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The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence

Antimicrobial peptides (AMPs) offer a promising solution to the antibiotic resistance crisis. However, an unresolved serious concern is that the evolution of resistance to therapeutic AMPs may generate cross-resistance to host AMPs, compromising a cornerstone of the innate immune response. We system...

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Autores principales: Jangir, Pramod K, Ogunlana, Lois, Szili, Petra, Czikkely, Marton, Shaw, Liam P, Stevens, Emily J, Yu, Yang, Yang, Qiue, Wang, Yang, Pál, Csaba, Walsh, Timothy R, MacLean, Craig R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10129329/
https://www.ncbi.nlm.nih.gov/pubmed/37094804
http://dx.doi.org/10.7554/eLife.84395
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author Jangir, Pramod K
Ogunlana, Lois
Szili, Petra
Czikkely, Marton
Shaw, Liam P
Stevens, Emily J
Yu, Yang
Yang, Qiue
Wang, Yang
Pál, Csaba
Walsh, Timothy R
MacLean, Craig R
author_facet Jangir, Pramod K
Ogunlana, Lois
Szili, Petra
Czikkely, Marton
Shaw, Liam P
Stevens, Emily J
Yu, Yang
Yang, Qiue
Wang, Yang
Pál, Csaba
Walsh, Timothy R
MacLean, Craig R
author_sort Jangir, Pramod K
collection PubMed
description Antimicrobial peptides (AMPs) offer a promising solution to the antibiotic resistance crisis. However, an unresolved serious concern is that the evolution of resistance to therapeutic AMPs may generate cross-resistance to host AMPs, compromising a cornerstone of the innate immune response. We systematically tested this hypothesis using globally disseminated mobile colistin resistance (MCR) that has been selected by the use of colistin in agriculture and medicine. Here, we show that MCR provides a selective advantage to Escherichia coli in the presence of key AMPs from humans and agricultural animals by increasing AMP resistance. Moreover, MCR promotes bacterial growth in human serum and increases virulence in a Galleria mellonella infection model. Our study shows how the anthropogenic use of AMPs can drive the accidental evolution of resistance to the innate immune system of humans and animals. These findings have major implications for the design and use of therapeutic AMPs and suggest that MCR may be difficult to eradicate, even if colistin use is withdrawn.
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spelling pubmed-101293292023-04-26 The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence Jangir, Pramod K Ogunlana, Lois Szili, Petra Czikkely, Marton Shaw, Liam P Stevens, Emily J Yu, Yang Yang, Qiue Wang, Yang Pál, Csaba Walsh, Timothy R MacLean, Craig R eLife Evolutionary Biology Antimicrobial peptides (AMPs) offer a promising solution to the antibiotic resistance crisis. However, an unresolved serious concern is that the evolution of resistance to therapeutic AMPs may generate cross-resistance to host AMPs, compromising a cornerstone of the innate immune response. We systematically tested this hypothesis using globally disseminated mobile colistin resistance (MCR) that has been selected by the use of colistin in agriculture and medicine. Here, we show that MCR provides a selective advantage to Escherichia coli in the presence of key AMPs from humans and agricultural animals by increasing AMP resistance. Moreover, MCR promotes bacterial growth in human serum and increases virulence in a Galleria mellonella infection model. Our study shows how the anthropogenic use of AMPs can drive the accidental evolution of resistance to the innate immune system of humans and animals. These findings have major implications for the design and use of therapeutic AMPs and suggest that MCR may be difficult to eradicate, even if colistin use is withdrawn. eLife Sciences Publications, Ltd 2023-04-25 /pmc/articles/PMC10129329/ /pubmed/37094804 http://dx.doi.org/10.7554/eLife.84395 Text en © 2023, Jangir et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Evolutionary Biology
Jangir, Pramod K
Ogunlana, Lois
Szili, Petra
Czikkely, Marton
Shaw, Liam P
Stevens, Emily J
Yu, Yang
Yang, Qiue
Wang, Yang
Pál, Csaba
Walsh, Timothy R
MacLean, Craig R
The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title_full The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title_fullStr The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title_full_unstemmed The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title_short The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
title_sort evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10129329/
https://www.ncbi.nlm.nih.gov/pubmed/37094804
http://dx.doi.org/10.7554/eLife.84395
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