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Targeting DDX11 promotes PARP inhibitor sensitivity in hepatocellular carcinoma by attenuating BRCA2-RAD51 mediated homologous recombination – Oncogene

  • Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.

    Article 
    PubMed 

    Google Scholar
     

  • Ronot M, Bouattour M, Wassermann J, Bruno O, Dreyer C, Larroque B, et al. Alternative response criteria (Choi, European association for the study of the liver, and modified Response Evaluation Criteria in Solid Tumors [RECIST]) Versus RECIST 1.1 in patients with advanced hepatocellular carcinoma treated with sorafenib. Oncologist. 2014;19:394–402.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer. 2006;6:674–87.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7–30.

    Article 
    PubMed 

    Google Scholar
     

  • Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913–7.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006;7:517–28.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem. 2008;77:229–57.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sasaki M, Lange J, Keeney S. Genome destabilization by homologous recombination in the germ line. Nat Rev Mol Cell Biol. 2010;11:182–95.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • De Soto JA, Deng C-X. PARP-1 inhibitors: are they the long-sought genetically specific drugs for BRCA1/2-associated breast cancers? Int J Med Sci. 2006;3:117–23.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Murai J, Huang SN, Das BB, Renaud A, Zhang Y, Doroshow JH, et al. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res. 2012;72:5588–99.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009;361:123–34.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gerring SL, Spencer F, Hieter P. The CHL 1 (CTF 1) gene product of Saccharomyces cerevisiae is important for chromosome transmission and normal cell cycle progression in G2/M. EMBO J. 1990;9:4347–58.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Spencer F, Gerring SL, Connelly C, Hieter P. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics. 1990;124:237–49.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van der Lelij P, Chrzanowska KH, Godthelp BC, Rooimans MA, Oostra AB, Stumm M, et al. Warsaw breakage syndrome, a cohesinopathy associated with mutations in the XPD helicase family member DDX11/ChlR1. Am J Hum Genet. 2010;86:262–6.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • van Schie JJM, Faramarz A, Balk JA, Stewart GS, Cantelli E, Oostra AB, et al. Warsaw Breakage Syndrome associated DDX11 helicase resolves G-quadruplex structures to support sister chromatid cohesion. Nat Commun. 2020;11:4287.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jegadesan NK, Branzei D. DDX11 loss causes replication stress and pharmacologically exploitable DNA repair defects. Proc Natl Acad Sci USA. 2021;118:e2024258118.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bhattacharya C, Wang X, Becker D. The DEAD/DEAH box helicase, DDX11, is essential for the survival of advanced melanomas. Mol Cancer. 2012;11:82.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sui Y, Liu J, Zhang J, Zheng Z, Wang Z, Jia Z, et al. Expression and gene regulation network of adenosine receptor A2B in Lung Adenocarcinoma: a potential diagnostic and prognostic biomarker. Front Mol Biosci. 2021;8:663011.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Calì F, Bharti SK, Di Perna R, Brosh RM, Pisani FM. Tim/Timeless, a member of the replication fork protection complex, operates with the Warsaw breakage syndrome DNA helicase DDX11 in the same fork recovery pathway. Nucleic Acids Res. 2016;44:705–17.

    Article 
    PubMed 

    Google Scholar
     

  • Cortone G, Zheng G, Pensieri P, Chiappetta V, Tatè R, Malacaria E, et al. Interaction of the Warsaw breakage syndrome DNA helicase DDX11 with the replication fork-protection factor Timeless promotes sister chromatid cohesion. PLoS Genet. 2018;14:e1007622.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lerner LK, Holzer S, Kilkenny ML, Šviković S, Murat P, Schiavone D, et al. Timeless couples G-quadruplex detection with processing by DDX11 helicase during DNA replication. EMBO J. 2020;39:e104185.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Abe T, Ooka M, Kawasumi R, Miyata K, Takata M, Hirota K, et al. Warsaw breakage syndrome DDX11 helicase acts jointly with RAD17 in the repair of bulky lesions and replication through abasic sites. Proc Natl Acad Sci USA. 2018;115:8412–7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stoepker C, Faramarz A, Rooimans MA, van Mil SE, Balk JA, Velleuer E, et al. DNA helicases FANCM and DDX11 are determinants of PARP inhibitor sensitivity. DNA Repair. 2015;26:54–64.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Inoue A, Li T, Roby SK, Valentine MB, Inoue M, Boyd K, et al. Loss of ChlR1 helicase in mouse causes lethality due to the accumulation of aneuploid cells generated by cohesion defects and placental malformation. Cell Cycle. 2007;6:1646–54.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rossi F, Helbling-Leclerc A, Kawasumi R, Jegadesan NK, Xu X, Devulder P, et al. SMC5/6 acts jointly with Fanconi anemia factors to support DNA repair and genome stability. EMBO Rep. 2020;21:e48222.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Olivieri M, Cho T, Álvarez-Quilón A, Li K, Schellenberg MJ, Zimmermann M, et al. A Genetic Map of the Response to DNA Damage in Human Cells. Cell. 2020;182:481–96.e21.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gunn A, Stark JM. I-SceI-based assays to examine distinct repair outcomes of mammalian chromosomal double strand breaks. Methods Mol Biol. 2012;920:379–91.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Luo K, Li L, Li Y, Wu C, Yin Y, Chen Y, et al. A phosphorylation-deubiquitination cascade regulates the BRCA2-RAD51 axis in homologous recombination. Genes Dev. 2016;30:2581–95.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khanna KK, Lavin MF, Jackson SP, Mulhern TD. ATM, a central controller of cellular responses to DNA damage. Cell Death Differ. 2001;8:1052–65.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kastan MB, Lim DS. The many substrates and functions of ATM. Nat Rev Mol Cell Biol. 2000;1:179–86.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang C, Tang H, Geng A, Dai B, Zhang H, Sun X, et al. Rational combination therapy for hepatocellular carcinoma with PARP1 and DNA-PK inhibitors. Proc Natl Acad Sci USA. 2020;117:26356–65.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li J, Liu L, Liu X, Xu P, Hu Q, Yu Y. The role of upregulated DDX11 as a potential prognostic and diagnostic biomarker in lung adenocarcinoma. J Cancer. 2019;10:4208–16.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hirota Y, Lahti JM. Characterization of the enzymatic activity of hChlR1, a novel human DNA helicase. Nucleic Acids Res. 2000;28:917–24.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Motegi A, Masutani M, Yoshioka K-I, Bessho T. Aberrations in DNA repair pathways in cancer and therapeutic significances. Semin Cancer Biol. 2019;58:29–46.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Brown JS, O’Carrigan B, Jackson SP, Yap TA. Targeting DNA repair in cancer: beyond PARP Inhibitors. Cancer Discov. 2017;7:20–37.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Haeussler M, Schönig K, Eckert H, Eschstruth A, Mianné J, Renaud J-B, et al. Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 2016;17:148.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guo J, Duan L, He X, Li S, Wu Y, Xiang G, et al. A combined model of human iPSC-derived liver organoids and hepatocytes reveals ferroptosis in DGUOK mutant mtDNA depletion syndrome. Adv Sci. 2021;8:2004680.

    Article 
    CAS 

    Google Scholar
     

  • Zhou Y, Caron P, Legube G, Paull TT. Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res. 2014;42:e19.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang S, Cao K, Liao Y, Zhang W, Zheng J, Li X, et al. CDCA2 protects against oxidative stress by promoting BRCA1-NRF2 signaling in hepatocellular carcinoma. Oncogene. 2021;40:4368–83.

    Article 
    CAS 
    PubMed 

    Google Scholar