Small molecule targeting of transcription-replication conflict for selective chemotherapy

Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer therapeutic implications. Proliferating cell nuclear antigen (PCNA) is critical to DNA replication and repair processes. Through a rational d...

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Published inCell chemical biology Vol. 30; no. 10; pp. 1235 - 1247.e6
Main Authors Gu, Long, Li, Min, Li, Caroline M., Haratipour, Pouya, Lingeman, Robert, Jossart, Jennifer, Gutova, Margarita, Flores, Linda, Hyde, Caitlyn, Kenjić, Nikola, Li, Haiqing, Chung, Vincent, Li, Hongzhi, Lomenick, Brett, Von Hoff, Daniel D., Synold, Timothy W., Aboody, Karen S., Liu, Yilun, Horne, David, Hickey, Robert J., Perry, J. Jefferson P., Malkas, Linda H.
Format Journal Article
LanguageEnglish
Published United States Elsevier Ltd 19.10.2023
Subjects
DNA repair
DNA replication stress
PCNA
transcription-replication conflict
transcription-replication conflict
PCNA
DNA repair
DNA replication stress
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Abstract Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer therapeutic implications. Proliferating cell nuclear antigen (PCNA) is critical to DNA replication and repair processes. Through a rational drug design approach, we identified a small molecule PCNA inhibitor, AOH1996, which selectively kills cancer cells. AOH1996 enhances the interaction between PCNA and the largest subunit of RNA polymerase II, RPB1, and dissociates PCNA from actively transcribed chromatin regions, while inducing DNA double-stranded breaks in a transcription-dependent manner. Attenuation of RPB1 interaction with PCNA, by a point mutation in RPB1’s PCNA-binding region, confers resistance to AOH1996. Orally administrable and metabolically stable, AOH1996 suppresses tumor growth as a monotherapy or as a combination treatment but causes no discernable side effects. Inhibitors of transcription replication conflict resolution may provide a new and unique therapeutic avenue for exploiting this cancer-selective vulnerability. [Display omitted] •Crystallography-directed medicinal chemistry identifies a PCNA ligand (AOH1996)•AOH1996 enhances PCNA and RPB1 interaction and interferes with TRC resolution•AOH1996 induces DNA double-stranded breaks in a transcription dependent manner•Given orally, AOH1996 suppresses tumor growth but causes no discernable side effect Gu et al. used crystallography-directed medicinal chemistry to identify a small molecule ligand of PCNA that interferes with the resolution of transcription-replication conflicts. This compound was found to be orally active and inhibited tumor growth in animals without causing any discernable toxicity even at 6 times its effective dose.
AbstractList Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer therapeutic implications. Proliferating cell nuclear antigen (PCNA) is critical to DNA replication and repair processes. Through a rational drug design approach, we identified a small molecule PCNA inhibitor, AOH1996, which selectively kills cancer cells. AOH1996 enhances the interaction between PCNA and the largest subunit of RNA polymerase II, RPB1, and dissociates PCNA from actively transcribed chromatin regions, while inducing DNA double-stranded breaks in a transcription-dependent manner. Attenuation of RPB1 interaction with PCNA, by a point mutation in RPB1's PCNA-binding region, confers resistance to AOH1996. Orally administrable and metabolically stable, AOH1996 suppresses tumor growth as a monotherapy or as a combination treatment but causes no discernable side effects. Inhibitors of transcription replication conflict resolution may provide a new and unique therapeutic avenue for exploiting this cancer-selective vulnerability.
Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer therapeutic implications. Proliferating cell nuclear antigen (PCNA) is critical to DNA replication and repair processes. Through a rational drug design approach, we identified a small molecule PCNA inhibitor, AOH1996, which selectively kills cancer cells. AOH1996 enhances the interaction between PCNA and the largest subunit of RNA polymerase II, RPB1, and dissociates PCNA from actively transcribed chromatin regions, while inducing DNA double-stranded breaks in a transcription-dependent manner. Attenuation of RPB1 interaction with PCNA, by a point mutation in RPB1’s PCNA-binding region, confers resistance to AOH1996. Orally administrable and metabolically stable, AOH1996 suppresses tumor growth as a monotherapy or as a combination treatment but causes no discernable side effects. Inhibitors of transcription replication conflict resolution may provide a new and unique therapeutic avenue for exploiting this cancer-selective vulnerability. Gu et al. used crystallography-directed medicinal chemistry to identify a small molecule ligand of PCNA that interferes with the resolution of transcription-replication conflicts. This compound was found to be orally active and inhibited tumor growth in animals without causing any discernable toxicity even at 6 times its effective dose.
Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer therapeutic implications. Proliferating cell nuclear antigen (PCNA) is critical to DNA replication and repair processes. Through a rational drug design approach, we identified a small molecule PCNA inhibitor, AOH1996, which selectively kills cancer cells. AOH1996 enhances the interaction between PCNA and the largest subunit of RNA polymerase II, RPB1, and dissociates PCNA from actively transcribed chromatin regions, while inducing DNA double-stranded breaks in a transcription-dependent manner. Attenuation of RPB1 interaction with PCNA, by a point mutation in RPB1’s PCNA-binding region, confers resistance to AOH1996. Orally administrable and metabolically stable, AOH1996 suppresses tumor growth as a monotherapy or as a combination treatment but causes no discernable side effects. Inhibitors of transcription replication conflict resolution may provide a new and unique therapeutic avenue for exploiting this cancer-selective vulnerability. [Display omitted] •Crystallography-directed medicinal chemistry identifies a PCNA ligand (AOH1996)•AOH1996 enhances PCNA and RPB1 interaction and interferes with TRC resolution•AOH1996 induces DNA double-stranded breaks in a transcription dependent manner•Given orally, AOH1996 suppresses tumor growth but causes no discernable side effect Gu et al. used crystallography-directed medicinal chemistry to identify a small molecule ligand of PCNA that interferes with the resolution of transcription-replication conflicts. This compound was found to be orally active and inhibited tumor growth in animals without causing any discernable toxicity even at 6 times its effective dose.
Author Li, Haiqing
Hickey, Robert J.
Li, Min
Liu, Yilun
Li, Caroline M.
Lomenick, Brett
Malkas, Linda H.
Aboody, Karen S.
Jossart, Jennifer
Von Hoff, Daniel D.
Haratipour, Pouya
Horne, David
Kenjić, Nikola
Lingeman, Robert
Chung, Vincent
Gu, Long
Gutova, Margarita
Synold, Timothy W.
Perry, J. Jefferson P.
Flores, Linda
Hyde, Caitlyn
Li, Hongzhi
AuthorAffiliation 7 Department of Medical Oncology, City of Hope, Duarte, CA, USA
8 Department of Bioinformatics, Beckman Research Institute of City of Hope, Duarte, CA, USA
11 Department of Medical Oncology and Therapeutics Research, Beckman Research Institute of City of Hope, Duarte, CA, USA
2 Department of Cancer Genetics and Epigenetics, Beckman Research Institute of City of Hope, Duarte, CA, USA
3 Department of Cancer Biology & Molecular Medicine, Beckman Research Institute of City of Hope, Duarte, CA, USA
6 Department of Genomics, Beckman Research Institute of City of Hope, Duarte, CA, USA
1 Department of Molecular Diagnostics & Experimental Therapeutics, Beckman Research Institute of City of Hope, Duarte, CA, USA
5 Department of Biochemistry, University of California Riverside, Riverside, CA, USA
10 Clinical Translational Research Division, Translational Genomics Research Institute, 445N 5th Street, Phoenix, AZ 85004, USA
4 Department of Developmental & Stem Cell Biology, Beckman Research Institute of Cit
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Issue 10
Keywords transcription-replication conflict
PCNA
DNA repair
DNA replication stress
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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Notes AUTHOR CONTRIBUTIONS
L.H.M., R.J.H., Y.L., V.C., D.V.H., K.S.A., J.J.P.P., and L.G. conceptualized the idea and supervised the project; L.G., M.L., R.L., J.J., and C.M.L. designed and performed most experiments; T.W.S. designed and supervised the pharmacokinetics studies; D.H and P.H. were responsible for the design and synthesis of the analog compounds; M.G., L.F., and C.H. performed the in vivo combination therapy study; J.J. primarily performed the crystallography studies with support from N.K.; H.L. performed the computer modeling analysis; B.L. performed the proteomic study; H.L. analyzed the proteomic data; L.G. and J.J.P.P. wrote the manuscript.
ORCID 0000-0002-3536-5056
OpenAccessLink https://www.sciencedirect.com/science/article/pii/S2451945623002210
PMID 37531956
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PublicationTitle Cell chemical biology
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Snippet Targeting transcription replication conflicts, a major source of endogenous DNA double-stranded breaks and genomic instability could have important anticancer...
SourceID pubmedcentral
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pubmed
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SourceType Open Access Repository
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Publisher
StartPage 1235
SubjectTerms DNA repair
DNA replication stress
PCNA
transcription-replication conflict
Title Small molecule targeting of transcription-replication conflict for selective chemotherapy
URI https://dx.doi.org/10.1016/j.chembiol.2023.07.001
https://www.ncbi.nlm.nih.gov/pubmed/37531956
https://pubmed.ncbi.nlm.nih.gov/PMC10592352
Volume 30
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