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Biochemical Properties of Tyrosinase from Aspergillus Terreus And molecules Article Biochemical Properties of Tyrosinase from Aspergillus terreus and Penicillium copticola; Undecanoic Acid from Aspergillus flavus, an Endophyte of Moringa oleifera, Is a Novel Potent Tyrosinase Inhibitor Hanaa Salah Maamoun 1, Gamal H. Rabie 1, Ibrahim Shaker 2, Bothaina A. Alaidaroos 3 and Ashraf S. A. El-Sayed 1,* 1 Enzymology and Fungal Biotechnology Lab., Botany and Microbiology Department, Faculty of Science, Zagazig University, Zagazig 44519, Egypt; [email protected] (H.S.M.); [email protected] (G.H.R.) 2 Limnology Department, Central Laboratory of Aquaculture Research, Tell El Kebir 41626, Egypt; [email protected] 3 Biology Department, Faculty of Science, King Abdulaziz University, Jeddah 21955, Saudi Arabia; [email protected] * Correspondence: [email protected] or [email protected] Abstract: Tyrosinase is a copper-containing monooxygenase catalyzing the O-hydroxylation of tyrosine to 3,4-dihydroxyphenylalanine then to dopaquinone that is profoundly involved in melanin synthesis in eukaryotes. Overactivation of tyrosinase is correlated with hyperpigmentation that is Citation: Salah Maamoun, H.; Rabie, metabolically correlated with severe pathological disorders, so, inhibition of this enzyme is the most G.H.; Shaker, I.; A. Alaidaroos, B.; effective approach in controlling the overproduction of melanin and its hazardous effects. Thus, El-Sayed, A.S.A. Biochemical searching for a powerful, selective inhibitor of human tyrosinase to limit the hyper-synthesis of Properties of Tyrosinase from melanin is a challenge. Unlike the difficulty of overexpression of human tyrosinase, using fungal Aspergillus terreus and Penicillium tyrosinase as a model enzyme to the human one to evaluate the mechanistics of enzyme inhibition in copticola; Undecanoic Acid from response to various compounds is the most feasible strategy. Thus, the purification of highly catalytic- Aspergillus flavus, an Endophyte of Moringa oleifera, Is a Novel Potent efficient fungal tyrosinase, exploring a novel inhibitor, and evaluating the mechanistics of enzyme Tyrosinase Inhibitor. Molecules 2021, inhibition are the main objectives of this work. Aspergillus terreus and Penicillium copticola were 26, 1309. https://doi.org/10.3390/ reported as the most potential tyrosinase producers. The biochemical properties suggest that this molecules26051309 enzyme displays a higher structural and catalytic proximity to human tyrosinase. Upon nutritional bioprocessing by Plackett–Burman design, the yield of tyrosinase was increased by about 7.5-folds, Academic Editor: Elisa Nuti compared to the control. The purified tyrosinase was strongly inhibited by kojic acid and A. flavus DCM extracts with IC50 values of 15.1 and 12.6 µg/mL, respectively. From the spectroscopic analysis, Received: 28 January 2021 the main anti-tyrosinase compounds of A. flavus extract was resolved, and verified as undecanoic Accepted: 20 February 2021 acid. Further studies are ongoing to unravel the in vivo effect and cytotoxicity of this compound in Published: 1 March 2021 fungi and human, that could be a novel drug to various diseases associated with hyperpigmentation by melanin. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Keywords: Aspergillus terreus; Penicillium copticola; tyrosinase; kojic acid; undecanoic acid published maps and institutional affil- iations. 1. Introduction Tyrosinase is a copper-containing monooxygenase (EC 1.14.18.1) catalyzing the O- Copyright: © 2021 by the authors. O O Licensee MDPI, Basel, Switzerland. hydroxylation of monophenols into -diphenols (monophenolase) and oxidation of - This article is an open access article diphenols to O-quinones (diphenolase) [1]. Tyrosinase is profoundly involved in melanin distributed under the terms and synthesis via O-hydroxylation of tyrosine into 3,4-dihydroxyphenylalanine (L-DOPA) and conditions of the Creative Commons oxidation of L-DOPA into dopaquinone, that further transformed into melanin through Attribution (CC BY) license (https:// multiple enzymatic processes [2]. Practically, the biosynthetic pathway of melanin in creativecommons.org/licenses/by/ microorganisms is quite different from humans; in fungi, melanin was mainly synthe- 4.0/). sized from 1,8-dihydroxynaphthalene (DHN) precursors (DHN-melanin) [3,4] through the Molecules 2021, 26, 1309. https://doi.org/10.3390/molecules26051309 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x 2 of 19 Molecules 2021, 26, 1309 through multiple enzymatic processes [2]. Practically, the biosynthetic pathway of mela-2 of 18 nin in microorganisms is quite different from humans; in fungi, melanin was mainly syn- thesized from 1,8-dihydroxynaphthalene (DHN) precursors (DHN-melanin) [3,4] through the polyketide pathway, with maonyl-CoA as the starter and extender units [5]. In hu- polyketide pathway, with maonyl-CoA as the starter and extender units [5]. In humans mans and few microbes, melanin pigments are synthesized by L-DOPA pathway based and few microbes, melanin pigments are synthesized by L-DOPA pathway based on ty- on tyrosine as precursors that hydroxylated to L-DOPA, then oxidized into dopaquinone androsine further as precursors into melanin that pigment hydroxylated [6]. Melanin to L-DOPA, is the main then oxidizedpigment in into skin, dopaquinone hair, and eyes and further into melanin pigment [6]. Melanin is the main pigment in skin, hair, and eyes of of human, produced by melanocytes through melanogenesis [7], which is the most im- human, produced by melanocytes through melanogenesis [7], which is the most important portant photoprotective factor in response to ultraviolet radiation damage from the sun photoprotective factor in response to ultraviolet radiation damage from the sun [8]. The [8]. The melanogenesis process is initiated with the oxidation of L-tyrosine to dopaquinone melanogenesis process is initiated with the oxidation of L-tyrosine to dopaquinone (DQ) by (DQ) by tyrosinase and the resulting quinone serves as a substrate for the synthesis of tyrosinase and the resulting quinone serves as a substrate for the synthesis of eumelanin eumelanin and pheomelanin [9]. The synthesized DQ undergoes intramolecular cycliza- and pheomelanin [9]. The synthesized DQ undergoes intramolecular cyclization to produce tion to produce indoline, leukodopachrome (cyclodopa), and dopachrome [2,9,10]. Do- indoline, leukodopachrome (cyclodopa), and dopachrome [2,9,10]. Dopachrome gradu- pachrome gradually decomposes to give dihydroxyindole (DHI) and dihydroxyindole-2- ally decomposes to give dihydroxyindole (DHI) and dihydroxyindole-2-carboxylicacid carboxylicacid (DHICA)[9]. The biosynthetic mechanisms of melanin in fungi is illus- (DHICA) [9]. The biosynthetic mechanisms of melanin in fungi is illustrated in Scheme1 . trated in Scheme 1. Melanin is a negatively charged amorphous polymer derived from Melanin is a negatively charged amorphous polymer derived from multiple enzymatic multipleand autoxidative enzymatic polycondensationand autoxidative polycon of variousdensation quinone of groupsvarious ofquinone hydrophobic groups proper-of hy- drophobicties [10]. Melaninproperties pigments [10]. Melanin retain pigments the ability retain to deactivate the ability free to deactivate radicals, peroxidesfree radicals, and peroxidesabsorb heavy and metalsabsorb andheavy toxic metals electrophilic and toxic metabolites, electrophilic thus metabolites, exhibiting profoundthus exhibiting antioxi- profounddant activity antioxidant [4,5]. Melanin activity pigments [4,5]. Melanin absorb lightpigments in a wideabsorb spectrum light in range a wide enclosing spectrum UV, rangetheir absorptionenclosing UV, intensity their decreasesabsorption slowly intensit withy decreases increasing slowly light wavelengths,with increasing and light upon wavelengths,interaction with and theupon UV interaction radiation (240–300with the UV nm), radiation photoionization (240–300 and nm), subsequent photoionization partial anddestruction subsequent of melaninspartial destruction can be observed of melanins [5,11]. can be observed [5,11]. Scheme 1. Scheme 1. BiosynthesisBiosynthesis of of melani melaninn in in human human and and fungi. fungi. The theory of stimulating melanogenesis upon overexposure to UV light stated the damageThe theory to the DNAof stimulating of melanocyte, melanogenesis thus over-inducting upon overexposure the melanocyte-stimulating to UV light stated the hor- damagemones (MSH),to the DNA that inof turnmelanocyte, stimulates thus the over tyrosinases-inducting activities, the melanocyte-stimulating multiplying the numbers hor- of monesmelanocytes (MSH), [that6,10 ,in12 ,turn13]. Thestimulates hyper-pigmentation, the tyrosinases dueactivities, to the multiplying overactivity the of tyrosinase,numbers ofis melanocytes usually associated [6,10,12,13]. with The pathological hyper-pigmenta disorderstion, such due as to agethe spots,overactivity ephelides, of tyrosinase, melasma, isand usually senile associated lentigines with [7,8 ].path Thus,ological regulating disorders the productivitysuch as age spots, of tyrosinase ephelides, is a melasma, metabolic andchallenge senile tolentigines balance the[7,8]. proper Thus, melanogenesis regulating the and productivity disorders from of hyperpigmentationtyrosinase is a metabolic [1,12–14 ]. challengeTyrosinase to balance is a highlythe proper conserved melanogene enzymesis showing and disorders high proximity from hyperpigmentation in molecular struc- [1,12–14].ture and catalytic properties
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