Seselin promotes cisplatin-induced apoptosis of AGS gastric cancer cells by inhibiting β-catenin expression

Authors

DOI:

https://doi.org/10.2298/ABS230314023S

Keywords:

seselin, cisplatin, coumarin, apoptosis, complementary therapy

Abstract

Paper description:

  • Seselin, one of coumarin derivatives, has an anticancer effect but its detailed mechanism of action is unknown.
  • Human gastric adenocarcinoma cells (AGS) were treated with cisplatin to investigate the effect of seselin on cell death. The role of seselin and cisplatin in cells was determined using a phospho-kinase array.
  • Seselin can regulate the level of β-catenin by modulating the phosphorylation of glycogen synthase kinase-3 beta (GSK-3β), extracellular-signal-regulated kinase (ERK) and Src tyrosine kinase, and can cooperate with cisplatin to promote cancer cell apoptosis.
  • Seselin can be used as an adjuvant drug in chemotherapy to reduce the clinical dosage of chemotherapy.

Abstract: Gastric cancer is a commonly diagnosed form of cancer, and cisplatin is commonly used as a chemotherapy drug for treating it. However, the side effects of cisplatin may reduce patients’ willingness to use it. Seselin, a derivative of coumarin, has been found to have anticancer properties as well as anticoagulant effects. In this study, we investigated the effect of seselin on promoting cisplatin-induced gastric cancer cell death using the cell proliferation reagent WST-1, BrdU incorporation and lactate dehydrogenase release. The role of seselin and cisplatin in the apoptosis of gastric cancer cells was analyzed using a phospho-kinase array and Western blot analysis. Seselin did not affect G2/M stasis, but it promoted cell death in AGS cells treated with cisplatin. Phospho-kinase array analysis revealed that cisplatin regulates intracellular p53 phosphorylation, while seselin regulates intracellular β-catenin expression by affecting the phosphorylation of glycogen synthase kinase-3 beta (GSK-3β), extracellular-signal-regulated kinase (ERK) and Src tyrosine kinase. Seselin and cisplatin promote the apoptosis of gastric cancer cells by the synergistic effect of two distinct signaling pathways. These findings suggest that seselin may be used as a complementary therapy to reduce the clinical dose of chemotherapy.

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References

Morgan E, Arnold M, Camargo MC, Gini A, Kunzmann AT, Matsuda T, Meheus F, Verhoeven RHA, Vignat J, Laversanne M, Ferlay, J, Soerjomataram, I. The current and future incidence and mortality of gastric cancer in 185 countries, 2020-40: A population-based modelling study. EClinicalMedicine. 2022;47:101404. https://doi.org/10.1016/j.eclinm.2022.101404

Li Y, Feng A, Zheng S, Chen C, Lyu J. Recent Estimates and Predictions of 5-Year Survival in Patients with Gastric Cancer: A Model-Based Period Analysis. Cancer Control. 2022:29:10732748221099227. https://doi.org/10.1177/10732748221099227

Petrelli F, Zaniboni A, Coinu A, Cabiddu M, Ghilardi M, Sgroi G, Barni S. Cisplatin or not in advanced gastric cancer: a systematic review and meta-analysis. PLoS One. 2013;8(12):e83022. https://doi.org/10.1371/journal.pone.0083022

Arany I, Safirstein RL. Cisplatin nephrotoxicity. Semin Nephrol. 2003;23(5):460-4. https://doi.org/10.1016/s0270-9295(03)00089-5

Tang C, Livingston MJ, Safirstein R, Dong Z. Cisplatin nephrotoxicity: new insights and therapeutic implications. Nat Rev Nephrol. 2023;19(1):53-72. https://doi.org/10.1038/s41581-022-00631-7

Tang Q, Wang X, Jin H, Mi Y, Liu L, Dong M, Chen Y, Zou Z. Cisplatin-induced ototoxicity: Updates on molecular mechanisms and otoprotective strategies. Eur J Pharm Biopharm. 2021;163:60-71. https://doi.org/10.1016/j.ejpb.2021.03.008

Zhang X, Qiu H, Li C, Cai P, Qi F. The positive role of traditional Chinese medicine as an adjunctive therapy for cancer. Biosci Trends. 2021;15(5):283-98. https://doi.org/10.5582/bst.2021.01318

Jiao L, Dong C, Liu J, Chen Z, Zhang L, Xu J, Shen X, Che J, Yang Y, Huang H Li, H, Sun J, Jiang Y, Mao Z, Chen P, Gong Y, Jin X, Xu L.Effects of Chinese Medicine as Adjunct Medication for Adjuvant Chemotherapy Treatments of Non-Small Cell Lung Cancer Patients. Sci Rep. 2017;7:46524. https://doi.org/10.1038/srep46524

Ling Y. Traditional Chinese medicine in the treatment of symptoms in patients with advanced cancer. Ann Palliat Med. 2013;2(3):141-52. https://doi.org/10.3978/j.issn.2224-5820.2013.04.05

Xiang Y, Guo Z, Zhu P, Chen J, Huang Y. Traditional Chinese medicine as a cancer treatment: Modern perspectives of ancient but advanced science. Cancer Med. 2019;8(5):1958-75. https://doi.org/10.1002/cam4.2108

Kasperkiewicz K, Ponczek MB, Owczarek J, Guga P, Budzisz E. Antagonists of Vitamin K-Popular Coumarin Drugs and New Synthetic and Natural Coumarin Derivatives. Molecules. 2020;25(6):1465. https://doi.org/10.3390/molecules25061465

Banikazemi Z, Mirazimi SM, Dashti F, Mazandaranian MR, Akbari M, Morshedi K, Aslanbeigi F, Rashidian A, Chamanara M, Hamblin MR, Taghizadeh M, Mirzaei H. Coumarins and Gastrointestinal Cancer: A New Therapeutic Option? Front Oncol. 2021;11:752784. https://doi.org/10.3389/fonc.2021.752784

Nishino H, Okuyama T, Takata M, Shibata S, Tokuda H, Takayasu J, Hasegawa T, Nishino A, Ueyama H, Iwashima A. Studies on the anti-tumor-promoting activity of naturally occurring substances. IV. Pd-II [(+)anomalin, (+)praeruptorin B], a seselin-type coumarin, inhibits the promotion of skin tumor formation by 12-O-tetradecanoylphorbol-13-acetate in 7,12-dimethylbenz[a]anthracene-initiated mice. Carcinogenesis. 1990;11(9):1557-61. https://doi.org/10.1093/carcin/11.9.1557

Feng L, Sun Y, Song P, Xu L, Wu X, Wu X, Shen Y, Sun Y, Kong L, Wu X, Xu Q. Seselin ameliorates inflammation via targeting Jak2 to suppress the proinflammatory phenotype of macrophages. Br J Pharmacol. 2019;176(2):317-33. https://doi.org/10.1111/bph.14521

Lu PH, Liao TH, Chen YH, Hsu YL, Kuo CY, Chan CC, Wang LK, Chern CY, Tsai FM. Coumarin Derivatives Inhibit ADP-Induced Platelet Activation and Aggregation. Molecules. 2022;27(13): 4054. https://doi.org/10.3390/molecules27134054

Liu CJ, Wang LK, Kuo CY, Chen ML, Tzeng IS, Tsai FM. Tournefortia sarmentosa Inhibits the Hydrogen Peroxide-Induced Death of H9c2 Cardiomyocytes. Evid Based Complement Alternat Med. 2021;2021:8219141. https://doi.org/10.1155/2021/8219141

Wang CH, Lu TJ, Wang LK, Wu CC, Chen ML, Kuo CY, Shyu RY, Tsai FM. Tazarotene-induced gene 1 interacts with Polo-like kinase 2 and inhibits cell proliferation in HCT116 colorectal cancer cells. Cell Biol Int. 2021;45(11):2347-56. https://doi.org/10.1002/cbin.11681

Trejo-Solis C, Escamilla-Ramirez A, Jimenez-Farfan D, Castillo-Rodriguez RA, Flores-Najera A, Cruz-Salgado A. Crosstalk of the Wnt/beta-Catenin Signaling Pathway in the Induction of Apoptosis on Cancer Cells. Pharmaceuticals (Basel). 2021;14(9):871. https://doi.org/10.3390/ph14090871

Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22(4):526-39. https://doi.org/10.1038/cdd.2014.216

Li YJ, Wei ZM, Meng YX, Ji XR. Beta-catenin up-regulates the expression of cyclinD1, c-myc and MMP-7 in human pancreatic cancer: relationships with carcinogenesis and metastasis. World J Gastroenterol. 2005;11(14):2117-23. https://doi.org/10.3748/wjg.v11.i14.2117

Nusse R, Clevers H. Wnt/beta-Catenin Signaling, Disease, and Emerging Therapeutic Modalities. Cell. 2017;169(6):985-99. https://doi.org/10.1016/j.cell.2017.05.016

Pelaz SG, Tabernero A. Src: coordinating metabolism in cancer. Oncogene. 2022;41(45):4917-28. https://doi.org/10.1038/s41388-022-02487-4

Zhang Y, Wang X. Targeting the Wnt/beta-catenin signaling pathway in cancer. J Hematol Oncol. 2020;13(1):165. https://doi.org/10.1186/s13045-020-00990-3

He R, Du S, Lei T, Xie X, Wang Y. Glycogen synthase kinase 3beta in tumorigenesis and oncotherapy (Review). Oncol Rep. 2020;44(6):2373-85. https://doi.org/10.3892/or.2020.7817

Chiurillo MA. Role of the Wnt/beta-catenin pathway in gastric cancer: An in-depth literature review. World J Exp Med. 2015;5(2):84-102. https://doi.org/10.5493/wjem.v5.i2.84

Mello AA, Leal MF, Rey JA, Pinto GR, Lamarao LM, Montenegro RC, Alves AP, Assumpcao PP, Borges Bdo N, Smith MC, Burbano, RR. Deregulated Expression of SRC, LYN and CKB Kinases by DNA Methylation and Its Potential Role in Gastric Cancer Invasiveness and Metastasis. PLoS One. 2015;10(10):e0140492. https://doi.org/10.1371/journal.pone.0140492

DE Fátima Ferreira Borges DA Costa J, DE Castro Sant' Anna C, Muniz JAPC, DA Rocha CAM, Lamarão LM, DE Fátima Aquino Moreira Nunes C, DE Assumpção PP, Burbano RR.. Deregulation of the SRC Family Tyrosine Kinases in Gastric Carcinogenesis in Non-human Primates. Anticancer Res. 2018;38(11):6317-20. https://doi.org/10.21873/anticanres.12988

Lee SK, Hwang JH, Choi KY. Interaction of the Wnt/beta-catenin and RAS-ERK pathways involving co-stabilization of both beta-catenin and RAS plays important roles in the colorectal tumorigenesis. Adv Biol Regul. 2018;68:46-54. https://doi.org/10.1016/j.jbior.2018.01.001

Ryu WJ, Han G, Lee SH, Choi KY. Suppression of Wnt/beta-catenin and RAS/ERK pathways provides a therapeutic strategy for gemcitabine-resistant pancreatic cancer. Biochem Biophys Res Commun. 2021;549:40-6. https://doi.org/10.1016/j.bbrc.2021.02.076

Glibo M, Serman A, Karin-Kujundzic V, Bekavac Vlatkovic I, Miskovic B, Vranic S, Serman L. The role of glycogen synthase kinase 3 (GSK3) in cancer with emphasis on ovarian cancer development and progression: A comprehensive review. Bosn J Basic Med Sci. 2021;21(1):5-18. https://doi.org/10.17305/bjbms.2020.5036

Liebl MC, Hofmann TG. Cell Fate Regulation upon DNA Damage: p53 Serine 46 Kinases Pave the Cell Death Road. Bioessays. 2019;41(12):e1900127. https://doi.org/10.1002/bies.201900127

Yogosawa S, Yoshida K. Tumor suppressive role for kinases phosphorylating p53 in DNA damage-induced apoptosis. Cancer Sci. 2018;109(11):3376-82. https://doi.org/10.1111/cas.13792

Liu J, Xiao Q, Xiao J, Niu C, Li Y, Zhang X, Zhou Z, Shu G, Yin G. Wnt/beta-catenin signalling: function, biological mechanisms, and therapeutic opportunities. Signal Transduct Target Ther. 2022;7(1):3. https://doi.org/10.1038/s41392-021-00762-6

Ali S, Tahir M, Khan AA, Chen XC, Ling M, Huang Y. Cisplatin Synergistically Enhances Antitumor Potency of Conditionally Replicating Adenovirus via p53 Dependent or Independent Pathways in Human Lung Carcinoma. Int J Mol Sci. 2019;20(5):1125. https://doi.org/10.3390/ijms20051125

Kleih M, Bopple K, Dong M, Gaissler A, Heine S, Olayioye MA, Aulitzky WE, Essmann F. Direct impact of cisplatin on mitochondria induces ROS production that dictates cell fate of ovarian cancer cells. Cell Death Dis. 2019;10(11):851. https://doi.org/10.1038/s41419-019-2081-4

Zamble DB, Jacks T, Lippard SJ. p53-Dependent and -independent responses to cisplatin in mouse testicular teratocarcinoma cells. Proc Natl Acad Sci U S A. 1998;95(11):6163-68. https://doi.org/10.1073/pnas.95.11.6163

McSweeney KR, Gadanec LK, Qaradakhi T, Ali BA, Zulli A, Apostolopoulos V. Mechanisms of Cisplatin-Induced Acute Kidney Injury: Pathological Mechanisms, Pharmacological Interventions, and Genetic Mitigations. Cancers (Basel). 2021;13(7):1572. https://doi.org/10.3390/cancers13071572

Waissbluth S, Maass JC, Sanchez HA, Martinez AD. Supporting Cells and Their Potential Roles in Cisplatin-Induced Ototoxicity. Front Neurosci. 2022;16:867034. https://doi.org/10.3389/fnins.2022.867034

Qin M, Huang Q, Yang X, Yu L, Tang Y, Zhang C, Qin D, Zou W, Deng J, Liu J, Hu H, Wang L, Wu, A, Wu J. Taxillus chinensis (DC.) Danser: a comprehensive review on botany, traditional uses, phytochemistry, pharmacology, and toxicology. Chin Med. 2022;17(1):136. https://doi.org/10.1186/s13020-022-00694-5

Meyer-Hamme G, Beckmann K, Radtke J, Efferth T, Greten HJ, Rostock M, Schroder S. A survey of chinese medicinal herbal treatment for chemotherapy-induced oral mucositis. Evid Based Complement Alternat Med. 2013;2013:284959. https://doi.org/10.1155/2013/284959

Lai YJ, Tai CJ, Wang CW, Choong CY, Lee BH, Shi YC, Tai CJ. Anti-Cancer Activity of Solanum nigrum (AESN) through Suppression of Mitochondrial Function and Epithelial-Mesenchymal Transition (EMT) in Breast Cancer Cells. Molecules. 2016;21(5):553. https://doi.org/10.3390/molecules21050553

Nawaz A, Jamal A, Arif A, Parveen Z. In vitro cytotoxic potential of Solanum nigrum against human cancer cell lines. Saudi J Biol Sci. 2021;28(8):4786-92. https://doi.org/10.1016/j.sjbs.2021.05.004

Ju SM, Kang JG, Bae JS, Pae HO, Lyu YS, Jeon BH. The Flavonoid Apigenin Ameliorates Cisplatin-Induced Nephrotoxicity through Reduction of p53 Activation and Promotion of PI3K/Akt Pathway in Human Renal Proximal Tubular Epithelial Cells. Evid Based Complement Alternat Med. 2015;2015:186436. https://doi.org/10.1155/2015/186436

Wang SW, Xu Y, Weng YY, Fan XY, Bai YF, Zheng XY, Lou LJ, Zhang F. Astilbin ameliorates cisplatin-induced nephrotoxicity through reducing oxidative stress and inflammation. Food Chem Toxicol. 2018;114:227-36. https://doi.org/10.1016/j.fct.2018.02.041

Kachadourian R, Leitner HM, Day BJ. Selected flavonoids potentiate the toxicity of cisplatin in human lung adenocarcinoma cells: a role for glutathione depletion. Int J Oncol. 2007;31(1):161-8. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3983955

Mon MT, Yodkeeree S, Punfa W, Pompimon W, Limtrakul P. Alkaloids from Stephania venosa as Chemo-Sensitizers in SKOV3 Ovarian Cancer Cells via Akt/NF-kappaB Signaling. Chem Pharm Bull (Tokyo). 2018;66(2):162-9. https://doi.org/10.1248/cpb.c17-00687

Zhang Y, Chen S, Wei C, Rankin GO, Rojanasakul Y, Ren N, Ye X, Chen YC. Dietary Compound Proanthocyanidins from Chinese bayberry (Myrica rubra Sieb. et Zucc.) leaves inhibit angiogenesis and regulate cell cycle of cisplatin-resistant ovarian cancer cells via targeting Akt pathway. J Funct Foods. 2018;40:573-81. https://doi.org/10.1016/j.jff.2017.11.045

Dasari S, Njiki S, Mbemi A, Yedjou CG, Tchounwou PB. Pharmacological Effects of Cisplatin Combination with Natural Products in Cancer Chemotherapy. Int J Mol Sci. 2022;23(3):1532. https://doi.org/10.3390/ijms23031532

Kim HJ, Choi JW, Ree J, Lim JS, Lee J, Kim JI, Thapa SB, Sohng JK, Park YI. Aloe emodin 3-O-glucoside inhibits cell growth and migration and induces apoptosis of non-small-cell lung cancer cells via suppressing MEK/ERK and Akt signalling pathways. Life Sci. 2022;300:120495. https://doi.org/10.1016/j.lfs.2022.120495

Mijatovic S, Maksimovic-Ivanic D, Radovic J, Miljkovic D, Kaludjerovic GN, Sabo TJ, Trajkovic V. Aloe emodin decreases the ERK-dependent anticancer activity of cisplatin. Cell Mol Life Sci. 2005;62(11):1275-82. https://doi.org/10.1007/s00018-005-5041-3

Chen SH, Chang JY. New Insights into Mechanisms of Cisplatin Resistance: From Tumor Cell to Microenvironment. Int J Mol Sci. 2019;20(17):4136. https://doi.org/10.3390/ijms20174136

Li L, Liu HC, Wang C, Liu X, Hu FC, Xie N, Lu L, Chen X, Huang HZ. Overexpression of beta-Catenin Induces Cisplatin Resistance in Oral Squamous Cell Carcinoma. Biomed Res Int. 2016;2016:5378567. https://doi.org/10.1155/2016/5378567

Zhang J, Liu J, Li H, Wang J. beta-Catenin signaling pathway regulates cisplatin resistance in lung adenocarcinoma cells by upregulating Bcl-xl. Mol Med Rep. 2016;13(3):2543-51. https://doi.org/10.3892/mmr.2016.4882

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Published

2023-10-26

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Shyu R-Y, Wang C-H, Wu C-C, Wang L-K, Tsai F-M. Seselin promotes cisplatin-induced apoptosis of AGS gastric cancer cells by inhibiting β-catenin expression. Arch Biol Sci [Internet]. 2023Oct.26 [cited 2024May9];75(3):287-9. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/8523

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