Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer

Abstract Chaperone-mediated autophagy (CMA), a type of selective degradation of cytosolic proteins in lysosomes, is commonly upregulated in cancer cells, contributing to their survival and growth. The lack of a specific target for CMA inhibition has limited CMA blockage to genetic manipulations or g...

Full description

Saved in:
Bibliographic Details
Main Authors: Mericka McCabe, Rajanya Bhattacharyya, Rebecca Sereda, Olaya Santiago-Fernández, Rabia R Khawaja, Antonio Diaz, Kristen Lindenau, Deniz Gulfem Ozturk, Thomas P Garner, Simone Sidoli, Ana Maria Cuervo, Evripidis Gavathiotis
Format: Article
Language:English
Published: Springer Nature 2025-06-01
Series:EMBO Molecular Medicine
Subjects:
Online Access:https://doi.org/10.1038/s44321-025-00254-y
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849235046632783872
author Mericka McCabe
Rajanya Bhattacharyya
Rebecca Sereda
Olaya Santiago-Fernández
Rabia R Khawaja
Antonio Diaz
Kristen Lindenau
Deniz Gulfem Ozturk
Thomas P Garner
Simone Sidoli
Ana Maria Cuervo
Evripidis Gavathiotis
author_facet Mericka McCabe
Rajanya Bhattacharyya
Rebecca Sereda
Olaya Santiago-Fernández
Rabia R Khawaja
Antonio Diaz
Kristen Lindenau
Deniz Gulfem Ozturk
Thomas P Garner
Simone Sidoli
Ana Maria Cuervo
Evripidis Gavathiotis
author_sort Mericka McCabe
collection DOAJ
description Abstract Chaperone-mediated autophagy (CMA), a type of selective degradation of cytosolic proteins in lysosomes, is commonly upregulated in cancer cells, contributing to their survival and growth. The lack of a specific target for CMA inhibition has limited CMA blockage to genetic manipulations or global lysosomal function inhibition. Here, using genetic modulation, transcriptional analysis, and functional studies, we demonstrate a regulatory role for the interaction of the retinoic acid receptor alpha (RARα) and its corepressor, the nuclear receptor corepressor 1 (NCoR1), on CMA in non-small cell lung cancer (NSCLC). By targeting the disruption of the NCoR1/RARα complex with a structure-based screening strategy, we identified compound CIM7, a potent and selective CMA inhibitor that has no effect on macroautophagy. CIM7 preferentially inhibits CMA in NSCLC cells over normal cells, reduces tumor growth in NSCLC cells, and demonstrates efficacy in an in vivo xenograft mouse model with no observed toxicity in blood or major tissues. These findings reveal a druggable mechanism for selective CMA inhibition and a first-in-class CMA inhibitor as a potential therapeutic strategy for NSCLC.
format Article
id doaj-art-0a7e4bc06a6044e685f9b2d73a401ea5
institution Kabale University
issn 1757-4684
language English
publishDate 2025-06-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-0a7e4bc06a6044e685f9b2d73a401ea52025-08-20T04:02:55ZengSpringer NatureEMBO Molecular Medicine1757-46842025-06-011771716175510.1038/s44321-025-00254-ySmall molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancerMericka McCabe0Rajanya Bhattacharyya1Rebecca Sereda2Olaya Santiago-Fernández3Rabia R Khawaja4Antonio Diaz5Kristen Lindenau6Deniz Gulfem Ozturk7Thomas P Garner8Simone Sidoli9Ana Maria Cuervo10Evripidis Gavathiotis11Department of Biochemistry, Albert Einstein College of MedicineDepartment of Biochemistry, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Biochemistry, Albert Einstein College of MedicineDepartment of Biochemistry, Albert Einstein College of MedicineDepartment of Biochemistry, Albert Einstein College of MedicineDepartment of Developmental and Molecular Biology, Albert Einstein College of MedicineDepartment of Biochemistry, Albert Einstein College of MedicineAbstract Chaperone-mediated autophagy (CMA), a type of selective degradation of cytosolic proteins in lysosomes, is commonly upregulated in cancer cells, contributing to their survival and growth. The lack of a specific target for CMA inhibition has limited CMA blockage to genetic manipulations or global lysosomal function inhibition. Here, using genetic modulation, transcriptional analysis, and functional studies, we demonstrate a regulatory role for the interaction of the retinoic acid receptor alpha (RARα) and its corepressor, the nuclear receptor corepressor 1 (NCoR1), on CMA in non-small cell lung cancer (NSCLC). By targeting the disruption of the NCoR1/RARα complex with a structure-based screening strategy, we identified compound CIM7, a potent and selective CMA inhibitor that has no effect on macroautophagy. CIM7 preferentially inhibits CMA in NSCLC cells over normal cells, reduces tumor growth in NSCLC cells, and demonstrates efficacy in an in vivo xenograft mouse model with no observed toxicity in blood or major tissues. These findings reveal a druggable mechanism for selective CMA inhibition and a first-in-class CMA inhibitor as a potential therapeutic strategy for NSCLC.https://doi.org/10.1038/s44321-025-00254-yAutophagyCMA InhibitorNCoR1Non-small Cell Lung CancerRARα
spellingShingle Mericka McCabe
Rajanya Bhattacharyya
Rebecca Sereda
Olaya Santiago-Fernández
Rabia R Khawaja
Antonio Diaz
Kristen Lindenau
Deniz Gulfem Ozturk
Thomas P Garner
Simone Sidoli
Ana Maria Cuervo
Evripidis Gavathiotis
Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
EMBO Molecular Medicine
Autophagy
CMA Inhibitor
NCoR1
Non-small Cell Lung Cancer
RARα
title Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
title_full Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
title_fullStr Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
title_full_unstemmed Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
title_short Small molecule disruption of RARα/NCoR1 interaction inhibits chaperone-mediated autophagy in cancer
title_sort small molecule disruption of rarα ncor1 interaction inhibits chaperone mediated autophagy in cancer
topic Autophagy
CMA Inhibitor
NCoR1
Non-small Cell Lung Cancer
RARα
url https://doi.org/10.1038/s44321-025-00254-y
work_keys_str_mv AT merickamccabe smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT rajanyabhattacharyya smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT rebeccasereda smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT olayasantiagofernandez smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT rabiarkhawaja smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT antoniodiaz smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT kristenlindenau smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT denizgulfemozturk smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT thomaspgarner smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT simonesidoli smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT anamariacuervo smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer
AT evripidisgavathiotis smallmoleculedisruptionofrarancor1interactioninhibitschaperonemediatedautophagyincancer