degrade. Modification of the composition of the in vitro medium, such as the addition of indole precursors—anthranilic acid and serine—can have a positive influence on the content of indole compounds in mycelia [55]. In one experimental study, in vitro culture medium was supplemented with various concentrations of serine or anthranilic acid (0.1–0.75 g/L). For in vitro cultures of A. bisporus and I. badia, the most optimal precursor concentration was 0.5 g/L of serine for A. bisporus or 0.5 g/L of anthranilic acid for both species analyzed according to the content of indole compounds. The addition of 0.5 g/L of serine to A. bisporus in vitro cultures resulted in the highest total concentration of indole compounds (186.37 mg/100 g dw). The addition of 0.5 g/L anthranilic acid to in vitro cultures of I. badia and A. bisporus resulted in the highest total concentration of indole compounds, 352.06 dw and >200 mg/100 g dw [55]. The liberation of biological substances, which is the number of substances released from the matrix of food or dietary supplement formula (tablets, hard capsules), can be measured in vitro using models of the human gastrointestinal tract. Therefore, only substances free of their matrix can be absorbed in the gastrointestinal tract. The analysis of the liberation of indole compounds was performed for Agaricus bisporus mycelia [56]. In the study, the content of indole compounds in artificial gastric and intestinal juice was measured after 5 time points—15, 30, 60, 90, and 120 min of incubation. The highest 5-OH-L-Trp content was established between 91.99 and 324.64 mg/100 g dw after 30 min of digestion in artificial gastric juice and after 150 min of incubation in artificial intestinal juice [56]. In a similar study on the release of indole compounds from fruiting bodies and Tricholoma equestre mycelia, 5-OH-L-Trp was released in the highest amount from freeze-dried mycelia after 120 min of incubation in artificial gastric juice (352.47 mg/100 g dw) and after 15 min of incubation in artificial gastric juice in the case of fruiting bodies (281.56 mg/100 g dw) [57]. For the fruiting bodies of Suilius bovinus, the highest content of released 5-OH-L-Trp was observed after 120 min of incubation in artificial gastric juice (237 mg/100 g dw) (for liberation study of Imleria badia, Boletus edulis, Cantharellus cibarius, Lactarius deliciosus, Leccinum scabrum, Armillaria mellea, Suillus luteus, Pleurotus ostreatus, Auricularia polytricha, see [58]). Based on the studies mentioned above, it can be concluded that indole compounds are released in the highest amount in artificial gastric juice compared to artificial intestinal juice. Trp is not readily liberated, regardless of whether it is from fruiting bodies or mycelia from in vitro cultures. However, 5-OH-L-Trp was one of the indole compounds that was released at the highest amount, regardless of the species analyzed [56,57,58][56][57][58]. Another important factor that should be considered when fruiting bodies or mycelium are thought to be a source of indole compounds is the bioavailability of these compounds. Bioavailability is a term used to describe the percentage or amount of a xenobiotic that reaches the systemic circulation [59]. In the case of the bioavailability analysis of secondary metabolites such as indole compounds, it will be the amount of indole compound that reaches the systemic circulation. The evaluation of the bioavailability of natural compounds in humans is rare due to requirements and restrictions imposed by ethics commissions, therefore, alternative methods involving, for example, the colon epithelial cells (CaCo-2) cell line are used to estimate the bioavailability of active substances [60]. In the study of indole absorption from Imleria badia mycelia, the CaCo-2 cell line was used to measure active transport, while semi-permeable membranes were used in the passive transport model after release of biological active substances in the human gastrointestinal tract model. The bioavailability of 5–hydroxy–L–tryptophan ranged from 5.21 to 11.92% using active transport modes (depending on mycelial in vitro culture conditions—an addition of zinc (VI) sulfate or zinc hydrogen aspartate). Through the passive transport model, 5–hydroxy–L–tryptophan accounted for 2% of the compound released into artificial digestive juices [61]

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