Dihydropyrimidinase protects from DNA replication stress caused by cytotoxic metabolites

Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihydropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corr...

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Published inNucleic acids research Vol. 48; no. 4; pp. 1886 - 1904
Main Authors Basbous, Jihane, Aze, Antoine, Chaloin, Laurent, Lebdy, Rana, Hodroj, Dana, Ribeyre, Cyril, Larroque, Marion, Shepard, Caitlin, Kim, Baek, Pruvost, Alain, Moreaux, Jérôme, Maiorano, Domenico, Mechali, Marcel, Constantinou, Angelos
Format Journal Article
LanguageEnglish
Published England Oxford University Press 28.02.2020
Subjects
Amidohydrolases - genetics
Animals
Antineoplastic Agents - therapeutic use
Biochemistry, Molecular Biology
Cell Transformation, Neoplastic - genetics
DNA Replication - genetics
Genome Integrity, Repair and
Humans
Life Sciences
Neoplasms - drug therapy
Neoplasms - genetics
Transcription, Genetic
Uracil - analogs & derivatives
Uracil - metabolism
Xenopus laevis - genetics
Xenopus laevis - growth & development
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Abstract Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihydropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corresponding normal tissues. How dihydropyrimidine metabolites affect cellular phenotypes remains elusive. Here we show that the accumulation of dihydropyrimidines induces the formation of DNA-protein crosslinks (DPCs) and causes DNA replication and transcriptional stress. We used Xenopus egg extracts to recapitulate DNA replication invitro. We found that dihydropyrimidines interfere directly with the replication of both plasmid and chromosomal DNA. Furthermore, we show that the plant flavonoid dihydromyricetin inhibits human DHP activity. Cellular exposure to dihydromyricetin triggered DPCs-dependent DNA replication stress in cancer cells. This study defines dihydropyrimidines as potentially cytotoxic metabolites that may offer an opportunity for therapeutic-targeting of DHP activity in solid tumors.
AbstractList Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihydropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corresponding normal tissues. How dihydropyrimidine metabolites affect cellular phenotypes remains elusive. Here we show that the accumulation of dihydropyrimidines induces the formation of DNA-protein crosslinks (DPCs) and causes DNA replication and transcriptional stress. We used Xenopus egg extracts to recapitulate DNA replication invitro. We found that dihydropyrimidines interfere directly with the replication of both plasmid and chromosomal DNA. Furthermore, we show that the plant flavonoid dihydromyricetin inhibits human DHP activity. Cellular exposure to dihydromyricetin triggered DPCs-dependent DNA replication stress in cancer cells. This study defines dihydropyrimidines as potentially cytotoxic metabolites that may offer an opportunity for therapeutic-targeting of DHP activity in solid tumors.
Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihydropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corresponding normal tissues. How dihydropyrimidine metabolites affect cellular phenotypes remains elusive. Here we show that the accumulation of dihydropyrimidines induces the formation of DNA–protein crosslinks (DPCs) and causes DNA replication and transcriptional stress. We used Xenopus egg extracts to recapitulate DNA replication in vitro . We found that dihydropyrimidines interfere directly with the replication of both plasmid and chromosomal DNA. Furthermore, we show that the plant flavonoid dihydromyricetin inhibits human DHP activity. Cellular exposure to dihydromyricetin triggered DPCs-dependent DNA replication stress in cancer cells. This study defines dihydropyrimidines as potentially cytotoxic metabolites that may offer an opportunity for therapeutic-targeting of DHP activity in solid tumors.
Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihy-dropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corresponding normal tissues. How dihydropyrimidine metabolites affect cellular phenotypes remains elusive. Here we show that the accumulation of di-hydropyrimidines induces the formation of DNA-protein crosslinks (DPCs) and causes DNA replication and transcriptional stress. We used Xenopus egg extracts to recapitulate DNA replication in vitro. We found that dihydropyrimidines interfere directly with the replication of both plasmid and chromo-somal DNA. Furthermore, we show that the plant flavonoid dihydromyricetin inhibits human DHP activity. Cellular exposure to dihydromyricetin triggered DPCs-dependent DNA replication stress in cancer cells. This study defines dihydropyrimidines as potentially cytotoxic metabolites that may offer an opportunity for therapeutic-targeting of DHP activity in solid tumors.
Abstract Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer progression. Dihydropyrimidines are degraded by dihydropyrimidinase (DHP), a zinc metalloenzyme that is upregulated in solid tumors but not in the corresponding normal tissues. How dihydropyrimidine metabolites affect cellular phenotypes remains elusive. Here we show that the accumulation of dihydropyrimidines induces the formation of DNA–protein crosslinks (DPCs) and causes DNA replication and transcriptional stress. We used Xenopus egg extracts to recapitulate DNA replication invitro. We found that dihydropyrimidines interfere directly with the replication of both plasmid and chromosomal DNA. Furthermore, we show that the plant flavonoid dihydromyricetin inhibits human DHP activity. Cellular exposure to dihydromyricetin triggered DPCs-dependent DNA replication stress in cancer cells. This study defines dihydropyrimidines as potentially cytotoxic metabolites that may offer an opportunity for therapeutic-targeting of DHP activity in solid tumors.
Author Larroque, Marion
Aze, Antoine
Lebdy, Rana
Shepard, Caitlin
Basbous, Jihane
Hodroj, Dana
Moreaux, Jérôme
Kim, Baek
Pruvost, Alain
Chaloin, Laurent
Constantinou, Angelos
Mechali, Marcel
Ribeyre, Cyril
Maiorano, Domenico
AuthorAffiliation 6 Service de Pharmacologie et Immunoanalyse (SPI), Plateforme SMArt-MS, CEA, INRA, Université Paris-Saclay , 91191 Gif-sur-Yvette Cedex, France
2 Institut de Recherche en Infectiologie de Montpellier, CNRS, Université de Montpellier , 34293 Montpellier Cedex 5, France
3 Cancer Research Center of Toulouse (CRCT) , 31037 Toulouse Cedex 1, France
5 School of Medicine, Emory University , Atlanta, GA 30322, USA
4 Institut du Cancer de Montpellier (ICM) ,34298 Montpellier Cedex 5, France
1 Institute of Human Genetics (IGH), CNRS, Université de Montpellier , 34396 Montpellier Cedex 5, France
AuthorAffiliation_xml – name: 2 Institut de Recherche en Infectiologie de Montpellier, CNRS, Université de Montpellier , 34293 Montpellier Cedex 5, France
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– name: 5 School of Medicine, Emory University , Atlanta, GA 30322, USA
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Snippet Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer...
Abstract Imbalance in the level of the pyrimidine degradation products dihydrouracil and dihydrothymine is associated with cellular transformation and cancer...
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SubjectTerms Amidohydrolases - genetics
Animals
Antineoplastic Agents - therapeutic use
Biochemistry, Molecular Biology
Cell Transformation, Neoplastic - genetics
DNA Replication - genetics
Genome Integrity, Repair and
Humans
Life Sciences
Neoplasms - drug therapy
Neoplasms - genetics
Transcription, Genetic
Uracil - analogs & derivatives
Uracil - metabolism
Xenopus laevis - genetics
Xenopus laevis - growth & development
Title Dihydropyrimidinase protects from DNA replication stress caused by cytotoxic metabolites
URI https://www.ncbi.nlm.nih.gov/pubmed/31853544
https://search.proquest.com/docview/2328755774
https://hal.science/hal-02556387
https://pubmed.ncbi.nlm.nih.gov/PMC7038975
Volume 48
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