Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics

Abstract Antibiotic‐resistant enterococci represent a significant global health challenge. Unfortunately, most β‐lactam antibiotics are not applicable for enterococcal infections due to intrinsic resistance. To extend their antimicrobial spectrum, polycationic peptides are conjugated to examples fro...

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Main Authors: Julia Werner, Florian Umstätter, Manuel B. Böhmann, Hannah Müller, Barbro Beijer, Tobias Hertlein, Laura Kaschnitz, Veronika Bram, Christian Kleist, Karel D. Klika, Eric Mühlberg, Gabriel Braune, Sabrina Wohlfart, Martin Gärtner, Silke Peter, Stefan Zimmermann, Uwe Haberkorn, Knut Ohlsen, Heike Brötz‐Oesterhelt, Walter Mier, Philipp Uhl
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202411406
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author Julia Werner
Florian Umstätter
Manuel B. Böhmann
Hannah Müller
Barbro Beijer
Tobias Hertlein
Laura Kaschnitz
Veronika Bram
Christian Kleist
Karel D. Klika
Eric Mühlberg
Gabriel Braune
Sabrina Wohlfart
Martin Gärtner
Silke Peter
Stefan Zimmermann
Uwe Haberkorn
Knut Ohlsen
Heike Brötz‐Oesterhelt
Walter Mier
Philipp Uhl
author_facet Julia Werner
Florian Umstätter
Manuel B. Böhmann
Hannah Müller
Barbro Beijer
Tobias Hertlein
Laura Kaschnitz
Veronika Bram
Christian Kleist
Karel D. Klika
Eric Mühlberg
Gabriel Braune
Sabrina Wohlfart
Martin Gärtner
Silke Peter
Stefan Zimmermann
Uwe Haberkorn
Knut Ohlsen
Heike Brötz‐Oesterhelt
Walter Mier
Philipp Uhl
author_sort Julia Werner
collection DOAJ
description Abstract Antibiotic‐resistant enterococci represent a significant global health challenge. Unfortunately, most β‐lactam antibiotics are not applicable for enterococcal infections due to intrinsic resistance. To extend their antimicrobial spectrum, polycationic peptides are conjugated to examples from each of the four classes of β‐lactam antibiotics. Remarkably, the β‐lactam–peptide conjugates gained an up to 1000‐fold increase in antimicrobial activity against vancomycin‐susceptible and vancomycin‐resistant enterococci. Even against β‐lactam‐resistant Gram‐negative strains, the conjugates are found to be effective despite their size exceeding the exclusion volume of porins. The extraordinary gain of activity can be explained by an altered mode of killing. Of note, the conjugates showed a concentration‐dependent activity in contrast to the parent β‐lactam antibiotics that exhibited a time‐dependent mode of action. In comparison to the parent β‐lactams, the conjugates showed altered affinities to the penicillin‐binding proteins. Furthermore, it is found that peptide conjugation also resulted in a different elimination route of the compounds when administered to rodents. In mice systemically infected with vancomycin‐resistant enterococci, treatment with a β‐lactam–peptide conjugate reduced bacterial burden in the liver compared to its originator. Therefore, peptide modification of β–lactam antibiotics represents a promising platform strategy to broaden their efficacy spectrum, particularly against enterococci.
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spelling doaj-art-c8cf6c9c25604e73b81684810e69cbf82025-08-20T02:55:53ZengWileyAdvanced Science2198-38442024-12-011148n/an/a10.1002/advs.202411406Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam AntibioticsJulia Werner0Florian Umstätter1Manuel B. Böhmann2Hannah Müller3Barbro Beijer4Tobias Hertlein5Laura Kaschnitz6Veronika Bram7Christian Kleist8Karel D. Klika9Eric Mühlberg10Gabriel Braune11Sabrina Wohlfart12Martin Gärtner13Silke Peter14Stefan Zimmermann15Uwe Haberkorn16Knut Ohlsen17Heike Brötz‐Oesterhelt18Walter Mier19Philipp Uhl20Department of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Pharmaceutical Technology Institute of Pharmacy and Molecular Biotechnology Heidelberg University 69120 Heidelberg GermanyMicrobial Bioactive Compounds Interfaculty Institute of Microbiology and Infection Medicine University of Tübingen 72076 Tübingen GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyInstitute of Molecular Infection Biology University of Würzburg 97080 Würzburg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyNMR Spectroscopy Analysis Unit German Cancer Research Center (DKFZ) 69120 Heidelberg GermanyDepartment of Pharmaceutical Technology Institute of Pharmacy and Molecular Biotechnology Heidelberg University 69120 Heidelberg GermanyInstitute of Molecular Infection Biology University of Würzburg 97080 Würzburg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Pharmaceutical and Bioorganic Chemistry Institute of Pharmacy and Molecular Biotechnology Heidelberg University 69120 Heidelberg GermanyMedical Microbiology Interfaculty Institute of Microbiology and Infection Medicine University of Tübingen 72076 Tübingen GermanyDepartment of Infectious Diseases Medical Microbiology and Hygiene Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyInstitute of Molecular Infection Biology University of Würzburg 97080 Würzburg GermanyMicrobial Bioactive Compounds Interfaculty Institute of Microbiology and Infection Medicine University of Tübingen 72076 Tübingen GermanyDepartment of Nuclear Medicine Heidelberg University Hospital 69120 Heidelberg GermanyDepartment of Pharmaceutical Technology Institute of Pharmacy and Molecular Biotechnology Heidelberg University 69120 Heidelberg GermanyAbstract Antibiotic‐resistant enterococci represent a significant global health challenge. Unfortunately, most β‐lactam antibiotics are not applicable for enterococcal infections due to intrinsic resistance. To extend their antimicrobial spectrum, polycationic peptides are conjugated to examples from each of the four classes of β‐lactam antibiotics. Remarkably, the β‐lactam–peptide conjugates gained an up to 1000‐fold increase in antimicrobial activity against vancomycin‐susceptible and vancomycin‐resistant enterococci. Even against β‐lactam‐resistant Gram‐negative strains, the conjugates are found to be effective despite their size exceeding the exclusion volume of porins. The extraordinary gain of activity can be explained by an altered mode of killing. Of note, the conjugates showed a concentration‐dependent activity in contrast to the parent β‐lactam antibiotics that exhibited a time‐dependent mode of action. In comparison to the parent β‐lactams, the conjugates showed altered affinities to the penicillin‐binding proteins. Furthermore, it is found that peptide conjugation also resulted in a different elimination route of the compounds when administered to rodents. In mice systemically infected with vancomycin‐resistant enterococci, treatment with a β‐lactam–peptide conjugate reduced bacterial burden in the liver compared to its originator. Therefore, peptide modification of β–lactam antibiotics represents a promising platform strategy to broaden their efficacy spectrum, particularly against enterococci.https://doi.org/10.1002/advs.202411406enterococcipolycationic peptidesresistanceβ‐lactam antibiotics
spellingShingle Julia Werner
Florian Umstätter
Manuel B. Böhmann
Hannah Müller
Barbro Beijer
Tobias Hertlein
Laura Kaschnitz
Veronika Bram
Christian Kleist
Karel D. Klika
Eric Mühlberg
Gabriel Braune
Sabrina Wohlfart
Martin Gärtner
Silke Peter
Stefan Zimmermann
Uwe Haberkorn
Knut Ohlsen
Heike Brötz‐Oesterhelt
Walter Mier
Philipp Uhl
Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
Advanced Science
enterococci
polycationic peptides
resistance
β‐lactam antibiotics
title Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
title_full Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
title_fullStr Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
title_full_unstemmed Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
title_short Conjugation of Polycationic Peptides Extends the Efficacy Spectrum of β‐Lactam Antibiotics
title_sort conjugation of polycationic peptides extends the efficacy spectrum of β lactam antibiotics
topic enterococci
polycationic peptides
resistance
β‐lactam antibiotics
url https://doi.org/10.1002/advs.202411406
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