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@ARTICLE{Weller:638759,
author = {Weller, Caroline and Burnett, G. Leslie and Jiang, Lingyan
and Chakraborty, Sujata and Zhang, Dongyu and Vita, Nicole
A. and Dilly, Julien and Kim, Eejung and Maldonato, Benjamin
and Seamon, Kyle and Eilerts, Diane F. and Milin, Anthony
and Marquez, Abby and Spradlin, Jessica and Helland, Ciara
and Gould, Andrea and Ziv, Tamar Bar and Dinh, Phuong and
Steele, Shelby L. and Wang, Zhican and Mu, Yunming and
Chugh, Seema and Feng, Hanrong and Hennessey, Conner and
Wang, Junning and Roth, Jennifer and Rees, Matthew and
Ronan, Melissa and Wolpin, Brian M. and Hahn, William C. and
Holderfield, Matthew and Wang, Zhengping and Koltun, Elena
S. and Singh, Mallika and Gill, Adrian L. and Smith,
Jacqueline A. M. and Aguirre, Andrew J. and Jiang, Jingjing
and Knox, John E. and Wildes, David},
title = {{A} neomorphic protein interface catalyzes covalent
inhibition of {RAS} {G}12{D} aspartic acid in tumors},
journal = {Science / Science now},
volume = {389},
number = {6758},
issn = {0036-8075},
address = {Washington, DC},
publisher = {Assoc.},
reportid = {PUBDB-2025-04190},
pages = {eads0239},
year = {2025},
note = {ISSN 1095-9203 not unique: **3 hits**. Waiting for
fulltext},
abstract = {INTRODUCTIONMutant RAS is the primary oncogenic driver in
RAS-addicted cancers. RAS proteins act as molecular switches
that cycle between a guanosine triphosphate–bound “ON”
state and a guanosine diphosphate–bound “OFF” state.
Under normal circumstances, cell growth is tightly regulated
by modulating the population of RAS in the ON versus the OFF
state. In RAS-addicted cancers, mutations in RAS shift this
balance towards the ON state, leading to increased RAS
signaling and uncontrolled cell growth. Mutations in RAS are
present in nearly a quarter of a million new cancer cases
each year and are particularly frequent in pancreatic,
colorectal, and lung cancers.RATIONALEHistorically,
RAS-addicted cancers have been challenging to treat with
targeted drug therapies. Mutant-selective inhibitors that
covalently and irreversibly inactivate mutant RAS are
advantageous because they target the mutant protein present
only in cancer cells and can achieve sustained target
engagement even in the context of variable tumor exposures
that often result from typical inhibitor dosing schedules.
Such irreversible inhibitors of KRASG12C, in which glycine
is replaced with a reactive thiol-containing cysteine
residue, have been approved for both lung and colorectal
cancers, but no similar therapies are available for the most
common RAS mutation, KRASG12D. This mutation introduces a
carboxylate-containing aspartic acid residue that has low
reactivity and high abundance on protein surfaces compared
with cysteine, thereby posing substantial hurdles to the
design of irreversible inhibitors that have sufficient
potency and selectivity yet maintain the properties
necessary to enable once-daily oral dosing.RESULTSTo create
covalent inhibitors of KRASG12D, we used structure-based
drug design to modify compounds that bind the abundant
intracellular chaperone cyclophilin A (CYPA) and create a
neomorphic protein-protein interface between CYPA and active
RAS to covalently modify the D12 mutation located in the
induced pocket at the interface. Precisely positioning
reactive groups within this privileged environment enabled
selective, enzyme-like rate enhancement of the covalent
reaction between D12 and aziridine warheads that have low
intrinsic reactivity. X-ray crystal structures and
computational methods confirmed a role for the
protein-protein interface in enabling selective reactivity.
This approach yielded the investigational agent zoldonrasib
(RMC-9805), currently undergoing clinical evaluation
(NCT06040541), and the preclinical compound RMC-9945. These
compounds efficiently covalently engaged RASG12D and
potently suppressed oncogenic RAS signaling in
RASG12D-mutant cancer cell lines in a CYPA-dependent manner.
Consistent with the mechanism of action, the compounds
exhibited low-potency noncovalent inhibition of RAS-driven
proliferation in cell lines and patient-derived organoids
with wild-type and non-G12D mutant RAS, and covalency
conferred selectivity and durability of inhibition toward
RASG12D. The chemical and metabolic stability was sufficient
to enable once-daily oral dosing in mice, and zoldonrasib
displayed marked antitumor activity in multiple preclinical
models of KRASG12D-mutant pancreatic, lung, and colorectal
cancers.CONCLUSIONCreation of a neomorphic protein-protein
interface at RAS through chemical remodeling of the cellular
chaperone CYPA selectively accelerated covalent bond
formation between an inhibitor and an aspartic acid residue,
enabling discovery of potent and irreversible inhibitors of
the most common RAS mutation in human cancers. Zoldonrasib
is an orally bioavailable, RAS(ON) G12D–selective covalent
inhibitor that drives deep and durable tumor regressions in
multiple preclinical models of KRASG12D cancers across
indications. This strategy has the potential to greatly
expand the repertoire of residues on cancer drivers or other
proteins of therapeutic value that can be targeted by
covalent warheads and may enable additional mechanisms of
target modulation.},
cin = {EMBL-User},
ddc = {320},
cid = {I:(DE-H253)EMBL-User-20120814},
pnm = {6G3 - PETRA III (DESY) (POF4-6G3)},
pid = {G:(DE-HGF)POF4-6G3},
experiment = {EXP:(DE-H253)P-P13-20150101},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:40705880},
doi = {10.1126/science.ads0239},
url = {https://bib-pubdb1.desy.de/record/638759},
}