Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics

Abstract Novel scaffolds for broad-spectrum antibiotics are rare and in strong demand because of the increase in antimicrobial resistance. The cystobactamids, discovered from myxobacterial sources, have a unique hexapeptidic scaffold with five arylamides and possess potent, resistance-breaking prope...

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Main Authors: Moritz Stappert, Daniel Kohnhäuser, Tim Seedorf, Janetta Coetzee, Katharina Rox, Hazel L. S. Fuchs, Katarina Cirnski, Christian Leitner, Jennifer Herrmann, Andreas Kirschning, Rolf Müller, Mark Brönstrup
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Communications Chemistry
Online Access:https://doi.org/10.1038/s42004-024-01337-6
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author Moritz Stappert
Daniel Kohnhäuser
Tim Seedorf
Janetta Coetzee
Katharina Rox
Hazel L. S. Fuchs
Katarina Cirnski
Christian Leitner
Jennifer Herrmann
Andreas Kirschning
Rolf Müller
Mark Brönstrup
author_facet Moritz Stappert
Daniel Kohnhäuser
Tim Seedorf
Janetta Coetzee
Katharina Rox
Hazel L. S. Fuchs
Katarina Cirnski
Christian Leitner
Jennifer Herrmann
Andreas Kirschning
Rolf Müller
Mark Brönstrup
author_sort Moritz Stappert
collection DOAJ
description Abstract Novel scaffolds for broad-spectrum antibiotics are rare and in strong demand because of the increase in antimicrobial resistance. The cystobactamids, discovered from myxobacterial sources, have a unique hexapeptidic scaffold with five arylamides and possess potent, resistance-breaking properties. This study investigates the role of the central D-ring pharmacophore in cystobactamids, a para-aminobenzoic acid (PABA) moiety that is additionally substituted by hydroxy and isopropoxy functions. We varied the two oxygenated substituents and replaced both amide connectors with bioisosteres. Synthetic routes were developed that included metal-mediated aromatic functionalization or heterocycle formations, leading to 19 novel analogues. The antibiotic efficacy of all analogues was determined against bacteria from the ESKAPE pathogen panel. While the replacement and the repositioning of hydroxy and isopropoxy substituents was not advantageous, exchanging PABA by terephthalic acid amides led to the highly potent analogue 42 with broad-spectrum activity, insensitivity towards AlbD-mediated degradation and promising pharmacokinetic properties in mice. The study highlights the steep structure-activity relationships in the tetrasubstituted D-ring and a surprisingly favorable reversion of the amide connecting C and D.
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spelling doaj-art-b595c14c19e3465bb481bd5a0c131d1a2025-08-20T02:50:03ZengNature PortfolioCommunications Chemistry2399-36692024-11-017111510.1038/s42004-024-01337-6Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibioticsMoritz Stappert0Daniel Kohnhäuser1Tim Seedorf2Janetta Coetzee3Katharina Rox4Hazel L. S. Fuchs5Katarina Cirnski6Christian Leitner7Jennifer Herrmann8Andreas Kirschning9Rolf Müller10Mark Brönstrup11Department of Chemical Biology, Helmholtz Centre for Infection ResearchDepartment of Chemical Biology, Helmholtz Centre for Infection ResearchInstitut für Organische Chemie und Biomolekulares Wirkstoffzentrum (BMWZ), Leibniz Universität Hannover Schneiderberg 1BHelmholtz Institute for Pharmaceutical Research Saarland, Universitätscampus E8.1Department of Chemical Biology, Helmholtz Centre for Infection ResearchDepartment of Chemical Biology, Helmholtz Centre for Infection ResearchHelmholtz Institute for Pharmaceutical Research Saarland, Universitätscampus E8.1Institut für Organische Chemie und Biomolekulares Wirkstoffzentrum (BMWZ), Leibniz Universität Hannover Schneiderberg 1BHelmholtz Institute for Pharmaceutical Research Saarland, Universitätscampus E8.1Institut für Organische Chemie und Biomolekulares Wirkstoffzentrum (BMWZ), Leibniz Universität Hannover Schneiderberg 1BHelmholtz Institute for Pharmaceutical Research Saarland, Universitätscampus E8.1Department of Chemical Biology, Helmholtz Centre for Infection ResearchAbstract Novel scaffolds for broad-spectrum antibiotics are rare and in strong demand because of the increase in antimicrobial resistance. The cystobactamids, discovered from myxobacterial sources, have a unique hexapeptidic scaffold with five arylamides and possess potent, resistance-breaking properties. This study investigates the role of the central D-ring pharmacophore in cystobactamids, a para-aminobenzoic acid (PABA) moiety that is additionally substituted by hydroxy and isopropoxy functions. We varied the two oxygenated substituents and replaced both amide connectors with bioisosteres. Synthetic routes were developed that included metal-mediated aromatic functionalization or heterocycle formations, leading to 19 novel analogues. The antibiotic efficacy of all analogues was determined against bacteria from the ESKAPE pathogen panel. While the replacement and the repositioning of hydroxy and isopropoxy substituents was not advantageous, exchanging PABA by terephthalic acid amides led to the highly potent analogue 42 with broad-spectrum activity, insensitivity towards AlbD-mediated degradation and promising pharmacokinetic properties in mice. The study highlights the steep structure-activity relationships in the tetrasubstituted D-ring and a surprisingly favorable reversion of the amide connecting C and D.https://doi.org/10.1038/s42004-024-01337-6
spellingShingle Moritz Stappert
Daniel Kohnhäuser
Tim Seedorf
Janetta Coetzee
Katharina Rox
Hazel L. S. Fuchs
Katarina Cirnski
Christian Leitner
Jennifer Herrmann
Andreas Kirschning
Rolf Müller
Mark Brönstrup
Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
Communications Chemistry
title Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
title_full Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
title_fullStr Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
title_full_unstemmed Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
title_short Synthetic studies on the tetrasubstituted D-ring of cystobactamids lead to potent terephthalic acid antibiotics
title_sort synthetic studies on the tetrasubstituted d ring of cystobactamids lead to potent terephthalic acid antibiotics
url https://doi.org/10.1038/s42004-024-01337-6
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