Evodiamine induces reactive oxygen species‑dependent apoptosis and necroptosis in human melanoma A‑375 cells

Liu,Ning; Li,Yongxi; Chen,Guanzhi; Ge,Keli

doi:10.3892/ol.2020.11983

Evodiamine induces reactive oxygen species‑dependent apoptosis and necroptosis in human melanoma A‑375 cells

Authors:
- Ning Liu
- Yongxi Li
- Guanzhi Chen
- Keli Ge
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Affiliations: Department of Dermatology, The Affiliated Qingdao Municipal Hospital of Qingdao University, Qingdao, Shandong 266011, P.R. China, Department of Dermatology, The Affiliated Hospital of Qingdao University, Qingdao, Shandong 266000, P.R. China, Institute of Integrated Medicine, Medical College, Qingdao University, Qingdao, Shandong 266023, P.R. China
Published online on: August 13, 2020 https://doi.org/10.3892/ol.2020.11983
Article Number: 121
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Melanoma is a common solid malignant tumor with a high frequency of metastasis and relapse. Evodiamine (EVO), a natural small molecule, has recently attracted considerable attention due to its pharmacological action, including its anticancer effects. However, the mechanism of the cytotoxic effect exerted by EVO on tumor cells is not yet fully understood. The present study aimed to evaluate the antitumor effects of evodiamine in human melanoma A‑375 cells. The results demonstrated that EVO inhibited cell proliferation and induced cell cycle arrest at the G2/M stage in human melanoma A‑375 cells. The results also revealed that EVO exposure induced the activation of caspase‑3, caspase‑9 and poly (ADP‑ribose) polymerase 1, as well as mitochondrial membrane potential dissipation in a time‑dependent manner, indicating that EVO induced intrinsic apoptosis in A‑375 cells. Furthermore, the results revealed that receptor‑interacting serine/threonine kinase (RIP) and RIP3 were sequentially activated, suggesting that necroptosis may also be involved in EVO‑induced cell death in A‑375 cells. In addition, co‑treatment with catalase was demonstrated to significantly attenuate the EVO‑induced cell death in A‑375 cells, indicating that reactive oxygen species (ROS) may serve an important role in EVO‑induced cell death. In conclusion, the results of the present study unveiled a novel mechanism of drug action by EVO in human melanoma cells and suggested its potential value in treating human melanoma by inducing cell death via ROS activation.

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1	Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI
2	Leonardi GC, Falzone L, Salemi R, Zanghì A, Spandidos DA, Mccubrey JA, Candido S and Libra M: Cutaneous melanoma: From pathogenesis to therapy (Review). Int J Oncol. 52:1071–1080. 2018.PubMed/NCBI
3	Lee SH, Son JK, Jeong BS, Jeong TC, Chang HW, Lee ES and Jahng Y: Progress in the studies on rutaecarpine. Molecules. 13:272–300. 2008. View Article : Google Scholar : PubMed/NCBI
4	Lin H, Tsai SC, Chen JJ, Chiao YC, Wang SW, Wang GJ, Chen CF and Wang PS: Effects of evodiamine on the secretion of testosterone in rat testicular interstitial cells. Metabolism. 48:1532–1535. 1999. View Article : Google Scholar : PubMed/NCBI
5	Yoshizumi M, Houchi H, Ishimura Y, Hirose M, Kitagawa T, Tsuchiya K, Minakuchi K and Tamaki T: Effect of evodiamine on catecholamine secretion from bovine adrenal medulla. J Med Invest. 44:79–82. 1997.PubMed/NCBI
6	Kobayashi Y: The nociceptive and anti-nociceptive effects of evodiamine from fruits of Evodia rutaecarpa in mice. Planta Med. 69:425–428. 2003. View Article : Google Scholar : PubMed/NCBI
7	Chiou WF, Sung YJ, Liao JF, Shum AY and Chen CF: Inhibitory effect of dehydroevodiamine and evodiamine on nitric oxide production in cultured murine macrophages. J Nat Prod. 60:708–711. 1997. View Article : Google Scholar : PubMed/NCBI
8	Kobayashi Y, Nakano Y, Kizaki M, Hoshikuma K, Yokoo Y and Kamiya T: Capsaicin-like anti-obese activities of evodiamine from fruits of Evodia rutaecarpa, a vanilloid receptor agonist. Planta Med. 67:628–633. 2001. View Article : Google Scholar : PubMed/NCBI
9	Chiou WF, Chou CJ, Shum AY and Chen CF: The vasorelaxant effect of evodiamine in rat isolated mesenteric arteries: Mode of action. Eur J Pharmacol. 215:277–283. 1992. View Article : Google Scholar : PubMed/NCBI
10	Tsai TH, Lee TF, Chen CF and Wang LC: Thermoregulatory effects of alkaloids isolated from Wu-chu-yu in afebrile and febrile rats. Pharmacol Biochem Behav. 50:293–298. 1995. View Article : Google Scholar : PubMed/NCBI
11	King CL, Kong YC, Wong NS, Yeung HW, Fong HH and Sankawa U: Uterotonic effect of Evodia rutaecarpa alkaloids. J Nat Prod. 43:577–582. 1980. View Article : Google Scholar : PubMed/NCBI
12	Lee TJ, Kim EJ, Kim S, Jung EM, Park JW, Jeong SH, Park SE, Yoo YH and Kwon TK: Caspase-dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells. Mol Cancer Ther. 5:2398–2407. 2006. View Article : Google Scholar : PubMed/NCBI
13	Wang C, Wang MW, Tashiro SI, Onodera S and Ikejima T: Evodiamine induced human melanoma A375-S2 cell death partially through interleukin 1 mediated pathway. Biol Pharm Bull. 28:984–989. 2005. View Article : Google Scholar : PubMed/NCBI
14	Liao CH, Pan SL, Guh JH, Chang YL, Pai HC, Lin CH and Teng CM: Antitumor mechanism of evodiamine, a constituent from Chinese herb Evodiae fructus, in human multiple-drug resistant breast cancer NCI/ADR-RES cells in vitro and in vivo. Carcinogenesis. 26:968–975. 2005. View Article : Google Scholar : PubMed/NCBI
15	Kan SF, Yu CH, Pu HF, Hsu JM, Chen MJ and Wang PS: Anti-proliferative effects of evodiamine on human prostate cancer cell lines DU145 and PC3. J Cell Biochem. 101:44–56. 2007. View Article : Google Scholar : PubMed/NCBI
16	Fei XF, Wang BX, Li TJ, Tashiro SI, Minami M, Xing DJ and Ikejima T: Evodiamine, a constituent of Evodiae fructus, induces anti-proliferating effects in tumor cells. Cancer Sci. 94:92–98. 2003. View Article : Google Scholar : PubMed/NCBI
17	Ogasawara M, Matsubara T and Suzuki H: Inhibitory effects of evodiamine on in vitro invasion and experimental lung metastasis of murine colon cancer cells. Biol Pharm Bull. 24:917–920. 2001. View Article : Google Scholar : PubMed/NCBI
18	Ogasawara M, Matsunaga T, Takahashi S, Saiki I and Suzuki H: Anti-invasive and metastatic activities of evodiamine. Biol Pharm Bull. 25:1491–1493. 2002. View Article : Google Scholar : PubMed/NCBI
19	Dickinson BC and Chang CJ: Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol. 7:504–511. 2011. View Article : Google Scholar : PubMed/NCBI
20	Kong Q, Beel JA and Lillehei KO: A threshold concept for cancer therapy. Med Hypotheses. 55:29–35. 2000. View Article : Google Scholar : PubMed/NCBI
21	Schafer FQ and Buettner GR: Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med. 30:1191–1212. 2001. View Article : Google Scholar : PubMed/NCBI
22	Obrador E, Liu-Smith F, Dellinger RW, Salvador R, Meyskens FL and Estrela JM: Oxidative stress and antioxidants in the pathophysiology of malignant melanoma. Biol Chem. 400:589–612. 2019. View Article : Google Scholar : PubMed/NCBI
23	Wang R, Deng D, Shao N, Xu Y, Xue L, Peng Y, Liu Y and Zhi F: Evodiamine activates cellular apoptosis through suppressing PI3K/AKT and activating MAPK in glioma. OncoTargets Ther. 11:1183–1192. 2018. View Article : Google Scholar
24	Yang J, Wu LJ, Tashino S, Onodera S and Ikejima T: Protein tyrosine kinase pathway-derived ROS/NO productions contribute to G2/M cell cycle arrest in evodiamine-treated human cervix carcinoma HeLa cells. Free Radic Res. 44:792–802. 2010. View Article : Google Scholar : PubMed/NCBI
25	Linkermann A and Green DR: Necroptosis. N Engl J Med. 370:455–465. 2014. View Article : Google Scholar : PubMed/NCBI
26	Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alvarez-Diaz S, Lewis R, Lalaoui N, Metcalf D, Webb AI, et al: The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity. 39:443–453. 2013. View Article : Google Scholar : PubMed/NCBI
27	Glorieux C and Calderon PB: Catalase, a remarkable enzyme: Targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biol Chem. 398:1095–1108. 2017. View Article : Google Scholar : PubMed/NCBI
28	Huang DM, Guh JH, Huang YT, Chueh SC, Chiang PC and Teng CM: Induction of mitotic arrest and apoptosis in human prostate cancer pc-3 cells by evodiamine. J Urol. 173:256–261. 2005. View Article : Google Scholar : PubMed/NCBI
29	Malumbres M and Barbacid M: Cell cycle, CDKs and cancer: A changing paradigm. Nat Rev Cancer. 9:153–166. 2009. View Article : Google Scholar : PubMed/NCBI
30	Taylor WR and Stark GR: Regulation of the G2/M transition by p53. Oncogene. 20:1803–1815. 2001. View Article : Google Scholar : PubMed/NCBI
31	Booher RN, Holman PS and Fattaey A: Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J Biol Chem. 272:22300–22306. 1997. View Article : Google Scholar : PubMed/NCBI
32	Sui H, Zhou LH, Zhang YL, Huang JP, Liu X, Ji Q, Fu XL, Wen HT, Chen ZS, Deng WL, et al: Evodiamine suppresses ABCG2 mediated drug resistance by inhibiting p50/p65 NF-kB pathway in colorectal cancer. J Cell Biochem. 117:1471–1481. 2016. View Article : Google Scholar : PubMed/NCBI
33	Yang J, Cai X, Lu W, Hu C, Xu X, Yu Q and Cao P: Evodiamine inhibits STAT3 signaling by inducing phosphatase shatterproof 1 in hepatocellular carcinoma cells. Cancer Lett. 328:243–251. 2013. View Article : Google Scholar : PubMed/NCBI
34	Tait SW and Green DR: Mitochondria and cell death: Outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol. 11:621–632. 2010. View Article : Google Scholar : PubMed/NCBI
35	Czabotar PE, Lessene G, Strasser A and Adams JM: Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat Rev Mol Cell Biol. 15:49–63. 2014. View Article : Google Scholar : PubMed/NCBI
36	Delbridge AR, Grabow S, Strasser A and Vaux DL: Thirty years of BCL-2: Translating cell death discoveries into novel cancer therapies. Nat Rev Cancer. 16:99–109. 2016. View Article : Google Scholar : PubMed/NCBI
37	Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES and Wang X: Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479–489. 1997. View Article : Google Scholar : PubMed/NCBI
38	Riedl SJ and Salvesen GS: The apoptosome: Signalling platform of cell death. Nat Rev Mol Cell Biol. 8:405–413. 2007. View Article : Google Scholar : PubMed/NCBI
39	Fatokun AA, Dawson VL and Dawson TM: Parthanatos: Mitochondrial-linked mechanisms and therapeutic opportunities. Br J Pharmacol. 171:2000–2016. 2014. View Article : Google Scholar : PubMed/NCBI
40	Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW, et al: Molecular mechanisms of cell death: Recommendations of the nomenclature committee on cell death 2018. Cell Death Differ. 25:486–541. 2018. View Article : Google Scholar : PubMed/NCBI
41	Galluzzi L, Bravo-San Pedro JM, Vitale I, Aaronson SA, Abrams JM, Adam D, Alnemri ES, Altucci L, Andrews D, Annicchiarico-Petruzzelli M, et al: Essential versus accessory aspects of cell death: Recommendations of the NCCD 2015. Cell Death Differ. 22:58–73. 2015. View Article : Google Scholar : PubMed/NCBI
42	Prabhakaran K, Li L, Borowitz JL and Isom GE: Caspase inhibition switches the mode of cell death induced by cyanide by enhancing reactive oxygen species generation and PARP-1 activation. Toxicol Appl Pharmacol. 195:194–202. 2004. View Article : Google Scholar : PubMed/NCBI
43	Steinhart L, Belz K and Fulda S: Smac mimetic and demethylating agents synergistically trigger cell death in acute myeloid leukemia cells and overcome apoptosis resistance by inducing necroptosis. Cell Death Dis. 4:e8022013. View Article : Google Scholar : PubMed/NCBI
44	Dunai ZA, Imre G, Barna G, Korcsmaros T, Petak I, Bauer PI and Mihalik R: Staurosporine induces necroptotic cell death under caspase-compromised conditions in U937 cells. PLoS One. 7:e419452012. View Article : Google Scholar : PubMed/NCBI