5,199
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Inhibitors of Jumonji C domain-containing histone lysine demethylases overcome cisplatin and paclitaxel resistance in non-small cell lung cancer through APC/Cdh1-dependent degradation of CtIP and PAF15

, , &
Pages 65-75 | Received 05 Jul 2021, Accepted 05 Dec 2021, Published online: 31 Jan 2022

References

  • Bayo J, Tran TA, Wang L, Pena-Llopis S, Das AK, Martinez ED. Jumonji inhibitors overcome radioresistance in cancer through changes in H3K4 methylation at double-strand breaks. Cell Rep. 2018;25(4):1040–50 e5. doi:10.1016/j.celrep.2018.09.081.
  • D’Oto A, Tian QW, Davidoff AM, Yang J. Histone demethylases and their roles in cancer epigenetics. J of Med Oncol and Ther. 2016;1(2):34–40.
  • Franci G, Ciotta A, Altucci L. The Jumonji family: past, present and future of histone demethylases in cancer. Biomol Concepts. 2014;5(3):209–224. doi:10.1515/bmc-2014-0010.
  • Khoury-Haddad H, Nadar-Ponniah PT, Awwad S, Ayoub N. The emerging role of lysine demethylases in DNA damage response: dissecting the recruitment mode of KDM4D/JMJD2D to DNA damage sites. Cell Cycle. 2015;14(7):950–958. doi:10.1080/15384101.2015.1014147.
  • Park SY, Park JW, Chun YS. Jumonji histone demethylases as emerging therapeutic targets. Pharmacol Res. 2016;105:146–151. doi:10.1016/j.phrs.2016.01.026.
  • Hojfeldt JW, Agger K, Helin K. Histone lysine demethylases as targets for anticancer therapy. Nat Rev Drug Discov. 2013;12(12):917–930. doi:10.1038/nrd4154.
  • Rotili D, Mai A. Targeting histone demethylases: a new avenue for the fight against cancer. Genes Cancer. 2011;2(6):663–679. doi:10.1177/1947601911417976.
  • Dalvi MP, Wang L, Zhong R, Kollipara RK, Park H, Bayo J, Yenerall P, Zhou Y, Timmons BC, Rodriguez-Canales J, et al. Taxane-platin-resistant lung cancers co-develop hypersensitivity to Jumonjic demethylase inhibitors. Cell Rep. 2017;19(8):1669–1684. doi:10.1016/j.celrep.2017.04.077.
  • Kuo KT, Huang WC, Bamodu OA, Lee WH, Wang CH, Hsiao M, Wang LS, Yeh CT. Histone demethylase JARID1B/KDM5B promotes aggressiveness of non-small cell lung cancer and serves as a good prognostic predictor. Clin Epigenet. 2018;10(1):107. doi:10.1186/s13148-018-0533-9.
  • Li S, Jiang L, He Q, Wei W, Wang Y, Zhang X, Liu J, Chen K, Chen J, Xie D. The prognostic significance of JMJD3 in primary sarcomatoid carcinoma of the lung, a rare subtype of lung cancer. Onco Targets Ther. 2019;12:9385–9393. doi:10.2147/OTT.S225596.
  • Toyokawa G, Taguchi K, Edagawa M, Shimamatsu S, Toyozawa R, Nosaki K, Hirai F, Yamaguchi M, Shimokawa M, Seto T, et al. The prognostic impact of Jumonji domain-containing 2B in patients with resected lung adenocarcinoma. Anticancer Res. 2016;36(9):4841–4846. doi:10.21873/anticanres.11046.
  • Duan L, Perez RE, Chastain PD 2nd, Mathew MT, Bijukumar DR, Maki CG. JMJD2 promotes acquired cisplatin resistance in non-small cell lung carcinoma cells. Oncogene. 2019;38(28):5643–5657. doi:10.1038/s41388-019-0814-6.
  • Hou J, Wu J, Dombkowski A, Zhang K, Holowatyj A, Boerner JL, Yang ZQ. Genomic amplification and a role in drug-resistance for the KDM5A histone demethylase in breast cancer. Am J Transl Res. 2012;4(3):247–256.
  • Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell. 2010;141(1):69–80. doi:10.1016/j.cell.2010.02.027.
  • Vinogradova M, Gehling VS, Gustafson A, Arora S, Tindell CA, Wilson C, Williamson KE, Guler GD, Gangurde P, Manieri W, et al. An inhibitor of KDM5 demethylases reduces survival of drug-tolerant cancer cells. Nat Chem Biol. 2016;12(7):531–538. doi:10.1038/nchembio.2085.
  • He C, Sun J, Liu C, Jiang Y, Hao Y. Elevated H3K27me3 levels sensitize osteosarcoma to cisplatin. Clin Epigenet. 2019;11(1):8. doi:10.1186/s13148-018-0605-x.
  • Zhang B, Long Q, Wu S, Xu Q, Song S, Han L, Qian M, Ren X, Liu H, Jiang J, et al. KDM4 orchestrates epigenomic remodeling of senescent cells and potentiates the senescence-associated secretory phenotype. Nat Aging. 2021;1(5):454–472. doi:10.1038/s43587-021-00063-1.
  • Wang L, Chang J, Varghese D, Dellinger M, Kumar S, Best AM, Ruiz J, Bruick R, Pena-Llopis S, Xu J, et al. A small molecule modulates Jumonji histone demethylase activity and selectively inhibits cancer growth. Nat Commun. 2013;4(1):2035. doi:10.1038/ncomms3035.
  • Burgess JT, Rose M, Boucher D, Plowman J, Molloy C, Fisher M, O’Leary C, Richard DJ, O’Byrne KJ, Bolderson E. The therapeutic potential of DNA damage repair pathways and genomic stability in lung cancer. Front Oncol. 2020;10:1256. doi:10.3389/fonc.2020.01256.
  • Chen P, Li J, Chen YC, Qian H, Chen YJ, Su JY, Wu M, Lan T. The functional status of DNA repair pathways determines the sensitization effect to cisplatin in non-small cell lung cancer cells. Cellular Oncol. 2016;39(6):511–522. doi:10.1007/s13402-016-0291-7.
  • Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31(15):1869–1883. doi:10.1038/onc.2011.384.
  • Canovas B, Igea A, Sartori AA, Gomis RR, Paull TT, Isoda M, Perez-Montoyo H, Serra V, Gonzalez-Suarez E, Stracker TH, et al. Targeting p38alpha increases DNA damage, chromosome instability, and the anti-tumoral response to taxanes in breast cancer cells. Cancer Cell. 2018;33(6):1094–110 e8. doi:10.1016/j.ccell.2018.04.010.
  • Emanuele MJ, Ciccia A, Elia AE, Elledge SJ. Proliferating cell nuclear antigen (PCNA)-associated KIAA0101/PAF15 protein is a cell cycle-regulated anaphase-promoting complex/cyclosome substrate. Proceedings of the National Academy of Sciences of the United States of America; 2011; 108:9845–9850.
  • Lafranchi L, de Boer HR, de Vries EG, Ong SE, Sartori AA, van Vugt MA. APC/C(Cdh1) controls CtIP stability during the cell cycle and in response to DNA damage. EMBO J. 2014;33(23):2860–2879. doi:10.15252/embj.201489017.
  • Pfleger CM, Lee E, Kirschner MW. Substrate recognition by the Cdc20 and Cdh1 components of the anaphase-promoting complex. Genes Dev. 2001;15(18):2396–2407. doi:10.1101/gad.918201.
  • Price PM, Yu F, Kaldis P, Aleem E, Nowak G, Safirstein RL, Megyesi J. Dependence of cisplatin-induced cell death in vitro and in vivo on cyclin-dependent kinase 2. J of the Am Soc of Nephrol: JASN. 2006;17(9):2434–2442. doi:10.1681/ASN.2006020162.
  • Lukas C, Sorensen CS, Kramer E, Santoni-Rugiu E, Lindeneg C, Peters JM, Bartek J, Lukas J. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex. Nature. 1999;401(6755):815–818. doi:10.1038/44611.
  • Oakes V, Wang W, Harrington B, Lee WJ, Beamish H, Chia KM, Pinder A, Goto H, Inagaki M, Pavey S, et al. Cyclin A/Cdk2 regulates Cdh1 and claspin during late S/G2 phase of the cell cycle. Cell Cycle. 2014;13(20):3302–3311. doi:10.4161/15384101.2014.949111.
  • Sorensen CS, Lukas C, Kramer ER, Peters JM, Bartek J, Lukas J. A conserved cyclin-binding domain determines functional interplay between anaphase-promoting complex-Cdh1 and cyclin A-Cdk2 during cell cycle progression. Mol Cell Biol. 2001;21(11):3692–3703. doi:10.1128/MCB.21.11.3692-3703.2001.
  • Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. Human CtIP promotes DNA end resection. Nature. 2007;450(7169):509–514. doi:10.1038/nature06337.
  • Povlsen LK, Beli P, Wagner SA, Poulsen SL, Sylvestersen KB, Poulsen JW, Nielsen ML, Bekker-Jensen S, Mailand N, Choudhary C. Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nat Cell Biol. 2012;14(10):1089–1098. doi:10.1038/ncb2579.