High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform

IntroductionCarbapenemase-producing bacteria undermine the efficacy of carbapenems, a class of last-resort antibiotics used primarily to treat infections caused by multidrug-resistant Gram-negative pathogens. Carbapenemases are among the most alarming antimicrobial resistance mechanisms because they...

Full description

Saved in:
Bibliographic Details
Main Authors: Sascha D. Braun, Martin Reinicke, Celia Diezel, Elke Müller, Katrin Frankenfeld, Thomas Schumacher, Hugo Arends, Stefan Monecke, Ralf Ehricht
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1650094/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849222619015938048
author Sascha D. Braun
Sascha D. Braun
Martin Reinicke
Martin Reinicke
Celia Diezel
Celia Diezel
Elke Müller
Elke Müller
Katrin Frankenfeld
Thomas Schumacher
Hugo Arends
Stefan Monecke
Stefan Monecke
Ralf Ehricht
Ralf Ehricht
Ralf Ehricht
author_facet Sascha D. Braun
Sascha D. Braun
Martin Reinicke
Martin Reinicke
Celia Diezel
Celia Diezel
Elke Müller
Elke Müller
Katrin Frankenfeld
Thomas Schumacher
Hugo Arends
Stefan Monecke
Stefan Monecke
Ralf Ehricht
Ralf Ehricht
Ralf Ehricht
author_sort Sascha D. Braun
collection DOAJ
description IntroductionCarbapenemase-producing bacteria undermine the efficacy of carbapenems, a class of last-resort antibiotics used primarily to treat infections caused by multidrug-resistant Gram-negative pathogens. Carbapenemases are among the most alarming antimicrobial resistance mechanisms because they inactivate all β-lactam antibiotics leaving clinicians with few or no therapeutic options. The genes encoding these enzymes are typically located on mobile genetic elements (MGE), which facilitate rapid horizontal gene transfer among different bacterial species. These MGE’s often additionally carry toxin-antitoxin systems that promote long-term persistence in bacterial populations. Carbapenem-resistant Enterobacteriaceae (CRE) often colonize the gastrointestinal tract without symptoms, serving as silent reservoirs for further dissemination. Infections caused by CRE are associated with high morbidity and mortality and are frequently resistant to multiple drug classes. Given the urgent clinical need for rapid diagnostics, immunochromatographic assays represent a promising and urgently needed approach for economic and available point-of-care detection. However, the development of such assays is often hindered by the time-consuming process of identifying high-affinity antibody pairs.MethodsTo accelerate this process, we evaluated a protein microarray platform as a high-throughput screening tool to identify optimal monoclonal antibody (mAb) pairs targeting the most clinically relevant carbapenemases. Monoclonal antibodies derived from hybridoma libraries and commercial sources were spotted in triplicates and tested in a single experiment against lysates from reference strains expressing the carbapenemase enzymes KPC, NDM, IMP, VIM, OXA-23/48/58, and MCR-1, an enzyme conferring resistance to colistin. Signal intensities were quantified, and diagnostic performance was assessed across four thresholds.ResultsA cut-off > 0.2 yielded the best balance, with approximately 61% balanced accuracy and ≥99% specificity. Around 22% of tested antibodies showed strong, reproducible reactivity. For several targets–such as KPC, IMP, VIM, OXA-58, and MCR-1–100% sensitivity was achieved. The array allowed simultaneous mapping of cross-reactivity, a key advantage over conventional ELISA workflows.DiscussionOur findings confirm that protein-based microarrays offer a robust, efficient platform for antibody pair selection, reducing reagent use while accelerating assay development. The validated antibody pairs are directly applicable to ELISA or lateral flow test formats and provide a strong foundation for next-generation diagnostics capable of detecting an evolving panel of carbapenemases in clinical settings.
format Article
id doaj-art-d8f5f384d45249bd96cefa9f286b791b
institution Kabale University
issn 1664-302X
language English
publishDate 2025-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj-art-d8f5f384d45249bd96cefa9f286b791b2025-08-26T04:12:43ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-08-011610.3389/fmicb.2025.16500941650094High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platformSascha D. Braun0Sascha D. Braun1Martin Reinicke2Martin Reinicke3Celia Diezel4Celia Diezel5Elke Müller6Elke Müller7Katrin Frankenfeld8Thomas Schumacher9Hugo Arends10Stefan Monecke11Stefan Monecke12Ralf Ehricht13Ralf Ehricht14Ralf Ehricht15Leibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyLeibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyLeibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyLeibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyINTER-ARRAY Part of fzmb GmbH, Bad Langensalza, GermanyInstitut Virion\Serion GmbH, Würzburg, GermanyInstitut Virion\Serion GmbH, Würzburg, GermanyLeibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyLeibniz Institute of Photonic Technology, Member of the Research Alliance “Leibniz Health Technologies” and the Leibniz Centre for Photonics in Infection Research (LPI), Jena, GermanyInfectoGnostics Research Campus Jena, Center for Applied Research, Jena, GermanyInstitute of Physical Chemistry, Friedrich Schiller University Jena, Jena, GermanyIntroductionCarbapenemase-producing bacteria undermine the efficacy of carbapenems, a class of last-resort antibiotics used primarily to treat infections caused by multidrug-resistant Gram-negative pathogens. Carbapenemases are among the most alarming antimicrobial resistance mechanisms because they inactivate all β-lactam antibiotics leaving clinicians with few or no therapeutic options. The genes encoding these enzymes are typically located on mobile genetic elements (MGE), which facilitate rapid horizontal gene transfer among different bacterial species. These MGE’s often additionally carry toxin-antitoxin systems that promote long-term persistence in bacterial populations. Carbapenem-resistant Enterobacteriaceae (CRE) often colonize the gastrointestinal tract without symptoms, serving as silent reservoirs for further dissemination. Infections caused by CRE are associated with high morbidity and mortality and are frequently resistant to multiple drug classes. Given the urgent clinical need for rapid diagnostics, immunochromatographic assays represent a promising and urgently needed approach for economic and available point-of-care detection. However, the development of such assays is often hindered by the time-consuming process of identifying high-affinity antibody pairs.MethodsTo accelerate this process, we evaluated a protein microarray platform as a high-throughput screening tool to identify optimal monoclonal antibody (mAb) pairs targeting the most clinically relevant carbapenemases. Monoclonal antibodies derived from hybridoma libraries and commercial sources were spotted in triplicates and tested in a single experiment against lysates from reference strains expressing the carbapenemase enzymes KPC, NDM, IMP, VIM, OXA-23/48/58, and MCR-1, an enzyme conferring resistance to colistin. Signal intensities were quantified, and diagnostic performance was assessed across four thresholds.ResultsA cut-off > 0.2 yielded the best balance, with approximately 61% balanced accuracy and ≥99% specificity. Around 22% of tested antibodies showed strong, reproducible reactivity. For several targets–such as KPC, IMP, VIM, OXA-58, and MCR-1–100% sensitivity was achieved. The array allowed simultaneous mapping of cross-reactivity, a key advantage over conventional ELISA workflows.DiscussionOur findings confirm that protein-based microarrays offer a robust, efficient platform for antibody pair selection, reducing reagent use while accelerating assay development. The validated antibody pairs are directly applicable to ELISA or lateral flow test formats and provide a strong foundation for next-generation diagnostics capable of detecting an evolving panel of carbapenemases in clinical settings.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1650094/fullcarbapenemaseprotein microarraymonoclonal antibodyantimicrobial resistancelateral flow assayhigh-throughput antibody screening
spellingShingle Sascha D. Braun
Sascha D. Braun
Martin Reinicke
Martin Reinicke
Celia Diezel
Celia Diezel
Elke Müller
Elke Müller
Katrin Frankenfeld
Thomas Schumacher
Hugo Arends
Stefan Monecke
Stefan Monecke
Ralf Ehricht
Ralf Ehricht
Ralf Ehricht
High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
Frontiers in Microbiology
carbapenemase
protein microarray
monoclonal antibody
antimicrobial resistance
lateral flow assay
high-throughput antibody screening
title High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
title_full High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
title_fullStr High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
title_full_unstemmed High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
title_short High-throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
title_sort high throughput screening of monoclonal antibodies against carbapenemases using a multiplex protein microarray platform
topic carbapenemase
protein microarray
monoclonal antibody
antimicrobial resistance
lateral flow assay
high-throughput antibody screening
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1650094/full
work_keys_str_mv AT saschadbraun highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT saschadbraun highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT martinreinicke highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT martinreinicke highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT celiadiezel highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT celiadiezel highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT elkemuller highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT elkemuller highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT katrinfrankenfeld highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT thomasschumacher highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT hugoarends highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT stefanmonecke highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT stefanmonecke highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT ralfehricht highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT ralfehricht highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform
AT ralfehricht highthroughputscreeningofmonoclonalantibodiesagainstcarbapenemasesusingamultiplexproteinmicroarrayplatform