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Electrophilic fatty acids impair RAD51 function and potentiate the effects of DNA-damaging agents on growth of triple-negative breast cells
Journal article   Open access   Peer reviewed

Electrophilic fatty acids impair RAD51 function and potentiate the effects of DNA-damaging agents on growth of triple-negative breast cells

Alparslan Asan, John J. Skoko, Chen-Shan Chen Woodcock, Bentley M. Wingert, Steven R. Woodcock, Daniel Normolle, Yi Huang, Jeremy M. Stark, Carlos J. Camacho, Bruce A. Freeman, …
The Journal of biological chemistry, Vol.294(2), pp.397-404
01/11/2019
DOI: 10.1074/jbc.AC118.005899
PMCID: PMC6333886
PMID: 30478172
url
https://doi.org/10.1074/jbc.AC118.005899View
Published (Version of record) Open Access

Abstract

Homologous recombination (HR)-directed DNA double-strand break (DSB) repair enables template-directed DNA repair to maintain genomic stability. RAD51 recombinase (RAD51) is a critical component of HR and facilitates DNA strand exchange in DSB repair. We report here that treating triple-negative breast cancer (TNBC) cells with the fatty acid nitroalkene 10-nitro-octadec-9-enoic acid (OA-NO2) in combination with the antineoplastic DNA-damaging agents doxorubicin, cisplatin, olaparib, and γ-irradiation (IR) enhances the antiproliferative effects of these agents. OA-NO2 inhibited IR-induced RAD51 foci formation and enhanced H2A histone family member X (H2AX) phosphorylation in TNBC cells. Analyses of fluorescent DSB reporter activity with both static-flow cytometry and kinetic live-cell studies enabling temporal resolution of recombination revealed that OA-NO2 inhibits HR and not nonhomologous end joining (NHEJ). OA-NO2 alkylated Cys-319 in RAD51, and this alkylation depended on the Michael acceptor properties of OA-NO2 because nonnitrated and saturated nonelectrophilic analogs of OA-NO2, octadecanoic acid and 10-nitro-octadecanoic acid, did not react with Cys-319. Of note, OA-NO2 alkylation of RAD51 inhibited its binding to ssDNA. RAD51 Cys-319 resides within the SH3-binding site of ABL proto-oncogene 1, nonreceptor tyrosine kinase (ABL1), so we investigated the effect of OA-NO2–mediated Cys-319 alkylation on ABL1 binding and found that OA-NO2 inhibits RAD51–ABL1 complex formation both in vitro and in cell-based immunoprecipitation assays. The inhibition of the RAD51–ABL1 complex also suppressed downstream RAD51 Tyr-315 phosphorylation. In conclusion, RAD51 Cys-319 is a functionally significant site for adduction of soft electrophiles such as OA-NO2 and suggests further investigation of lipid electrophile–based combinational therapies for TNBC.
breast cancer cysteine-mediated cross-linking DNA repair drug action drug discovery homologous recombination nitro fatty acid nitroalkene PARP1 Rad51 signal transduction triple negative breast cancer

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