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Ethnobotany and the Role of Plant Natural Products in Antibiotic Drug Discovery ¶ ¶ ¶ Gina Porras, Francoiş Chassagne, James T

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Ethnobotany and the Role of Plant Natural Products in Antibiotic Drug Discovery ¶ ¶ ¶ Gina Porras, Francoiş Chassagne, James T pubs.acs.org/CR Review Ethnobotany and the Role of Plant Natural Products in Antibiotic Drug Discovery ¶ ¶ ¶ Gina Porras, Francoiş Chassagne, James T. Lyles, Lewis Marquez, Micah Dettweiler, Akram M. Salam, Tharanga Samarakoon, Sarah Shabih, Darya Raschid Farrokhi, and Cassandra L. Quave* Cite This: https://dx.doi.org/10.1021/acs.chemrev.0c00922 Read Online ACCESS Metrics & More Article Recommendations *sı Supporting Information ABSTRACT: The crisis of antibiotic resistance necessitates creative and innovative approaches, from chemical identification and analysis to the assessment of bioactivity. Plant natural products (NPs) represent a promising source of antibacterial lead compounds that could help fill the drug discovery pipeline in response to the growing antibiotic resistance crisis. The major strength of plant NPs lies in their rich and unique chemodiversity, their worldwide distribution and ease of access, their various antibacterial modes of action, and the proven clinical effectiveness of plant extracts from which they are isolated. While many studies have tried to summarize NPs with antibacterial activities, a comprehensive review with rigorous selection criteria has never been performed. In this work, the literature from 2012 to 2019 was systematically reviewed to highlight plant-derived compounds with antibacterial activity by focusing on their growth inhibitory activity. A total of 459 compounds are included in this Review, of which 50.8% are phenolic derivatives, 26.6% are terpenoids, 5.7% are alkaloids, and 17% are classified as other metabolites. A selection of 183 compounds is further discussed regarding their antibacterial activity, biosynthesis, structure−activity relationship, mechanism of action, and potential as antibiotics. Emerging trends in the field of antibacterial drug discovery from plants are also discussed. This Review brings to the forefront key findings on the antibacterial potential of plant NPs for consideration in future antibiotic discovery and development efforts. CONTENTS 2.4.5. Nor-triterpenoids AI 2.4.6. Triterpenoids and Saponins AI 1. Introduction B 2.5. Other Metabolites AJ 1.1. Scope and Terminology B 2.5.1. Aliphatic Compounds AJ 2. Plant-Derived Compounds with Antibacterial 2.5.2. Ceramides AK Properties U 2.5.3. Cyclic Compounds AK 2.1. Overview U 2.5.4. Glycosides AK Downloaded via EMORY UNIV on November 9, 2020 at 17:20:48 (UTC). 2.1.1. Major Chemical Classes Investigated U 2.5.5. Fatty Acids AK 2.2. Alkaloids V 2.5.6. Organosulfurs and Derivatives AK 2.2.1. Overview V 2.5.7. Peptides AL 2.2.2. Quinolines V See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. 2.5.8. Steroids AL 2.2.3. Isoquinolines, Aporphines, and Phenan- 2.6. Summary of Antibacterial Compounds AL threnes W 3. Emerging Trends AP 2.2.4. Other Alkaloid Derivatives X 3.1. Chemical Innovations AQ 2.3. Phenolic Derivatives X 3.1.1. Machine Learning AQ 2.3.1. Overview X 3.1.2. Molecular Networking and Dereplica- 2.3.2. Chalcones X tion AQ 2.3.3. Coumarins Y 3.1.3. Metabolite Generation AR 2.3.4. Flavonoids Y 3.1.4. Endophytic Fungi AS 2.3.5. Lignans AB 3.1.5. Structure Elucidation AS 2.3.6. Quinones and Related Compounds AB 2.3.7. Xanthones AC 2.3.8. Other Phenolic Compounds AC Special Issue: Drug Resistance 2.4. Terpenoids AF Received: August 27, 2020 2.4.1. Overview AF 2.4.2. Monoterpenoids AF 2.4.3. Sesquiterpenoids and Derivatives AG 2.4.4. Diterpenoids AH © XXXX American Chemical Society https://dx.doi.org/10.1021/acs.chemrev.0c00922 A Chem. Rev. XXXX, XXX, XXX−XXX Chemical Reviews pubs.acs.org/CR Review 3.2. Pharmacological Innovations AT tion, compound isolation, dereplication, and plant sample 3.2.1. Drug Delivery Systems AT acquisition.5,7,11,12 3.2.2. Synergy AT Plants are particularly interesting as sources for antibiotic 3.2.3. Alternative Microbial Targets AT leads because they have developed complex defense mecha- 4. Conclusions and Future Perspectives AT nisms against microbes, such as the use of chemical defenses Associated Content AV involving a wide range of structurally unique secondary Supporting Information AV metabolites.13 Plants also possess other distinctive features Author Information AV promising for drug discovery, including their rich chemo- Corresponding Author AV diversity across the approximately 374 000 species of plants Authors AV worldwide,14 the proven clinical effectiveness of plant extracts Author Contributions AV in long-standing traditional medicinal practices across the Notes AV world,15 their ease of access, and the potential for synergistic Biographies AV interactions between phytochemicals and other bioactive Acknowledgments AW compounds.16 List of Abbreviations AW Ethnobotany is the scientific study of the interactions References AX between humankind and the plant kingdom; it has also been defined as the science of survival.17 The field encompasses studies on how humans use plants for food, medicine, art, 1. INTRODUCTION construction, music, ritual, and more. The history of medicine The ability to successfully treat infectious diseases is is rich in records of plants used to treat myriad ailments, threatened due to the rise of antimicrobial resistance including infectious diseases. Today, between 70 and 95% of (AMR). According to the Centers for Disease Control and people in the developing world continue to rely on plants for Prevention (CDC), about 2.9 million antibiotic-resistant their primary pharmacopeia.18 According to the Medicinal infections occur in the United States each year, resulting in Plant Names Services (MPNS), 28 187 species are used in 35 900 deaths.1 The CDC lists 16 bacteria and two fungi as medicine, representing nearly 7.5% of all plant life on Earth.19 urgent, serious, or concerning threats, including Mycobacterium Through focusing on those species already in use in traditional tuberculosis, of which there are extensively drug-resistant therapies for the treatment of infectious disease, a more strains, resistant to two of four first-line antibiotics and at targeted approach to identifying plant NPs with antibacterial least one of the three second-line antibiotics.2 properties can be achieved; this is known as the ethnobotanical Several factors are involved in the rise of antibiotic approach to drug discovery. resistance, especially the overuse and misuse of antibiotics in Plant NPs can act as antibacterials through various modes of human and animal health and the lack of development of new action. All antibiotics currently in the clinic work by inhibiting antibiotics. The field of antibiotic discovery and development bacterial growth, either in a bactericidal or bacteriostatic is in dire need of innovation to reinvigorate the pipeline that fashion, and this is achieved by drug-mediated perturbation of has not seen a new class of drugs discovered and approved by an essential cellular process. One of the main drawbacks of the FDA since the late 1980s.3 This status quo can be in large growth inhibition is the inevitable selection for resistance due part explained by the economics of antibiotics postapproval, to the rapid evolution of the bacterial genome under selective which has become so unfavorable to companies and investors pressure on essential cellular processes.20 Given the threat of that antibiotic start-ups and large pharmaceutical companies antibiotic resistance, a growing body of research is focused on alike are unable to survive in the antibiotics development the development of drugs that target bacterial virulence, a space.4 nonessential cellular process. Antivirulence drug candidates In the search for novel antibiotics, the screening of synthetic target systems such as biofilm formation and quorum sensing, combinatorial compound libraries has failed to meet expect- potentially exerting less selective pressure for resistance and ations and has consequently demonstrated the importance of less detrimental effects on commensal microbes.21 The exploring the biologically relevant chemical space.5,6 Com- potential of plant compounds to exert such antivirulence pounds that occupy this space in chemistry are already able, activities is covered in an exhaustive review by Silva et al.22 unlike the majority of synthetic compounds, to interact with Also, of note, the engineering of natural products by synthetic 7 biological machinery and potentially act as drugs. Natural chemistry was explored in depth by Rossiter et al.23 products (NPs) have a strong tendency to occupy this space, in 1.1. Scope and Terminology part due to their core purpose of interacting with biological systems and their vast range of chemical and structural We discuss the growth inhibitory activity of plants and define diversity that reaches complexities above what many synthetic antimicrobials here as an agent that kills or limits the growth of compound libraries possess.5 microorganisms (bacteria, fungi, parasites, viruses). We Historically, the discovery of penicillin by Alexander Fleming specifically use the terms “antibacterial” or “antibiotics” when in the 1920s was made from a culture of the fungus Penicillium describing agents that kill or inhibit the growth of bacteria. We notatum.8 To date, of the 162 antibacterial agents approved by focused on plant-derived compounds with an emphasis on the the U.S. Food and Drug Administration from 1981 to 2019, minimum inhibitory concentration (MIC) value, which is about 50% are from or derived from NPs.9 Almost all of these commonly used as an indicator of antibacterial potency. The have a microbial source rather than a plant source in part due MIC is defined as the lowest concentration of an antimicrobial to former limited accessibility of plant natural products for agent that inhibits the visible growth of a microorganism in drug discovery.10 The more recent improvement in accessi- vitro.24 To provide a comprehensive analysis on the topic, we bility of plant NPs is due to enhanced compatibility with high performed a thorough literature review by using electronic throughput screening (HTS) and advances in lead optimiza- databases (Web of Science, PubMed, SciFinder) and specific B https://dx.doi.org/10.1021/acs.chemrev.0c00922 Chem.
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