Oseltamivir aziridines are potent influenza neuraminidase inhibitors and imaging agents

M Merijn B. L. Vriends (Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University) E Elisha Moran (Department of Chemistry, University of York Heslington) M Martín Calvelo (Centro Singular de Investigación en Química Biolóxica e Materiais Moleculares (CiQUS) and Departamento de Química Orgánica Universidade de Santiago de Compostela) T Thomas Hansen I Isabelle B. Pickles (Department of Chemistry, The University York, Heslington, York YO10 5DD, United Kingdom) X Xincheng Xin (Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University) M Marieke Biezeno (Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University) Z Zachary W. B. Armstrong (Leiden Institute of Chemistry, Leiden University) M Maria J. Ferraz (Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University) L Lei Li A Alice Lilley (Worldwide Influenza Centre, The Francis Crick Institute) R Ruth Harvey D Dmitri V. Filippov (Leiden Institute of Chemistry, Leiden University , , ,) Q Qinghua Liao (Departament de Química Inorgaǹica i Orgaǹica (Seccióde Química Orgaǹica) and Institut de Química TeorÌica I Computacional, Universitat de Barcelona) S Sybrin P. Schröder (Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University) G Gijsbert A. van der Marel (Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands) M Marta Artola (Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University) J Johannes M. F. G. Aerts (Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University) J James N. Blaza J Jeroen D. C. Codée (Leiden Institute of Chemistry) C Carme Rovira (Departament de Química Inorgànica i Orgànica (Secció de Química Orgànica) and Institut de Química Teòrica i Computacional (IQTCUB)) H Herman S. Overkleeft (Leiden Institute of Chemistry) G Gideon J. Davies

Abstract

Influenza neuraminidase (NA) is a critical target for seasonal and pandemic antivirals, including the strains of current concern. Current treatments, such as Zanamivir and Oseltamivir, are limited by noncovalent binding and emerging resistance. We hypothesized that Oseltamivir aziridines would unite transition-state mimicry for tight binding, with aziridine-enabled covalent capture of the catalytic tyrosine, thereby supporting both therapy and activity-based quantification. Here, we present oseltamivir-based aziridines, inspired by cyclophellitol chemistry, that act as covalent inhibitors and activity-based probes via an N -acylaziridine warhead. Free-energy calculations, and NMR observations, indicate a 4 H 5 half-chair preference consistent with the NA transition state, and selected analogues inhibit multiple NA subtypes with low nanomolar binding constants. Diverse evidence establishes covalency: time-dependent inactivation, inhibitor washout, intact-mass shifts, MS/MS identification of a tyrosine adduct, and QM/MM reaction profiles, while cryoEM of N1 aligns with the proposed binding mode, revealing an elimination product. The inhibitors demonstrate formidable activity against diverse viral neuraminidases, including H5N1, and further enable imaging and quantification of active NA. With their dual therapeutic and diagnostic potential, these first-in-class inhibitors indeed benefit from transition state mimicry and covalency, and thus offer a powerful platform for antiviral development and neuraminidase imaging, addressing urgent global health needs in influenza treatment and prevention.

Article Details

Volume / Issue Vol. 123, Issue 13
Published March 31, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (23)

M

Merijn B. L. Vriends

Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University

E

Elisha Moran

Department of Chemistry, University of York Heslington

M

Martín Calvelo

Centro Singular de Investigación en Química Biolóxica e Materiais Moleculares (CiQUS) and Departamento de Química Orgánica Universidade de Santiago de Compostela

T

Thomas Hansen

I

Isabelle B. Pickles

Department of Chemistry, The University York, Heslington, York YO10 5DD, United Kingdom

X

Xincheng Xin

Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University

M

Marieke Biezeno

Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University

Z

Zachary W. B. Armstrong

Leiden Institute of Chemistry, Leiden University

M

Maria J. Ferraz

Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University

L

Lei Li

A

Alice Lilley

Worldwide Influenza Centre, The Francis Crick Institute

R

Ruth Harvey

D

Dmitri V. Filippov

Leiden Institute of Chemistry, Leiden University , , ,

Q

Qinghua Liao

Departament de Química Inorgaǹica i Orgaǹica (Seccióde Química Orgaǹica) and Institut de Química TeorÌica I Computacional, Universitat de Barcelona

S

Sybrin P. Schröder

Department of Bio-organic Synthesis, Leiden Institute of Chemistry, Leiden University

G

Gijsbert A. van der Marel

Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, 2333 CC Leiden, The Netherlands

M

Marta Artola

Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University

J

Johannes M. F. G. Aerts

Department of Medical Biochemistry, Leiden Institute of Chemistry, Leiden University

J

James N. Blaza

J

Jeroen D. C. Codée

Leiden Institute of Chemistry

C

Carme Rovira

Departament de Química Inorgànica i Orgànica (Secció de Química Orgànica) and Institut de Química Teòrica i Computacional (IQTCUB)

H

Herman S. Overkleeft

Leiden Institute of Chemistry

G

Gideon J. Davies