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Effects of Duodenal 5-Hydroxytryptophan Perfusion on Melatonin Synthesis in GI Tract of Sheep

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Effects of Duodenal 5-Hydroxytryptophan Perfusion on Melatonin Synthesis in GI Tract of Sheep molecules Article Effects of Duodenal 5-Hydroxytryptophan Perfusion on Melatonin Synthesis in GI Tract of Sheep Jun Pan 1,†, Fengming Li 1,†, Caidie Wang 1, Xiaobin Li 1, Shiqi Zhang 1, Wenjie Zhang 1, Guodong Zhao 1, Chen Ma 1, Guoshi Liu 2 and Kailun Yang 1,*,† 1 College of Animal Science, Xinjiang Agricultural University, Urumqi 830052, China; [email protected] (J.P.); [email protected] (F.L.); [email protected] (C.W.); [email protected] (X.L.); [email protected] (S.Z.); [email protected] (W.Z.); [email protected] (G.Z.); [email protected] (C.M.) 2 College of Animal Science and Technology, China Agricultural University, Beijing 100083, China; [email protected] * Correspondence: [email protected]; Tel.: +86-099-1876-2603 † The authors contributed equally to this work. Abstract: The purpose of this study is to investigate the potential effects of 5-hydroxytryptophan (5-HTP) duodenal perfusion on melatonin (MT) synthesis in the gastrointestinal (GI) tract of sheep. 5-hydroxytryptophan is a precursor in the melatonin synthetic pathway. The results showed that this method significantly increased melatonin production in the mucosa of all segments in GI tract including duodenum, jejunum, ileum, cecum and colon. The highest melatonin level was identified in the colon and this indicates that the microbiota located in the colon may also participate in the melatonin production. In addition, portion of the melatonin generated by the GI tract can pass the liver metabolism and enters the circulation via portal vein. The current study provides further Citation: Pan, J.; Li, F.; Wang, C.; Li, evidence to support that GI tract is the major site for melatonin synthesis and the GI melatonin also X.; Zhang, S.; Zhang, W.; Zhao, G.; contributes to the circulatory melatonin level since plasma melatonin concentrations in 5-HTP treated Ma, C.; Liu, G.; Yang, K. Effects of groups were significantly higher than those in the control group. In conclusion, the results show Duodenal 5-Hydroxytryptophan that 10–50 mg of 5-HTP flowing into the duodenum within 6 h effectively improve the production of Perfusion on Melatonin Synthesis in melatonin in the GI tract and melatonin concentration in sheep blood circulation during the day. GI Tract of Sheep. Molecules 2021, 26, 5275. https://doi.org/10.3390/ Keywords: sheep; intestinal mucosa; 5-hydroxytryptophan; melatonin; gastrointestinal track molecules26175275 Academic Editor: Raffaele Capasso 1. Introduction Received: 4 August 2021 Melatonin (MT) has multiple biological functions in mammals, including sleep pro- Accepted: 28 August 2021 Published: 31 August 2021 motion, immunoregulation, and antibacterial, anti-inflammatory, as well as antioxidative activities [1–4]. Since the first isolation of MT from bovine pineal gland [5], MT was believed Publisher’s Note: MDPI stays neutral to be exclusively produced in the pineal gland until MT was detected in the retina, Hard- with regard to jurisdictional claims in erian gland, cerebellum [6] and in the intestinal chromaffin cells [7]. These observations published maps and institutional affil- have expanded the melatonin synthetic sites to extrapineal tissues and organs. Currently, it iations. has been reported that melatonin is synthesized by mitochondria and many functions of melatonin is also mediated by the mitochondria [8]. As a result, virtually, every cell with mitochondria has the capacity to synthesize melatonin. For example, the total amounts of MT produced in the gastrointestinal tract (GI Tract) were estimated to be approximately 400 times more than that produced in the pineal gland [9]. As to its synthesis, tryptophan Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. (Trp) is its original precursor of melatonin in mammals [10]. First, Trp is decarboxylated to This article is an open access article 5-hydroxytryptophan (5-HTP) by the tryptophan hydroxylase (TPH) [11], and then 5-HTP distributed under the terms and is transformed into serotonin (5-HT) by aryl amino acid decarboxylase (AADC), and 5-HT is conditions of the Creative Commons converted to N-acetyl-5-hydroxytryptamine by a rate-limiting enzymes, arylalkylamine-N- Attribution (CC BY) license (https:// acetyltransferase (SNAT, previously AANAT), finally, the N-acetyl-5-hydroxytryptamine is creativecommons.org/licenses/by/ converted to melatonin by N-acetyl-5-hydroxytryptamine methyltransferase (ASMT, previ- 4.0/). ously HIOMT) [12]. Melatonin synthetic pathway in mammals is illustrated in the Figure1 . Molecules 2021, 26, 5275. https://doi.org/10.3390/molecules26175275 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 14 decarboxylase (AADC), and 5-HT is converted to N-acetyl-5-hydroxytryptamine by a rate-limiting enzymes, arylalkylamine-N-acetyltransferase (SNAT, previously AANAT), finally, the N-acetyl-5-hydroxytryptamine is converted to melatonin by Molecules 2021, 26, 5275 N-acetyl-5-hydroxytryptamine methyltransferase (ASMT, previously HIOMT) 2[12] of 13. Melatonin synthetic pathway in mammals is illustrated in the Figure 1. FigureFigure 1. 1. MelatoninMelatonin synthetic synthetic pathway pathway in inmammals. mammals. TPH: TPH: tryptophan tryptophan hydroxylase hydroxylase,, AADC: AADC: aryl aryl aminoamino acid acid decarboxylase decarboxylase,, SNAT: SNAT: serotonin serotonin N N-acetyltrasferase,-acetyltrasferase, ASMT: ASMT: N N-acetyltraptamine-acetyltraptamine me- methyl- thyltrasferase,trasferase, MAO: MAO: monoamine monoamine oxidase. oxidase. MTMT plays plays important important roles roles in in the the improvement improvement of of the the yields yields and and quality quality of of animal animal products.products. For For example,example, itit improves improves the the meat meat quality quality and and quantity quantity of cashmere of cashmeregoats [goats13,14] , [13,14]reduces, reduces somatic somatic cell count cell count and mastitis and mastitis in dairy in dairy cattle cattle to improve to improve the the quality quality of theof themilk milk [15 ,[15,16]16]. Currently,. Currently, in husbandryin husbandry industrial, industrial, the the methods methods used used to regulationto regulation of MTof MTlevels levels in animals in animals are primarilyare primarily to alter to thealter light/dark the light/dark cycle ofcycle the of environments the environments [17,18], [17,18]or by, implantationor by implantation [19,20], [19,20] injection, injection [21], and [21] oral, and administration oral administration [22] of [22] MT. of As MT. to As the exogenous melatonin administration, several factors should be considered including its to the exogenous melatonin administration, several factors should be considered in- bioavailability, acting duration, economic benefit, and delivery methods [22]. Addition- cluding its bioavailability, acting duration, economic benefit, and delivery methods [22]. ally, exogenous MT supplementation seems to reduce endogenous MT synthesis and to Additionally, exogenous MT supplementation seems to reduce endogenous MT synthe- down-regulate expression of the MT receptors [23–25]. Thus, researchers have tried to sis and to down-regulate expression of the MT receptors [23–25]. Thus, researchers have improve melatonin production by manipulating the availability of MT precursor, that is, to tried to improve melatonin production by manipulating the availability of MT precursor, give Trp to animals. The results are variable. Some studies indicated that only 1–2% of Trp that is, to give Trp to animals. The results are variable. Some studies indicated that only ingested were converted into 5-HT depending on the species [26]. Several studies have 1–2% of Trp ingested were converted into 5-HT depending on the species [26]. Several shown that Trp supply increases blood MT levels in the tested animals [27–30]. However, studies have shown that Trp supply increases blood MT levels in the tested animals this increase only occurs nocturnally, or at certain time points [31,32], while others reported [27–30]. However, this increase only occurs nocturnally, or at certain time points [31,32], the negative results with no increased melatonin production [33,34]. Specifically to sheep, while others reported the negative results with no increased melatonin production a study showed that 5-HTP supply increased the MT synthesis, but Trp supply failed to [33,34]achieve. Specifically this goal [35 to]. sheep, Due to a thestudy uncertainty showed that of Trp 5-HTP supply supply on melatonin increased productionthe MT syn- in thesis,sheep, but we Trp select supply the 5-HTP failed as to the achieve precursor this goal to feed [35] sheep. Due and to the attempt uncertainty to identify of Trp whether sup- plythis on treatment melatonin can production improve the in melatoninsheep, we productionselect the 5- inHTP sheep. as the Indeed, precursor we have to feed found sheep that andfeeding attempt 5-HTP to identify increases whether MT content this oftreatment blood plasma can improve from the the jugular melatonin vein inproduction sheep [36, 37in ] sheep.which Indeed, mainly reflectswe have the found pineal tha originatedt feeding melatonin5-HTP increases [9,38]. FewMT content studies haveof blood investigated plasma fromthe effects the jugular of 5-HTP vein supply in sheep on the[36,37] GI tract which melatonin mainly synthesisreflects the [39 pineal], especially, originated the different mela- toninsegments [9,38] of. Few GI tract.studies GI have tract investigated is considered the as effects one of of the 5 largest-HTP
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