Long-term, genome-wide kinetic analysis of the effect of the circadian clock and transcription on the repair of cisplatin-DNA adducts in the mouse liver.

Publisher: Elsevier Inc. on behalf of American Society for Biochemistry and Molecular Biology Country of Publication: United States NLM ID: 2985121R Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1083-351X (Electronic) Linking ISSN: 00219258 NLM ISO Abbreviation: J Biol Chem Subsets: MEDLINE

Publication: 2021- : [New York, NY] : Elsevier Inc. on behalf of American Society for Biochemistry and Molecular Biology
Original Publication: Baltimore, MD : American Society for Biochemistry and Molecular Biology

DNA Repair*; Circadian Clocks/*physiology ; Cisplatin/*metabolism ; DNA Adducts/*metabolism ; Liver/*metabolism; Animals ; Cisplatin/analysis ; Cisplatin/pharmacology ; DNA Adducts/analysis ; DNA Damage/drug effects ; Female ; Kinetics ; Mice ; Mice, Inbred C57BL ; Sequence Analysis, DNA/methods ; Time Factors

Cisplatin is the most commonly used chemotherapeutic drug for managing solid tumors. However, toxicity and the innate or acquired resistance of cancer cells to the drug limit its usefulness. Cisplatin kills cells by forming cisplatin-DNA adducts, most commonly the Pt-d(GpG) diadduct. We recently showed that, in mice, repair of this adduct 2 h following injection is controlled by two circadian programs. 1) The circadian clock controls transcription of 2000 genes in liver and, via transcription-directed repair, controls repair of the transcribed strand (TS) of these genes in a rhythmic fashion unique to each gene's phase of transcription. 2) The excision repair activity itself is controlled by the circadian clock with a single phase at which the repair of the nontranscribed strand (NTS) and the rest of the genome takes place. Here, we followed the repair kinetic for long periods genome-wide both globally and at single nucleotide resolution by the Excision Repair-sequencing (XR-seq) method to better understand cisplatin DNA damage and repair. We find that transcription-driven repair is nearly complete after 2 days, whereas weeks are required for repair of the NTS and the rest of the genome. TS repair oscillates in rhythmically expressed genes up to 2 days post injection, and in all expressed genes, we see a trend in TS repair with time from the 5' to 3' end. These findings help to understand the circadian- and transcription-dependent and -independent control of repair in response to cisplatin, and should aid in designing cisplatin chemotherapy regimens with improved therapeutic indexes.
(© 2019 Yang et al.)

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P30 ES010126 United States ES NIEHS NIH HHS; R01 ES027255 United States ES NIEHS NIH HHS; R35 GM118102 United States GM NIGMS NIH HHS

Keywords: DNA adduct; DNA damage; DNA repair; chemotherapy; chronotherapy; circadian clock; cisplatin; excision repair sequencing (XR-seq); kinetics; nucleotide excision repair; transcription-coupled repair

0 (DNA Adducts)
0 (cisplatin-DNA adduct)
Q20Q21Q62J (Cisplatin)

Date Created: 20190621 Date Completed: 20200316 Latest Revision: 20210317

20221213

PMC6690688

10.1074/jbc.RA119.009579

31217280