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Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii

The limited diversity in targets of available antibiotic therapies has put tremendous pressure on the treatment of bacterial pathogens, where numerous resistance mechanisms that counteract their function are becoming increasingly prevalent. Here, we utilize an unconventional anti-virulence screen of...

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Autores principales: Jonkergouw, Christopher, Beyeh, Ngong Kodiah, Osmekhina, Ekaterina, Leskinen, Katarzyna, Taimoory, S. Maryamdokht, Fedorov, Dmitrii, Anaya-Plaza, Eduardo, Kostiainen, Mauri A., Trant, John F., Ras, Robin H. A., Saavalainen, Päivi, Linder, Markus B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104825/
https://www.ncbi.nlm.nih.gov/pubmed/37059703
http://dx.doi.org/10.1038/s41467-023-37749-6
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author Jonkergouw, Christopher
Beyeh, Ngong Kodiah
Osmekhina, Ekaterina
Leskinen, Katarzyna
Taimoory, S. Maryamdokht
Fedorov, Dmitrii
Anaya-Plaza, Eduardo
Kostiainen, Mauri A.
Trant, John F.
Ras, Robin H. A.
Saavalainen, Päivi
Linder, Markus B.
author_facet Jonkergouw, Christopher
Beyeh, Ngong Kodiah
Osmekhina, Ekaterina
Leskinen, Katarzyna
Taimoory, S. Maryamdokht
Fedorov, Dmitrii
Anaya-Plaza, Eduardo
Kostiainen, Mauri A.
Trant, John F.
Ras, Robin H. A.
Saavalainen, Päivi
Linder, Markus B.
author_sort Jonkergouw, Christopher
collection PubMed
description The limited diversity in targets of available antibiotic therapies has put tremendous pressure on the treatment of bacterial pathogens, where numerous resistance mechanisms that counteract their function are becoming increasingly prevalent. Here, we utilize an unconventional anti-virulence screen of host-guest interacting macrocycles, and identify a water-soluble synthetic macrocycle, Pillar[5]arene, that is non-bactericidal/bacteriostatic and has a mechanism of action that involves binding to both homoserine lactones and lipopolysaccharides, key virulence factors in Gram-negative pathogens. Pillar[5]arene is active against Top Priority carbapenem- and third/fourth-generation cephalosporin-resistant Pseudomonas aeruginosa and Acinetobacter baumannii, suppressing toxins and biofilms and increasing the penetration and efficacy of standard-of-care antibiotics in combined administrations. The binding of homoserine lactones and lipopolysaccharides also sequesters their direct effects as toxins on eukaryotic membranes, neutralizing key tools that promote bacterial colonization and impede immune defenses, both in vitro and in vivo. Pillar[5]arene evades both existing antibiotic resistance mechanisms, as well as the build-up of rapid tolerance/resistance. The versatility of macrocyclic host-guest chemistry provides ample strategies for tailored targeting of virulence in a wide range of Gram-negative infectious diseases.
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spelling pubmed-101048252023-04-16 Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii Jonkergouw, Christopher Beyeh, Ngong Kodiah Osmekhina, Ekaterina Leskinen, Katarzyna Taimoory, S. Maryamdokht Fedorov, Dmitrii Anaya-Plaza, Eduardo Kostiainen, Mauri A. Trant, John F. Ras, Robin H. A. Saavalainen, Päivi Linder, Markus B. Nat Commun Article The limited diversity in targets of available antibiotic therapies has put tremendous pressure on the treatment of bacterial pathogens, where numerous resistance mechanisms that counteract their function are becoming increasingly prevalent. Here, we utilize an unconventional anti-virulence screen of host-guest interacting macrocycles, and identify a water-soluble synthetic macrocycle, Pillar[5]arene, that is non-bactericidal/bacteriostatic and has a mechanism of action that involves binding to both homoserine lactones and lipopolysaccharides, key virulence factors in Gram-negative pathogens. Pillar[5]arene is active against Top Priority carbapenem- and third/fourth-generation cephalosporin-resistant Pseudomonas aeruginosa and Acinetobacter baumannii, suppressing toxins and biofilms and increasing the penetration and efficacy of standard-of-care antibiotics in combined administrations. The binding of homoserine lactones and lipopolysaccharides also sequesters their direct effects as toxins on eukaryotic membranes, neutralizing key tools that promote bacterial colonization and impede immune defenses, both in vitro and in vivo. Pillar[5]arene evades both existing antibiotic resistance mechanisms, as well as the build-up of rapid tolerance/resistance. The versatility of macrocyclic host-guest chemistry provides ample strategies for tailored targeting of virulence in a wide range of Gram-negative infectious diseases. Nature Publishing Group UK 2023-04-14 /pmc/articles/PMC10104825/ /pubmed/37059703 http://dx.doi.org/10.1038/s41467-023-37749-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Jonkergouw, Christopher
Beyeh, Ngong Kodiah
Osmekhina, Ekaterina
Leskinen, Katarzyna
Taimoory, S. Maryamdokht
Fedorov, Dmitrii
Anaya-Plaza, Eduardo
Kostiainen, Mauri A.
Trant, John F.
Ras, Robin H. A.
Saavalainen, Päivi
Linder, Markus B.
Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title_full Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title_fullStr Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title_full_unstemmed Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title_short Repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant Pseudomonas aeruginosa and Acinetobacter baumannii
title_sort repurposing host-guest chemistry to sequester virulence and eradicate biofilms in multidrug resistant pseudomonas aeruginosa and acinetobacter baumannii
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104825/
https://www.ncbi.nlm.nih.gov/pubmed/37059703
http://dx.doi.org/10.1038/s41467-023-37749-6
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