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J Mol Biol . Allosteric targeting of the ACE2 dimer interface by a medium-sized compound inhibits SARS-CoV-2 entry

tetano

Editor, Senior Moderator
J Mol Biol


. 2026 Jun 22:169914.
doi: 10.1016/j.jmb.2026.169914. Online ahead of print.
Allosteric targeting of the ACE2 dimer interface by a medium-sized compound inhibits SARS-CoV-2 entry

Mariko Yokogawa[SUP] 1 [/SUP], Shunki Kaneichi[SUP] 1 [/SUP], Mahoro Horiuchi[SUP] 1 [/SUP], Taiga Otake[SUP] 1 [/SUP], Tomoki Yonezawa[SUP] 1 [/SUP], Yugo Shimizu[SUP] 2 [/SUP], Kazuyoshi Ikeda[SUP] 2 [/SUP], Yuichiro Yamamoto[SUP] 3 [/SUP], Shota Sakai[SUP] 4 [/SUP], Yoshimi Shimizu[SUP] 5 [/SUP], Kohji Noguchi[SUP] 6 [/SUP], Masayoshi Fukasawa[SUP] 6 [/SUP], Mitsuhiko Ikura[SUP] 7 [/SUP], Masanori Osawa[SUP] 8 [/SUP]


Affiliations
Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), enters host cells via interaction between the receptor-binding domain of the spike protein (RBD[SUB]SP[/SUB]) and the peptidase domain (PD) of the host angiotensin-converting enzyme 2 (ACE2). However, no drugs that directly inhibit this interaction have been clinically approved. To discover novel inhibitors, we developed an artificial intelligence (AI)-guided virtual screening approach focused on medium-sized synthetic compounds ≥500 Da. One hit compound inhibited the RBD[SUB]SP[/SUB]-PD[SUB]ACE2[/SUB] interaction and suppressed SARS-CoV-2 infection. Nuclear magnetic resonance (NMR) titration revealed direct binding to PD[SUB]ACE2[/SUB], not RBD[SUB]SP[/SUB]. ACE2 forms dimers that interconvert between tight and loose conformations, with the tight form stabilized by inter-subunit hydrogen bonds. Extensive NMR analysis using isotopically-labeled PD[SUB]ACE2[/SUB] identified a putative compound-binding region near the PD[SUB]ACE2[/SUB] dimer interface, distinct from the RBD[SUB]SP[/SUB]-binding site. Docking simulations and infection assays using ACE2 mutants deficient in inter-subunit hydrogen bonding provided further evidence for a model in which compound binding is compatible with the loose dimer conformation and may shift the conformational equilibrium away from the tight dimer state, thereby impairing viral entry. These findings uncovered a previously unrecognized allosteric regulatory region within ACE2, which can be targeted by medium-sized molecules to modulate ACE2 conformational equilibrium to inhibit SARS-CoV-2 infection.

Keywords: ACE2 dimer; Medium-sized molecule; Protein-protein interaction; SARS-CoV-2; Solution NMR.

 
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