A Lead to Fight ESKAPEE Pathogenic Bacteria? Violette Hamers, Clément Huguet, Mélanie Bourjot, Aurelie Urbain
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Antibacterial Compounds from Mushrooms: A Lead to Fight ESKAPEE Pathogenic Bacteria? Violette Hamers, Clément Huguet, Mélanie Bourjot, Aurelie Urbain To cite this version: Violette Hamers, Clément Huguet, Mélanie Bourjot, Aurelie Urbain. Antibacterial Compounds from Mushrooms: A Lead to Fight ESKAPEE Pathogenic Bacteria?. Planta Medica, Georg Thieme Verlag, 2020, 10.1055/a-1266-6980. hal-03004189 HAL Id: hal-03004189 https://hal.archives-ouvertes.fr/hal-03004189 Submitted on 13 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Complimentary and personal copy for Violette Hamers, Clément Huguet, Mélanie Bourjot, Aurélie Urbain www.thieme.com Antibacterial Compounds from Mushrooms: A Lead to Fight ESKAPEE Pathogenic Bacteria? DOI 10.1055/a-1266-6980 Planta Med This electronic reprint is provided for non- commercial and personal use only: this reprint may be forwarded to individual colleagues or may be used on the authorʼs homepage. This reprint is not provided for distribution in repositories, including social and scientific networks and platforms. Publishing House and Copyright: © 2020 by Georg Thieme Verlag KG Rüdigerstraße 14 70469 Stuttgart ISSN 0032‑0943 Any further use only by permission of the Publishing House Reviews Antibacterial Compounds from Mushrooms: A Lead to Fight ESKAPEE Pathogenic Bacteria? Authors Violette Hamers, Clément Huguet, Mélanie Bourjot, Aurélie Urbain Affiliation ABSTRACT Faculté de pharmacie, Université de Strasbourg, Infectious diseases are among the greatest threats to global CNRS, IPHC UMR 7178, CAMBAP, Strasbourg, France health in the 21st century, and one critical concern is due to antibiotic resistance developed by an increasing number of Key words bacterial strains. New resistance mechanisms are emerging mushrooms, macromycetes, natural products, antibacterial, with many infections becoming more and more difficult if antibiotics, ESKAPEE not impossible to treat. This growing phenomenon not only is associated with increased mortality but also with longer received July 20, 2020 hospital stays and higher medical costs. For these reasons, accepted after revision September 18, 2020 there is an urgent need to find new antibiotics targeting published online pathogenic microorganisms such as ESKAPEE bacteria. Most Bibliography of currently approved antibiotics are derived from micro- Planta Med 2020 organisms, but higher fungi could constitute an alternative DOI 10.1055/a-1266-6980 and remarkable reservoir of anti-infectious compounds. For ISSN 0032‑0943 instance, pleuromutilins constitute the first class of antibiotics © 2020. Thieme. All rights reserved. derived from mushrooms. However, macromycetes still repre- Georg Thieme Verlag KG, Rüdigerstraße 14, sent a largely unexplored source. Publications reporting the 70469 Stuttgart, Germany antibacterial potential of mushroom extracts are emerging, but few purified compounds have been evaluated for their Correspondence bioactivity on pathogenic bacterial strains. Therefore, the Dr Aurélie Urbain aim of this review is to compile up-to-date data about natural ChimieAnalytiquedesMoléculesBioactiveset products isolated from fruiting body fungi, which significantly Pharmacognosie, IPHC UMR 7178, Université de Strasbourg inhibit the growth of ESKAPEE pathogenic bacteria. When 74 route du Rhin, CS 60024, 67401 Illkirch Cedex, France available, data regarding modes of action and cytotoxicity, Phone:+33368854180,Fax:+33368854325 mandatory when considering a possible drug development, [email protected] have been discussed in order to highlight the most promising compounds. Supplementary material is available under https://doi.org/10.1055/a-1266-6980 Electronic reprint for personal use Introduction compounds has been extended to marine microorganisms or en- dophytic fungi, which also need to activate a whole antimicrobial Nowadays, 97% of approved antibiotics have a microbial origin, chemical arsenal to impose themselves in their highly competitive from either soil fungi (e.g., penicillin) or bacteria (e.g., streptomy- environment [2,3]. In comparison to cultured bacteria and fungi, cin) [1]. These antibacterial agents have revolutionized the treat- there has been considerably less attention devoted to investigat- ment of infections such as tuberculosis, pneumonia, leprosy, and ing macroscopic fungi. Indeed, as they are also exposed to various gonorrhea. Unfortunately, the overuse and misuse of antibiotics biotic stresses, both at the underground (mycelium) and aerial has gradually led to acquired drug resistance in bacterial strains, (fruiting body) level, they synthesize a variety of antibacterial mol- an ever-increasing phenomenon. Almost a century after Flemingʼs ecules. In Western countries, mushrooms are considered above all discovery of penicillin, there is a sore need to identify new anti- for their culinary and nutritional value, like truffles or boletus bacterial drugs capable of fighting infections caused by multi- mushrooms that deliver a sought-after flavor, or white mush- drug-resistant (MDR) bacteria. rooms, low in calories but providing a good source of dietary fi- Alternative sources could represent an interesting reservoir of bers, proteins, vitamins, and minerals. In Asia, where traditional such molecules. Over the past decade, search for antibacterial Chinese medicine prevails, many mushrooms are not only popular Hamers V et al. Antibacterial Compounds from … Planta Med | © 2020. Thieme. All rights reserved. Reviews ingredients in cuisine, but they are also reputed for their health mannii, P. aeruginosa,andEnterobacter species, bacteria whose ini- benefits, like shiitake or Ganoderma lucidum, with numerous stud- tials have given the acronym ESKAPE. This designation also high- ies reporting their immunomodulatory properties and anticancer lights the ability of these pathogens to escape from many antibi- potential [4, 5]. Yet, the interest in macromycetes as an alternative otics, leading to severe diseases, such as bloodstream infections source of antibacterial agents seems to emerge somewhat [6, 7], and pneumonia, associated with a high degree of mortality [17]. and a new class of mushroom-derived antibiotics, pleuromutilins, Although E. coli is not included in the ESKAPE group, this Gram- has been released recently [8]. negative Enterobacteriaceae can produce enzymes involved in Although numerous recent publications report the antibacteri- antibiotic resistance, such as carbapenemase and extended-spec- al activity of mushroom extracts, studies dealing with purified and trum beta-lactamases (ESBL). These resistance mechanisms make identified compounds are still scarce. Therefore, this review aims it a critical priority pathogen regarding the WHO list. On these ar- at establishing a state of the art on mushroom molecules that af- guments, we have decided to include in this review mushrooms fect bacteria development. Some publications report antibacterial metabolites that inhibit E. coli growth, leading to a review focus- activity against nonpathogenic bacteria, such as the Gram-posi- ing on the extended ESKAPEE pathogenic bacteria. tive model Bacillus subtilis. We have considered that it would be Even if these microorganisms are often associated with MDR, much more valuable to pay attention to molecules inhibiting the we will see that many studies presented in this review have not growth of pathogenic bacteria only. For this reason, we have de- necessarily been performed on resistant strains. For instance, all cided to focus this review on fungal compounds exhibiting an compounds reported to be active against K. pneumoniae, P. aerugi- antibacterial activity toward bacteria that represent a major nosa,andEnterobacter species have been evaluated on various threat in this context of antibiotic resistance, namely ESKAPEE strains not showing any special resistance to usual medication. bacteria: Enterococcus faecium (▶ Table 1), Staphylococcus aureus On the contrary, all compounds inhibiting E. faecium growth have (▶ Table 2), Klebsiella pneumoniae (▶ Table 3), Acinetobacter bau- been tested on vancomycin-resistant strains. For S. aureus and mannii (▶ Table 4), Pseudomonas aeruginosa (▶ Table 5), Entero- E. coli, some molecules were active against ESBL-producing or me- bacter species (▶ Table 6), and Escherichia coli (▶ Table 7)[9]. thicillin-resistant strains; few metabolites were even active against The applied search strategy consisted in the systematic litera- a multiresistant A. baumannii strain. Some antibacterial assess- ture reporting mushroom antibacterial compounds active against ments have also been carried out in the presence of phenylala- ESKAPEE bacteria, without any time limitation. Electronic data- nine-arginine β-naphthylamide (PAβN), an efflux inhibitor that bases including SciFinder, Web of Science, Science Direct, permeabilizes the outer membrane of Gram-negative bacteria PubMed, and Google Scholar were screened using the following such as K. pneumoniae, A. baumannii, P. aeruginosa,andEntero- keywords: “antibacterial, antimicrobial,