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Antimicrobial and Wound Healing Potential of a New Chemotype from Piper Cubeba L

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Antimicrobial and Wound Healing Potential of a New Chemotype from Piper Cubeba L plants Article Antimicrobial and Wound Healing Potential of a New Chemotype from Piper cubeba L. Essential Oil and In Silico Study on S. aureus tyrosyl-tRNA Synthetase Protein Fahad Alminderej 1, Sana Bakari 2, Tariq I. Almundarij 3, Mejdi Snoussi 4,5 , Kaïss Aouadi 1,6 and Adel Kadri 2,7,* 1 Department of Chemistry, College of Science, Qassim University, Buraidah 51452, Saudi Arabia; [email protected] (F.A.); [email protected] (K.A.) 2 Department of Chemistry, Faculty of Science of Sfax, University of Sfax, B.P. 1171, Sfax 3000, Tunisia; [email protected] 3 Department of Veterinary Medicine, College of Agriculture and Veterinary Medicine, Qassim University, PO Box 6622, Buraidah 51452, Saudi Arabia; [email protected] 4 Department of Biology, College of Science, Hail University, P.O. Box 2440, Ha’il 2440, Saudi Arabia; [email protected] 5 Laboratory of Genetics, Biodiversity and Valorization of Bio-Resources (LR11ES41), University of Monastir, Higher Institute of Biotechnology of Monastir, Avenue Tahar Haddad, BP74, Monastir 5000, Tunisia 6 Faculty of Sciences of Monastir, University of Monastir, Avenue of the Environment, Monastir 5019, Tunisia 7 Faculty of Science and Arts in Baljurashi, Albaha University, P.O. Box (1988), Albaha 65527, Saudi Arabia * Correspondence: [email protected]; Fax: +216-74-27-44-37 Abstract: Piper cubeba is an important plant commonly known as cubeb or Java pepper, and it is cultivated for its fruit and essential oils, largely used to treat various diseases. Up to today, there was no scientific report on wound healing activity. Thus, this study was initiated to evaluate for the first time the antimicrobial activity and wound healing potential of a new chemotype from Piper cubeba Citation: Alminderej, F.; Bakari, S.; essential oil (PCEO) from fruits. Thirteen microbial strains have been selected to investigate the Almundarij, T.I.; Snoussi, M.; Aouadi, antimicrobial potential of PCEO. For the evaluation of the wound healing potential, sixteen rats were K.; Kadri, A. Antimicrobial and excised on the dorsal back and divided into four groups. The effect of PCEO on the malondialde- Wound Healing Potential of a New hyde (MDA) and superoxide dismutase (SOD) activities in the healed wound area of rats and the Chemotype from Piper cubeba L. biochemical parameters and skin histological analysis were also assessed. Results: Data showed Essential Oil and In Silico Study on that PCEO exhibited a powerful antimicrobial potential especially against Listeria monocytogenes and S. aureus tyrosyl-tRNA Synthetase Staphylococcus aureus. In addition, the topical application of PCEO cream appears to increase the SOD Protein. Plants 2021, 10, 205. https:// doi.org/10.3390/plants10020205 level, wound healing and contraction but reduced the MDA amount suggesting an impressive and a rapid cutaneous healing power. Additionally, histopathological analysis of the granulation tissue Received: 29 November 2020 revealed that the derma is properly restored and arranged after treatment with PCEO. The docking Accepted: 15 January 2021 analysis of PCEO constituents against S. aureus tyrosyl-tRNA synthetase enzyme showed binding Published: 22 January 2021 energies values in the range of −7.2 to −4.8 kcal/mol. In conclusion, the topic use of PCEO healing cream showed significant effect in accelerating the healing process, which may be attributed to the Publisher’s Note: MDPI stays neutral synergetic effect of antioxidant and antimicrobial properties of PCEO volatile constituents, making it with regard to jurisdictional claims in a relevant therapeutic agent for the management of wounds and therefore confirming the popular published maps and institutional affil- traditional uses of this plant. iations. Keywords: Piper cubeba L.; dry berries; volatile oil; antimicrobial; healing effect; biochemical parame- ters; molecular docking Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article 1. Introduction distributed under the terms and The oxidative stress (as the results of elevated intracellular levels of reactive oxygen conditions of the Creative Commons species (ROS)) along with redox signaling play a substantial role in regulating normal Attribution (CC BY) license (https:// wound healing under pathological conditions [1]. ROS are centrally involved and having creativecommons.org/licenses/by/ 4.0/). a significant role in the orchestration of the normal wound-healing response acting as Plants 2021, 10, 205. https://doi.org/10.3390/plants10020205 https://www.mdpi.com/journal/plants Plants 2021, 10, 205 2 of 20 cellular messengers to many immunocytes and non-lymphoid cells [1,2]. They also directly damage microbes that invade tissues and are known to play a pivotal role in regulating healing at low concentrations [2]. The normal healing response begins when the tissue is injured. Afterwards, an inflammatory response manifests itself and the collagen level starts to increase via cells below the dermis. During the wound-healing response, a number of cells used these radicals, including platelets, macrophages, fibroblasts, endothelial cells and keratinocytes [3]. Wound healing is a complex biological process, which consists of a well-ordered progression of events allowing restoring the integrity of damaged tissue and homeostasis after injury via the inflammatory phase, proliferation stages and tissue remodeling. Thereby, redox signaling and increased oxidative stress are responsible for impaired wound repair. The hydrogen peroxide (H2O2) produced by dismutation of superoxide acts as intracellular messengers with low concentrations (100–250 µM) by stim- ulating key phases of wound healing including cell recruitment, production of cytokines and angiogenesis, however excessive and uncontrolled amount of ROS generation have deleterious effects by accelerating the non-healing wounds [4–8]. The antioxidants have been applied to remove the deleterious detrimental effects of ROS, by donating their own electrons, and therefore preventing them from capturing electrons from other important molecules, such as DNA, proteins and lipids [1]. Thus, various medicinal herbs and plants have been reported to offer promising biosources of bioactive molecules with various bio- logical properties such as antioxidant [9–14], antimicrobial [10,12–15], antibiofilm [16,17], antiquorum sensing [11,17,18] and antidiabetic [19]. On the other hand, several treatments are available for the wound management such as analgesics, antibiotics and nonsteroidal anti-inflammatory drugs, but most of them produce numerous unwanted side effects [8,20]. Due to the emergence and spread resistance of microorganisms colonizing infections to an- tibiotics and synthetic drugs currently used in conventional wound healing cure, growing attention has been afforded to the search for natural wound healing agents. Plant-based bioactive compounds have therefore been a potential source of antioxidants and healing agents, which have received a great deal of attention due to the increased of oxidative stress [21]. Their role is to induce rapid re-epithelialization of wounds with minimal scarring associated with potent antimicrobial effects [22]. Consequently, there is a need to use essential oil containing many bioactive compounds to discover new treatment op- tions able to stimulate healing with antimicrobial potential to overcome the antimicrobial resistance and side effects. Throughout the world, the estimated global pharmaceutical market in 2022 is $1.12 trillion, indicating the growing demand for pharmaceuticals by a huge percentage of population. The Saudi market offers many wound care treatments, including Piper cubeba, which has been used as a remedy by the local population for various medical purposes [23,24]. Therefore, in light of the above facts and in the continuation of our investigations into Piper cubeba essential oil (PCEO) with therapeutic properties and limited data on this spice, we have now studied for the first time the effects of its essential oil on wound healing and also its antimicrobial activities against a wide range of strains supported by in silico study. Accordingly, the present study was designed to evaluate the antimicrobial activity of PCEO (new chemotype) from dry berries against thirteen pathogenic strains and to demonstrate for the first time their wound healing effects using an in vivo rat wound model based on a series of clinical, biochemical and histopathological assays. Furthermore, molecular docking studies were performed to investigate the potential binding mode of the selected PCEO phytocompounds against S. aureus TyrRS known as an attractive target enzyme for finding new antibacterial agents. 2. Results 2.1. Phytochemical Descriptions Continuous to our previous work on the effectiveness of PCEO, GC–MS analyses have been already carried out recently by our team and here we are only able to present the structure of the identified compounds, which will be used for biological activities and Plants 2021, 10, 205 3 of 20 Plants 2020, 9, x FOR PEER REVIEW 3 of 21 thethe molecular molecular docking docking study study [24]. [24]. The The chemical chemical structures structures of of the the twenty-four twenty-four compounds compounds identifiedidentified in in the the essential essential oil oil tested tested using using the the GC–MS GC–MS technique technique are are listed in Figure 1 1.. FigureFigure 1. ChemicalChemical structure structure of of the the 24 24 compounds compounds identified identified in in the
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