Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX

We designed novel pre-drug compounds that transform into an active form that covalently modifies particular His residue in the active site, a difficult task to achieve, and applied to carbonic anhydrase (CAIX), a transmembrane protein, highly overexpressed in hypoxic solid tumors, important for canc...

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Main Authors: Aivaras Vaškevičius, Denis Baronas, Janis Leitans, Agnė Kvietkauskaitė, Audronė Rukšėnaitė, Elena Manakova, Zigmantas Toleikis, Algirdas Kaupinis, Andris Kazaks, Marius Gedgaudas, Aurelija Mickevičiūtė, Vaida Juozapaitienė, Helgi B Schiöth, Kristaps Jaudzems, Mindaugas Valius, Kaspars Tars, Saulius Gražulis, Franz-Josef Meyer-Almes, Jurgita Matulienė, Asta Zubrienė, Virginija Dudutienė, Daumantas Matulis
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/101401
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author Aivaras Vaškevičius
Denis Baronas
Janis Leitans
Agnė Kvietkauskaitė
Audronė Rukšėnaitė
Elena Manakova
Zigmantas Toleikis
Algirdas Kaupinis
Andris Kazaks
Marius Gedgaudas
Aurelija Mickevičiūtė
Vaida Juozapaitienė
Helgi B Schiöth
Kristaps Jaudzems
Mindaugas Valius
Kaspars Tars
Saulius Gražulis
Franz-Josef Meyer-Almes
Jurgita Matulienė
Asta Zubrienė
Virginija Dudutienė
Daumantas Matulis
author_facet Aivaras Vaškevičius
Denis Baronas
Janis Leitans
Agnė Kvietkauskaitė
Audronė Rukšėnaitė
Elena Manakova
Zigmantas Toleikis
Algirdas Kaupinis
Andris Kazaks
Marius Gedgaudas
Aurelija Mickevičiūtė
Vaida Juozapaitienė
Helgi B Schiöth
Kristaps Jaudzems
Mindaugas Valius
Kaspars Tars
Saulius Gražulis
Franz-Josef Meyer-Almes
Jurgita Matulienė
Asta Zubrienė
Virginija Dudutienė
Daumantas Matulis
author_sort Aivaras Vaškevičius
collection DOAJ
description We designed novel pre-drug compounds that transform into an active form that covalently modifies particular His residue in the active site, a difficult task to achieve, and applied to carbonic anhydrase (CAIX), a transmembrane protein, highly overexpressed in hypoxic solid tumors, important for cancer cell survival and proliferation because it acidifies tumor microenvironment helping invasion and metastases processes. The designed compounds have several functionalities: (1) primary sulfonamide group recognizing carbonic anhydrases (CA), (2) high-affinity moieties specifically recognizing CAIX among all CA isozymes, and (3) forming a covalent bond with the His64 residue. Such targeted covalent compounds possess both high initial affinity and selectivity for the disease target protein followed by complete irreversible inactivation of the protein via covalent modification. Our designed prodrug candidates bearing moderately active pre-vinylsulfone esters or weakly active carbamates optimized for mild covalent modification activity to avoid toxic non-specific modifications and selectively target CAIX. The lead inhibitors reached 2 pM affinity, the highest among known CAIX inhibitors. The strategy could be used for any disease drug target protein bearing a His residue in the vicinity of the active site.
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spelling doaj-art-d2000c0aa6154247b81fece6681bfd672025-08-20T01:58:28ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.101401Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IXAivaras Vaškevičius0https://orcid.org/0009-0006-8202-9748Denis Baronas1https://orcid.org/0000-0003-1878-0837Janis Leitans2Agnė Kvietkauskaitė3Audronė Rukšėnaitė4Elena Manakova5Zigmantas Toleikis6Algirdas Kaupinis7Andris Kazaks8Marius Gedgaudas9Aurelija Mickevičiūtė10Vaida Juozapaitienė11Helgi B Schiöth12Kristaps Jaudzems13Mindaugas Valius14Kaspars Tars15Saulius Gražulis16Franz-Josef Meyer-Almes17https://orcid.org/0000-0002-1001-3249Jurgita Matulienė18Asta Zubrienė19Virginija Dudutienė20Daumantas Matulis21https://orcid.org/0000-0002-6178-6276Department of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaLatvian Biomedical Research and Study Centre, Riga, LatviaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biological DNA Modification, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Protein - DNA Interactions, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaSector of Biocatalysis, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaProteomics Center, Institute of Biochemistry, Life Sciences Center, Vilnius University, Vilnius, LithuaniaLatvian Biomedical Research and Study Centre, Riga, LatviaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaFunctional Pharmacology and Neuroscience, Department of Surgical Sciences, Uppsala University, Uppsala, SwedenLatvian Institute of Organic Synthesis, Riga, LatviaProteomics Center, Institute of Biochemistry, Life Sciences Center, Vilnius University, Vilnius, LithuaniaLatvian Biomedical Research and Study Centre, Riga, LatviaSector of Crystallography and Chemical Informatics, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Chemical Engineering and Biotechnology, University of Applied Sciences Darmstadt, Darmstadt, GermanyDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaDepartment of Biothermodynamics and Drug Design, Institute of Biotechnology, Life Sciences Center, Vilnius University, Vilnius, LithuaniaWe designed novel pre-drug compounds that transform into an active form that covalently modifies particular His residue in the active site, a difficult task to achieve, and applied to carbonic anhydrase (CAIX), a transmembrane protein, highly overexpressed in hypoxic solid tumors, important for cancer cell survival and proliferation because it acidifies tumor microenvironment helping invasion and metastases processes. The designed compounds have several functionalities: (1) primary sulfonamide group recognizing carbonic anhydrases (CA), (2) high-affinity moieties specifically recognizing CAIX among all CA isozymes, and (3) forming a covalent bond with the His64 residue. Such targeted covalent compounds possess both high initial affinity and selectivity for the disease target protein followed by complete irreversible inactivation of the protein via covalent modification. Our designed prodrug candidates bearing moderately active pre-vinylsulfone esters or weakly active carbamates optimized for mild covalent modification activity to avoid toxic non-specific modifications and selectively target CAIX. The lead inhibitors reached 2 pM affinity, the highest among known CAIX inhibitors. The strategy could be used for any disease drug target protein bearing a His residue in the vicinity of the active site.https://elifesciences.org/articles/101401targeted covalent inhibitorscarbonic anhydrase IXvinylsulfonesulfonamidefluorescent thermal shift assayX-ray crystallography
spellingShingle Aivaras Vaškevičius
Denis Baronas
Janis Leitans
Agnė Kvietkauskaitė
Audronė Rukšėnaitė
Elena Manakova
Zigmantas Toleikis
Algirdas Kaupinis
Andris Kazaks
Marius Gedgaudas
Aurelija Mickevičiūtė
Vaida Juozapaitienė
Helgi B Schiöth
Kristaps Jaudzems
Mindaugas Valius
Kaspars Tars
Saulius Gražulis
Franz-Josef Meyer-Almes
Jurgita Matulienė
Asta Zubrienė
Virginija Dudutienė
Daumantas Matulis
Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
eLife
targeted covalent inhibitors
carbonic anhydrase IX
vinylsulfone
sulfonamide
fluorescent thermal shift assay
X-ray crystallography
title Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
title_full Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
title_fullStr Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
title_full_unstemmed Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
title_short Targeted anticancer pre-vinylsulfone covalent inhibitors of carbonic anhydrase IX
title_sort targeted anticancer pre vinylsulfone covalent inhibitors of carbonic anhydrase ix
topic targeted covalent inhibitors
carbonic anhydrase IX
vinylsulfone
sulfonamide
fluorescent thermal shift assay
X-ray crystallography
url https://elifesciences.org/articles/101401
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