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Bioactive Alkaloids from Genus Aspergillus: Mechanistic Interpretation of Their Antimicrobial and Potential SARS-Cov-2 Inhibitory Activity Using Molecular Modelling

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Bioactive Alkaloids from Genus Aspergillus: Mechanistic Interpretation of Their Antimicrobial and Potential SARS-Cov-2 Inhibitory Activity Using Molecular Modelling International Journal of Molecular Sciences Review Bioactive Alkaloids from Genus Aspergillus: Mechanistic Interpretation of Their Antimicrobial and Potential SARS-CoV-2 Inhibitory Activity Using Molecular Modelling Fadia S. Youssef 1 , Elham Alshammari 2 and Mohamed L. Ashour 1,3,* 1 Department of Pharmacognosy, Faculty of Pharmacy, Ain Shams University, Cairo 11566, Egypt; [email protected] 2 Department of Pharmacy Practice, College of Pharmacy, Princess Nourah bint Abdulrahman University, Riyadh 84428, Saudi Arabia; [email protected] 3 Department of Pharmaceutical Sciences, Pharmacy Program, Batterjee Medical College, Jeddah 21442, Saudi Arabia * Correspondence: [email protected]; Tel.: +20-10-68-222-354 Abstract: Genus Aspergillus represents a widely spread genus of fungi that is highly popular for possessing potent medicinal potential comprising mainly antimicrobial, cytotoxic and antioxidant properties. They are highly attributed to its richness by alkaloids, terpenes, steroids and polyke- tons. This review aimed to comprehensively explore the diverse alkaloids isolated and identified from different species of genus Aspergillus that were found to be associated with different marine organisms regarding their chemistry and biology. Around 174 alkaloid metabolites were reported, 66 of which showed important biological activities with respect to the tested biological activities Citation: Youssef, F.S.; Alshammari, mainly comprising antiviral, antibacterial, antifungal, cytotoxic, antioxidant and antifouling activities. E.; Ashour, M.L. Bioactive Alkaloids Besides, in silico studies on different microbial proteins comprising DNA-gyrase, topoisomerase IV, from Genus Aspergillus: Mechanistic Interpretation of Their Antimicrobial dihydrofolate reductase, transcriptional regulator TcaR (protein), and aminoglycoside nucleotidyl and Potential SARS-CoV-2 Inhibitory transferase were done for sixteen alkaloids that showed anti-infective potential for better mecha- Activity Using Molecular Modelling. nistic interpretation of their probable mode of action. The inhibitory potential of compounds vs. Int. J. Mol. Sci. 2021, 22, 1866. Angiotensin-Converting Enzyme 2 (ACE2) as an important therapeutic target combating COVID-19 https://doi.org/10.3390/ijms22041866 infection and its complication was also examined using molecular docking. Fumigatoside E showed the best fitting within the active sites of all the examined proteins. Thus, Aspergillus species isolated Academic Editors: from marine organisms could afford bioactive entities combating infectious diseases. Marie-Laure Fauconnier and Laurence Lins Keywords: alkaloids; antimicrobial activity; Aspergillus; molecular modelling Received: 13 January 2021 Accepted: 10 February 2021 Published: 13 February 2021 1. Introduction Publisher’s Note: MDPI stays neutral Recently, marine-derived fungi have gained significant attention as promising thera- with regard to jurisdictional claims in peutic approaches for the treatment of a wide array of human ailments and as successful published maps and institutional affil- tools for drug discovery [1]. This is mainly attributed to their richness by a diverse array of iations. secondary metabolites comprising terpenoids, alkaloids, peptides, lactones and steroids. These promising activities are represented by antiviral, antibacterial, anti-inflammatory and anticancer activity [2]. The significant diversity in physical and chemical structure of the environment where the marine-derived fungi grow has greatly reflected by the vast structural and functional variation in their produced secondary metabolites and their Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. biological activities [3]. Meanwhile, marine-derived fungal metabolites displayed a promis- This article is an open access article ing physico-chemical behavior and oral-bioavailability, constituting a safer therapeutic distributed under the terms and alternative when compared to synthetic molecules that are considerably important in the conditions of the Creative Commons process of pharmaceutical dosage form formulation [4,5]. Moreover, many alkaloids were Attribution (CC BY) license (https:// previously isolated from marine fungi and showed a vast array of biological activities [6–9]. creativecommons.org/licenses/by/ Genus Aspegillus represents a widely spread genus of fungi that are highly popular of 4.0/). possessing a potent medicinal potential comprising mainly antimicrobial, cytotoxic and Int. J. Mol. Sci. 2021, 22, 1866. https://doi.org/10.3390/ijms22041866 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 1866 2 of 22 Moreover, many alkaloids were previously isolated from marine fungi and showed a vast array of biological activities [6–9]. Int. J. Mol. Sci. 2021, 22, 1866 Genus Aspegillus represents a widely spread genus of fungi that are highly popular2 of 23 of possessing a potent medicinal potential comprising mainly antimicrobial, cytotoxic and antioxidant activities that are highly attributed to its richness by alkaloids, terpenes, steroid and polyketons. These secondary metabolites reflect the considerable importance antioxidantof genus Aspergillus activities both that arein the highly scientific attributed and pharmaceutical to its richness by industries alkaloids, levels terpenes, [10]. steroid and polyketons.Thus, this review These secondaryaimed to comprehensivel metabolites reflecty explore the considerable the diverse importance alkaloids ofisolated genus Aspergillusand identifiedboth from in the different scientific species and pharmaceutical of genus Aspergillus industries that were levels found [10]. to be associated with Thus,different this reviewmarine aimedorganisms to comprehensively regarding their explore chemistry the diverse and biology. alkaloids Classification isolated and identifiedwas done fromon the different basis of species alphabetical of genus arrangAspergillusement thatof species. were found Around to be 174 associated alkaloid with me- differenttabolites marinewere reported, organisms 66 regardingof which showed their chemistry important and biological biology. Classification activities mainly was donecom- onprising the basis antiviral, of alphabetical antibacterial, arrangement antifungal, of species.cytotoxic, Around antioxidant 174 alkaloid and antifouling metabolites activi- were reported,ties. In addition, 66 of which data showedillustrating important the bioactive biological alkaloids activities obtained mainly from comprising previously antiviral, men- antibacterial, antifungal, cytotoxic, antioxidant and antifouling activities. In addition, data tioned fungal strains, their sources and biological properties are compiled in Table 1 for illustrating the bioactive alkaloids obtained from previously mentioned fungal strains, better representation of the collected data. A pie chart illustrating the different biological their sources and biological properties are compiled in Table1 for better representation of activities for the bioactive alkaloids of genus Aspergillus was also provided. Besides, in the collected data. A pie chart illustrating the different biological activities for the bioactive silico studies on different microbial proteins were done for sixteen alkaloids that showed alkaloids of genus Aspergillus was also provided. Besides, in silico studies on different anti-infective potential for better mechanistic interpretation of their probable mode of microbial proteins were done for sixteen alkaloids that showed anti-infective potential action. In addition, the inhibitory potential of these compounds vs. Angioten- for better mechanistic interpretation of their probable mode of action. In addition, the sin-Converting Enzyme 2 (ACE2) as an important therapeutic target combating inhibitory potential of these compounds vs. Angiotensin-Converting Enzyme 2 (ACE2) as COVID-19 infection and its complication was also examined using molecular docking to an important therapeutic target combating COVID-19 infection and its complication was it can act as a guide for researchers who wish to continue exploring the anti-infectious also examined using molecular docking to it can act as a guide for researchers who wish to potential of alkaloid derived from genus Aspergillus. continue exploring the anti-infectious potential of alkaloid derived from genus Aspergillus. 2. Diverse Alkaloids Isolated and IdentifiedIdentified fromfrom DifferentDifferent SpeciesSpecies ofof GenusGenus Asper- Aspergillusgillus and Theirand TheirBiology Biology in Alphabetical in Alphabetical Arrangement Arrangement of Species of Species 2.1. A. carneus Aspergillus speciesspecies are are highly highly popular popular due due to to the the presence presence of aof wide a wide variety variety of alkaloids of alka- belongingloids belonging to diverse to diverse classes. classes. Prenylated Prenylated indole andindole quinazolinone and quinazolinone alkaloids alkaloids were isolated were fromisolatedA. carneusfrom A., acarneus marine, a associated marine associatedAspergillus Aspergillusspecies, while species, the formerwhile the is represented former is rep- by carneamidesresented by A-Ccarneamides (1–3); however, A-C the(1– latter3); however, is represented the bylatter carnequinazolines is represented A-C by (4car-–6). Unfortunately,nequinazolines noneA-C ( of4– the6). Unfortunately, isolated compounds none of revealed the isolated any antimicrobialcompounds revealed or cytotoxic any activitiesantimicrobial (Figure or 1cytotoxic)[11].
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