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Research Article

Tabersonine enhances cisplatin sensitivity by modulating Aurora kinase A and suppressing epithelial–mesenchymal transition in triple-negative breast cancer

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Pages 394-403 | Received 07 Dec 2023, Accepted 28 Apr 2024, Published online: 13 May 2024

References

  • Ashrafizadeh M, Zarrabi A, Hushmandi K, Kalantari M, Mohammadinejad R, Javaheri T, Sethi G. 2020. Association of the epithelial-mesenchymal transition (EMT) with cisplatin resistance. Int J Mol Sci. 21(11):4002. doi: 10.3390/ijms21114002.
  • Bavetsias V, Large JM, Sun C, Bouloc N, Kosmopoulou M, Matteucci M, Wilsher NE, Martins V, Reynisson J, Atrash B, et al. 2010. Imidazo[4,5-b]pyridine derivatives as inhibitors of Aurora kinases: lead optimization studies toward the identification of an orally bioavailable preclinical development candidate. J Med Chem. 53(14):5213–5228. doi: 10.1021/jm100262j.
  • Bou Zerdan M, Ghorayeb T, Saliba F, Allam S, Bou Zerdan M, Yaghi M, Bilani N, Jaafar R, Nahleh Z. 2022. Triple negative breast cancer: updates on classification and treatment in 2021. Cancers (Basel). 14(5):1253. doi: 10.3390/cancers14051253.
  • Cánovas B, Igea A, Sartori AA, Gomis RR, Paull TT, Isoda M, Pérez-Montoyo H, Serra V, González-Suárez E, Stracker TH, et al. 2018. Targeting p38alpha increases DNA damage, chromosome instability, and the anti-tumoral response to taxanes in breast cancer cells. Cancer Cell. 33(6):1094–1110 e1098. doi: 10.1016/j.ccell.2018.04.010.
  • Chandrashekar DS, Karthikeyan SK, Korla PK, Patel H, Shovon AR, Athar M, Netto GJ, Qin ZS, Kumar S, Manne U, et al. 2022. UALCAN: an update to the integrated cancer data analysis platform. Neoplasia. 25:18–27. doi: 10.1016/j.neo.2022.01.001.
  • Chen C, Song G, Xiang J, Zhang H, Zhao S, Zhan Y. 2017. AURKA promotes cancer metastasis by regulating epithelial-mesenchymal transition and cancer stem cell properties in hepatocellular carcinoma. Biochem Biophys Res Commun. 486(2):514–520. doi: 10.1016/j.bbrc.2017.03.075.
  • Chen K, Xu J, Tong YL, Yan JF, Pan Y, Wang WJ, Zheng L, Zheng XX, Hu C, Hu X, et al. 2023. Rab31 promotes metastasis and cisplatin resistance in stomach adenocarcinoma through Twist1-mediated EMT. Cell Death Dis. 14(2):115. doi: 10.1038/s41419-023-05596-4.
  • Chen SH, Chang JY. 2019. New insights into mechanisms of cisplatin resistance: from tumor cell to microenvironment. Int J Mol Sci. 20(17):4136. doi: 10.3390/ijms20174136.
  • Chen X, Yan Y, Liu W, Liu Y, Thakur A, Liang Q, Xu Z. 2023. Targeting RAS guanyl releasing protein 1 promotes T lymphocytes infiltrations and improves anti-programmed death receptor ligand 1 therapy response of triple-negative breast cancer. Clin Transl Med. 13(7):e1335.
  • Chen Y, Lin W, Chen P, Ye B, Luo W, Wang X, Huang W, Wu G, Liang G. 2023. Tabersonine alleviates obesity-induced cardiomyopathy by binding to transforming growth factor activated kinase 1 (TAK1) and inhibiting TAK1-mediated inflammation. Phytother Res. 37(3):860–871. doi: 10.1002/ptr.7666.
  • Dawei H, Honggang D, Qian W. 2018. AURKA contributes to the progression of oral squamous cell carcinoma (OSCC) through modulating epithelial-to-mesenchymal transition (EMT) and apoptosis via the regulation of ROS. Biochem Biophys Res Commun. 507(1–4):83–90. doi: 10.1016/j.bbrc.2018.10.170.
  • Deepak KGK, Vempati R, Nagaraju GP, Dasari VR, S N, Rao DN, Malla RR. 2020. Tumor microenvironment: challenges and opportunities in targeting metastasis of triple negative breast cancer. Pharmacol Res. 153:104683. doi: 10.1016/j.phrs.2020.104683.
  • Du R, Huang C, Liu K, Li X, Dong Z. 2021. Targeting AURKA in cancer: molecular mechanisms and opportunities for cancer therapy. Mol Cancer. 20(1):15. doi: 10.1186/s12943-020-01305-3.
  • Fancelli D, Moll J, Varasi M, Bravo R, Artico R, Berta D, Bindi S, Cameron A, Candiani I, Cappella P, et al. 2006. 1,4,5,6-Tetrahydropyrrolo[3,4-c]pyrazoles: identification of a potent Aurora kinase inhibitor with a favorable antitumor kinase inhibition profile. J Med Chem. 49(24):7247–7251. doi: 10.1021/jm060897w.
  • Ghosh S. 2019. Cisplatin: the first metal based anticancer drug. Bioorg Chem. 88:102925. doi: 10.1016/j.bioorg.2019.102925.
  • Gyorffy B. 2021. Survival analysis across the entire transcriptome identifies biomarkers with the highest prognostic power in breast cancer. Comput Struct Biotechnol J. 19:4101–4109.
  • Hashemi M, Arani HZ, Orouei S, Fallah S, Ghorbani A, Khaledabadi M, Kakavand A, Tavakolpournegari A, Saebfar H, Heidari H, et al. 2022. EMT mechanism in breast cancer metastasis and drug resistance: revisiting molecular interactions and biological functions. Biomed Pharmacother. 155:113774. doi: 10.1016/j.biopha.2022.113774.
  • Huang M, Liu C, Shao Y, Zhou S, Hu G, Yin S, Pu W, Yu H. 2022. Anti-tumor pharmacology of natural products targeting mitosis. Cancer Biol Med. 19(6):774–801. doi: 10.20892/j.issn.2095-3941.2022.0006.
  • Jalalirad M, Haddad TC, Salisbury JL, Radisky D, Zhang M, Schroeder M, Tuma A, Leof E, Carter JM, Degnim AC, et al. 2021. Aurora-A kinase oncogenic signaling mediates TGF-beta-induced triple-negative breast cancer plasticity and chemoresistance. Oncogene. 40(14):2509–2523. doi: 10.1038/s41388-021-01711-x.
  • Ke CS, Liu HS, Yen CH, Huang GC, Cheng HC, Huang CY, Su CL. 2014. Curcumin-induced Aurora-A suppression not only causes mitotic defect and cell cycle arrest but also alters chemosensitivity to anticancer drugs. J Nutr Biochem. 25(5):526–539. doi: 10.1016/j.jnutbio.2014.01.003.
  • Lemos Cruz P, Kulagina N, Guirimand G, De Craene JO, Besseau S, Lanoue A, Oudin A, Giglioli-Guivarc’h N, Papon N, Clastre M, et al. 2021. Optimization of tabersonine methoxylation to increase vindoline precursor synthesis in yeast cell factories. Molecules. 26(12):3596. doi: 10.3390/molecules26123596.
  • Lin C, Cui J, Peng Z, Qian K, Wu R, Cheng Y, Yin W. 2022. Efficacy of platinum-based and non-platinum-based drugs on triple-negative breast cancer: meta-analysis. Eur J Med Res. 27(1):201. doi: 10.1186/s40001-022-00839-0.
  • Liu T, Huang Y, Jiang L, Dong C, Gou Y, Lian J. 2021. Efficient production of vindoline from tabersonine by metabolically engineered Saccharomyces cerevisiae. Commun Biol. 4(1):1089. doi: 10.1038/s42003-021-02617-w.
  • Liu X, Li Z, Song Y, Wang R, Han L, Wang Q, Jiang K, Kang C, Zhang Q. 2016. AURKA induces EMT by regulating histone modification through Wnt/beta-catenin and PI3K/Akt signaling pathway in gastric cancer. Oncotarget. 7(22):33152–33164. doi: 10.18632/oncotarget.8888.
  • Liu X, Ouyang S, Yu B, Liu Y, Huang K, Gong J, Zheng S, Li Z, Li H, Jiang H. 2010. PharmMapper server: a web server for potential drug target identification using pharmacophore mapping approach. Nucleic Acids Res. 38:W609–614. doi: 10.1093/nar/gkq300.
  • Liu X, Zou H, Zhao Y, Chen H, Liu T, Wu Z, Yang C, Li Q, Li Y. 2020. Tanshinone inhibits NSCLC by downregulating AURKA through Let-7a-5p. Front Genet. 11:838. doi: 10.3389/fgene.2020.00838.
  • Luo J, Yao JF, Deng XF, Zheng XD, Jia M, Wang YQ, Huang Y, Zhu JH. 2018. 14, 15-EET induces breast cancer cell EMT and cisplatin resistance by up-regulating integrin alphavbeta3 and activating FAK/PI3K/AKT signaling. J Exp Clin Cancer Res. 37(1):23. doi: 10.1186/s13046-018-0694-6.
  • Nedeljkovic M, Damjanovic A. 2019. Mechanisms of chemotherapy resistance in triple-negative breast cancer-how we can rise to the challenge. Cells. 8:957.
  • Qian C, Wang J, Lin W, Chen Y, Yang J, Liu M, Sun X, Wu H, Zhang M, Wang Y, et al. 2023. Tabersonine attenuates obesity-induced renal injury via inhibiting NF-kappaB-mediated inflammation. Phytother Res. 37(6):2353–2363. doi: 10.1002/ptr.7756.
  • Serrano-Gomez SJ, Maziveyi M, Alahari SK. 2016. Regulation of epithelial-mesenchymal transition through epigenetic and post-translational modifications. Mol Cancer. 15(1):18. doi: 10.1186/s12943-016-0502-x.
  • Shi S, Song L, Liu Y, He Y. 2020. Activation of CREB protein with tabersonine attenuates STAT3 during atherosclerosis in apolipoprotein E-deficient mice. Dose Response. 18(1):1559325820912067. doi: 10.1177/1559325820912067.
  • Sun X, Gan L, Li N, Sun S, Li N. 2020. Tabersonine ameliorates osteoblast apoptosis in rats with dexamethasone-induced osteoporosis by regulating the Nrf2/ROS/Bax signalling pathway. AMB Express. 10(1):165. doi: 10.1186/s13568-020-01098-0.
  • Wang B, Sun T, Zhao Y, Wang S, Zhang J, Wang Z, Teng YE, Cai L, Yan M, Wang X, et al. 2022. A randomized phase 3 trial of gemcitabine or nab-paclitaxel combined with cisplatin as first-line treatment in patients with metastatic triple-negative breast cancer. Nat Commun. 13(1):4025. doi: 10.1038/s41467-022-31704-7.
  • Wang L, Arras J, Katsha A, Hamdan S, Belkhiri A, Ecsedy J, El-Rifai W. 2017. Cisplatin-resistant cancer cells are sensitive to Aurora kinase A inhibition by alisertib. Mol Oncol. 11(8):981–995. doi: 10.1002/1878-0261.12066.
  • Wu J, Powell F, Larsen NA, Lai Z, Byth KF, Read J, Gu RF, Roth M, Toader D, Saeh JC, et al. 2013. Mechanism and in vitro pharmacology of TAK1 inhibition by (5Z)-7-oxozeaenol. ACS Chem Biol. 8(3):643–650. doi: 10.1021/cb3005897.
  • Wu X, Zhang W, Font-Burgada J, Palmer T, Hamil AS, Biswas SK, Poidinger M, Borcherding N, Xie Q, Ellies LG, et al. 2014. Ubiquitin-conjugating enzyme Ubc13 controls breast cancer metastasis through a TAK1-p38 MAP kinase cascade. Proc Natl Acad Sci USA. 111(38):13870–13875. doi: 10.1073/pnas.1414358111.
  • Xu Z, Zhang Y, Dai H, Han B. 2022. Epithelial-mesenchymal transition-mediated tumor therapeutic resistance. Molecules. 27(15):4750. doi: 10.3390/molecules27154750.
  • Yan H, Luo B, Wu X, Guan F, Yu X, Zhao L, Ke X, Wu J, Yuan J. 2021. Cisplatin induces pyroptosis via activation of MEG3/NLRP3/caspase-1/GSDMD Pathway in triple-negative breast cancer. Int J Biol Sci. 17(10):2606–2621. doi: 10.7150/ijbs.60292.
  • Yin L, Duan JJ, Bian XW, Yu SC. 2020. Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Res. 22(1):61. doi: 10.1186/s13058-020-01296-5.
  • Yu Z, Cao W, Ren Y, Zhang Q, Liu J. 2020. ATPase copper transporter A, negatively regulated by miR-148a-3p, contributes to cisplatin resistance in breast cancer cells. Clin Transl Med. 10(1):57–73. doi: 10.1002/ctm2.19.
  • Zhang D, Li X, Hu Y, Jiang H, Wu Y, Ding Y, Yu K, He H, Xu J, Sun L, et al. 2018. Tabersonine attenuates lipopolysaccharide-induced acute lung injury via suppressing TRAF6 ubiquitination. Biochem Pharmacol. 154:183–192. doi: 10.1016/j.bcp.2018.05.004.