262
Views
3
CrossRef citations to date
0
Altmetric
Article

Genetic Interpretation of the Impacts of Honokiol and EGCG on Apoptotic and Self-Renewal Pathways in HEp-2 Human Laryngeal CD44high Cancer Stem Cells

, , , , , & ORCID Icon show all
Pages 2152-2173 | Received 18 Oct 2020, Accepted 09 Sep 2021, Published online: 30 Sep 2021

References

  • 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(6):394–424. doi:10.3322/caac.21492
  • Timmermans AJ, de Gooijer CJ, Hamming–Vrieze O, Hilgers FJ, van den Brekel MW. T3-T4 laryngeal cancer in The Netherlands Cancer Institute; 10-year results of the consistent application of an organ-preserving/-sacrificing protocol. Head Neck. 2015;37(10):1495–1503. doi:10.1002/hed.23789
  • Finlan L, Hupp T. Epidermal stem cells and cancer stem cells: insights into cancer and potential therapeutic strategies. Eur J Cancer. 2006;42(9):1283–1292. doi:10.1016/j.ejca.2006.01.047
  • Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414(6859):105–111. doi:10.1038/35102167
  • Shackleton M, Quintana E, Fearon ER, Morrison SJ. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell. 2009;138(5):822–829. doi:10.1016/j.cell.2009.08.017
  • Lee SH, Nam HJ, Kang HJ, Kwon HW, Lim YC. Epigallocatechin-3-gallate attenuates head and neck cancer stem cell traits through suppression of Notch pathway. Eur J Cancer. 2013;49(15):3210–3218. doi:10.1016/j.ejca.2013.06.025
  • Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol. 2011;82(12):1807–1821. doi:10.1016/j.bcp.2011.07.093
  • Lee J-H, Jeong Y-J, Lee S-W, Kim D, Oh S-J, Lim H-S, Oh H-K, Kim S-H, Kim W-J, Jung J-Y, et al. EGCG induces apoptosis in human laryngeal epidermoid carcinoma Hep2 cells via mitochondria with the release of apoptosis-inducing factor and endonuclease G. Cancer Lett. 2010;290(1):68–75. doi:10.1016/j.canlet.2009.08.027
  • Wang X, Hao M-W, Dong K, Lin F, Ren J-H, Zhang H-Z. Apoptosis induction effects of EGCG in laryngeal squamous cell carcinoma cells through telomerase repression. Arch Pharm Res. 2009;32(9):1263–1269. doi:10.1007/s12272-009-1912-8
  • Shin YS, Kang SU, Park JK, Kim YE, Kim YS, Baek SJ, Lee S-H, Kim C-H. Anti-cancer effect of (-)-epigallocatechin-3-gallate (EGCG) in head and neck cancer through repression of transactivation and enhanced degradation of β-catenin. Phytomedicine. 2016;23(12):1344–1355. doi:10.1016/j.phymed.2016.07.005
  • Liu L, Hou L, Gu S, Zuo X, Meng D, Luo M, Zhang X, Huang S, Zhao X. Molecular mechanism of epigallocatechin-3-gallate in human esophageal squamous cell carcinoma in vitro and in vivo. Oncol Rep. 2015;33(1):297–303. doi:10.3892/or.2014.3555
  • Efferth T. Stem cells, cancer stem-like cells, and natural products. Planta Med. 2012;78(10):935–942. doi:10.1055/s-0031-1298540
  • Chung SS, Vadgama JV. Curcumin and epigallocatechin gallate inhibit the cancer stem cell phenotype via down-regulation of STAT3–NFκB signaling. Anticancer Res. 2015;35(1):39–46.
  • Lin C-H, Chao L-K, Hung P-H, Chen Y-J. EGCG inhibits the growth and tumorigenicity of nasopharyngeal tumor-initiating cells through attenuation of STAT3 activation. Int J Clin Exp Pathol. 2014;7(5):2372–2381.
  • Kumazoe M, Takai M, Hiroi S, Takeuchi C, Yamanouchi M, Nojiri T, Onda H, Bae J, Huang Y, Takamatsu K, et al. PDE3 inhibitor and EGCG combination treatment suppress cancer stem cell properties in pancreatic ductal adenocarcinoma. Sci Rep. 2017;7(1):1917. doi:10.1038/s41598-017-02162-9
  • Toden S, Tran H-M, Tovar-Camargo OA, Okugawa Y, Goel A. Epigallocatechin-3-gallate targets cancer stem-like cells and enhances 5-fluorouracil chemosensitivity in colorectal cancer. Oncotarget. 2016;7(13):16158–16171. doi:10.18632/oncotarget.7567
  • Tang S-N, Singh C, Nall D, Meeker D, Shankar S, Srivastava RK. The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J Mol Signal. 2010;5:14. doi:10.1186/1750-2187-5-14
  • Zhu J, Jiang Y, Yang X, Wang S, Xie C, Li X, Li Y, Chen Y, Wang X, Meng Y, et al. Wnt/β-catenin pathway mediates (-)-epigallocatechin-3-gallate (EGCG) inhibition of lung cancer stem cells. Biochem Biophys Res Commun. 2017;482(1):15–21. doi:10.1016/j.bbrc.2016.11.038
  • Tang S-N, Fu J, Nall D, Rodova M, Shankar S, Srivastava RK. Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics. Int J Cancer. 2012;131(1):30–40. doi:10.1002/ijc.26323
  • Fried LE, Arbiser JL. Honokiol, a multifunctional antiangiogenic and antitumor agent. Antioxid Redox Signal. 2009;11(5):1139–1148. doi:10.1089/ars.2009.2440
  • Hahm E-R, Singh SV. Honokiol causes G0-G1 phase cell cycle arrest in human prostate cancer cells in association with suppression of retinoblastoma protein level/phosphorylation and inhibition of E2F1 transcriptional activity. Mol Cancer Ther. 2007;6(10):2686–2695. doi:10.1158/1535-7163.MCT-07-0217
  • Hua H, Chen W, Shen L, Sheng Q, Teng L. Honokiol augments the anti-cancer effects of oxaliplatin in colon cancer cells. Acta Biochim Biophys Sin (Shanghai). 2013;45(9):773–779. doi:10.1093/abbs/gmt071
  • Liu H, Zang C, Emde A, Planas-Silva MD, Rosche M, Kühnl A, Schulz C-O, Elstner E, Possinger K, Eucker J, et al. Anti-tumor effect of honokiol alone and in combination with other anti-cancer agents in breast cancer. Eur J Pharmacol. 2008;591(1-3):43–51. doi:10.1016/j.ejphar.2008.06.026
  • Ahn KS, Sethi G, Shishodia S, Sung B, Arbiser JL, Aggarwal BB. Honokiol potentiates apoptosis, suppresses osteoclastogenesis, and inhibits invasion through modulation of nuclear factor-kappaB activation pathway. Mol Cancer Res. 2006;4(9):621–633. doi:10.1158/1541-7786.MCR-06-0076
  • Ishitsuka K, Hideshima T, Hamasaki M, Raje N, Kumar S, Hideshima H, Shiraishi N, Yasui H, Roccaro AM, Richardson P, et al. Honokiol overcomes conventional drug resistance in human multiple myeloma by induction of caspase-dependent and -independent apoptosis. Blood. 2005;106(5):1794–1800. doi:10.1182/blood-2005-01-0346
  • Chen X-R, Lu R, Dan H-X, Liao G, Zhou M, Li X-Y, Ji N. Honokiol: a promising small molecular weight natural agent for the growth inhibition of oral squamous cell carcinoma cells. Int J Oral Sci. 2011;3(1):34–42. doi:10.4248/IJOS11014
  • Leeman-Neill RJ, Cai Q, Joyce SC, Thomas SM, Bhola NE, Neill DB, Arbiser JL, Grandis JR. Honokiol inhibits epidermal growth factor receptor signaling and enhances the antitumor effects of epidermal growth factor receptor inhibitors. Clin Cancer Res. 2010;16(9):2571–2579. doi:10.1158/1078-0432.CCR-10-0333
  • Singh T, Gupta NA, Xu S, Prasad R, Velu SE, Katiyar SK. Honokiol inhibits the growth of head and neck squamous cell carcinoma by targeting epidermal growth factor receptor. Oncotarget. 2015;6(25):21268–21282. doi:10.18632/oncotarget.4178
  • Kim D-W, Ko SM, Jeon Y-J, Noh Y-W, Choi N-J, Cho S-D, Moon HS, Cho YS, Shin J-C, Park S-M, et al. Anti-proliferative effect of honokiol in oral squamous cancer through the regulation of specificity protein 1. Int J Oncol. 2013;43(4):1103–1110. doi:10.3892/ijo.2013.2028
  • Huang J-S, Yao C-J, Chuang S-E, Yeh C-T, Lee L-M, Chen R-M, Chao W-J, Whang-Peng J, Lai G-M. Honokiol inhibits sphere formation and xenograft growth of oral cancer side population cells accompanied with JAK/STAT signaling pathway suppression and apoptosis induction. BMC Cancer. 2016;16:245. doi:10.1186/s12885-016-2265-6
  • Sengupta S, Nagalingam A, Muniraj N, Bonner MY, Mistriotis P, Afthinos A, Kuppusamy P, Lanoue D, Cho S, Korangath P, et al. Activation of tumor suppressor LKB1 by honokiol abrogates cancer stem-like phenotype in breast cancer via inhibition of oncogenic Stat3. Oncogene. 2017;36(41):5709–5721. doi:10.1038/onc.2017.164
  • Yao C-J, Lai G-M, Yeh C-T, Lai M-T, Shih P-H, Chao W-J, Whang-Peng J, Chuang S-E, Lai T-Y. Honokiol eliminates human oral cancer stem-like cells accompanied with suppression of Wnt/β-catenin signaling and apoptosis induction. Evid Based Complement Alternat Med. 2013;2013:146136.
  • Lai I-C, Shih P-H, Yao C-J, Yeh C-T, Wang-Peng J, Lui T-N, Chuang S-E, Hu T-S, Lai T-Y, Lai G-M, et al. Elimination of cancer stem-like cells and potentiation of temozolomide sensitivity by Honokiol in glioblastoma multiforme cells. PloS One. 2015;10(3):e0114830. doi:10.1371/journal.pone.0114830
  • Ponnurangam S, Mammen JMV, Ramalingam S, He Z, Zhang Y, Umar S, Subramaniam D, Anant S. Honokiol in combination with radiation targets notch signaling to inhibit colon cancer stem cells. Mol Cancer Ther. 2012;11(4):963–972. doi:10.1158/1535-7163.MCT-11-0999
  • Wang J, Wu Y, Gao W, Li F, Bo Y, Zhu M, Fu R, Liu Q, Wen S, Wang B, et al. Identification and characterization of CD133 + CD44+ cancer stem cells from human laryngeal squamous cell carcinoma cell lines. J Cancer. 2017;8(3):497–506. doi:10.7150/jca.17444
  • Guzel E, Karatas O, Ozgurses M, Ozen M. New insights into laryngeal squamous cell carcinoma: cancer stem-like cells. Cancer Res Front. 2015;1(2):138–148. doi:10.17980/2015.138
  • Wei X, Wang J, He J, Ma B, Chen J. Biological characteristics of CD133+ cancer stem cells derived from human laryngeal carcinoma cell line. Int J Clin Exp Med. 2014;7(9):2453–2462.
  • Chen H, Zhou L, Dou T, Wan G, Tang H, Tian J. BMI1’S maintenance of the proliferative capacity of laryngeal cancer stem cells. Head Neck. 2011;33(8):1115–1125. doi:10.1002/hed.21576
  • Chung SS, Aroh C, Vadgama JV. Constitutive activation of STAT3 signaling regulates hTERT and promotes stem cell-like traits in human breast cancer cells. PloS One. 2013;8(12):e83971. doi:10.1371/journal.pone.0083971
  • Takahashi E, Nagano O, Ishimoto T, Yae T, Suzuki Y, Shinoda T, Nakamura S, Niwa S, Ikeda S, Koga H, et al. Tumor necrosis factor-alpha regulates transforming growth factor-beta-dependent epithelial-mesenchymal transition by promoting hyaluronan-CD44-moesin interaction. J Biol Chem. 2010;285(6):4060–4073. doi:10.1074/jbc.M109.056523
  • Wang X, Liu M, Zhao C. Expression of ezrin and moesin related to invasion, metastasis and prognosis of laryngeal squamous cell carcinoma. Genet Mol Res. 2014;13(3):8002–8013. doi:10.4238/2014.September.29.13
  • Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 2004;6(6):R605–R615. doi:10.1186/bcr920
  • Dai M-Y, Fang F, Zou Y, Yi X, Ding Y-J, Chen C, Tao Z-Z, Chen S-M. Downregulation of Notch1 induces apoptosis and inhibits cell proliferation and metastasis in laryngeal squamous cell carcinoma. Oncol Rep. 2015;34(6):3111–3119. doi:10.3892/or.2015.4274
  • Lee SH, Do SI, Lee HJ, Kang HJ, Koo BS, Lim YC. Notch1 signaling contributes to stemness in head and neck squamous cell carcinoma. Lab Invest. 2016;96(5):508–516. doi:10.1038/labinvest.2015.163
  • Atlasi Y, Looijenga L, Fodde R. Cancer stem cells, pluripotency, and cellular heterogeneity: a WNTer perspective. Curr Top Dev Biol. 2014; 107: 373–404. doi:10.1016/B978-0-12-416022-4.00013-5
  • Lee SH, Koo BS, Kim JM, Huang S, Rho YS, Bae WJ, Kang HJ, Kim YS, Moon JH, Lim YC, et al. Wnt/β-catenin signalling maintains self-renewal and tumourigenicity of head and neck squamous cell carcinoma stem-like cells by activating Oct4. J Pathol. 2014;234(1):99–107. doi:10.1002/path.4383
  • Rohatgi R, Scott MP. Patching the gaps in Hedgehog signalling. Nat Cell Biol. 2007;9(9):1005–1009. doi:10.1038/ncb435
  • Dimitrova K, Stoehr M, Dehghani F, Dietz A, Wichmann G, Bertolini J, Mozet C. Overexpression of the Hedgehog signalling pathway in head and neck squamous cell carcinoma. Onkologie. 2013;36(5):279–286. doi:10.1159/000350322
  • Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, Yang SX, Ivy SP. Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update. Nat Rev Clin Oncol. 2015;12(8):445–464. doi:10.1038/nrclinonc.2015.61
  • Etienne-Selloum N, Dandache I, Sharif T, Auger C, Schini-Kerth VB. Polyphenolic compounds targeting p53-family tumor suppressors: current progress and challenges. In Y. Cheng (Ed.), Future aspects of tumor suppressor gene. 2013; 129–67. InTech. doi:10.5772/56471
  • Min NY, Kim J-H, Choi J-H, Liang W, Ko YJ, Rhee S, Bang H, Ham SW, Park AJ, Lee K-H, et al. Selective death of cancer cells by preferential induction of reactive oxygen species in response to (-)-epigallocatechin-3-gallate. Biochem Biophys Res Commun. 2012;421(1):91–7. doi:10.1016/j.bbrc.2012.03.120
  • Nihal M, Ahmad N, Mukhtar H, Wood GS. Anti-proliferative and proapoptotic effects of (-)-epigallocatechin-3-gallate on human melanoma: possible implications for the chemoprevention of melanoma. Int J Cancer. 2005;114(4):513–521. doi:10.1002/ijc.20785
  • Singh T, Prasad R, Katiyar SK. Inhibition of class I histone deacetylases in non-small cell lung cancer by honokiol leads to suppression of cancer cell growth and induction of cell death in vitro and in vivo. Epigenetics. 2013;8(1):54–65. doi:10.4161/epi.23078
  • Nam S, Smith DM, Dou QP. Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo. J Biol Chem. 2001;276(16):13322–13330. doi:10.1074/jbc.M004209200
  • Lin D, Yan Z, Chen A, Ye J, Hu A, Liu J, Peng J, Wu X. Anti-proliferative activity and structure-activity relationship of honokiol derivatives. Bioorg Med Chem. 2019;27(16):3729–3734. doi:10.1016/j.bmc.2019.06.042
  • Lin JM, Gowda AP, Sharma AK, Amin S. In vitro growth inhibition of human cancer cells by novel honokiol analogs. Bioorg Med Chem. 2012;20(10):3202–3211. doi:10.1016/j.bmc.2012.03.062
  • Orrenius S, Nicotera P, Zhivotovsky B. Cell death mechanisms and their implications in toxicology. Toxicol Sci. 2011;119(1):3–19. doi:10.1093/toxsci/kfq268
  • Tian W, Xu D, Han W, He H, Cai H, Chen H, Zhou M, Chen J, Deng Y-C. Cyclophilin D modulates cell death transition from early apoptosis to programmed necrosis induced by honokiol. Int J Oncol. 2013;42(5):1654–1663. doi:10.3892/ijo.2013.1863
  • Bleau A-M, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW, Holland EC. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell. 2009;4(3):226–235. doi:10.1016/j.stem.2009.01.007
  • Hepburn AC, Veeratterapillay R, Williamson SC, El-Sherif A, Sahay N, Thomas HD, Mantilla A, Pickard RS, Robson CN, Heer R, et al. Side population in human non-muscle invasive bladder cancer enriches for cancer stem cells that are maintained by MAPK signalling. PloS One. 2012;7(11):e50690. doi:10.1371/journal.pone.0050690
  • Zhou J, Wulfkuhle J, Zhang H, Gu P, Yang Y, Deng J, Margolick JB, Liotta LA, Petricoin E, Zhang Y, et al. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc Natl Acad Sci USA. 2007;104(41):16158–16163. doi:10.1073/pnas.0702596104
  • Chen X, Li Y, Lin Q, Wang Y, Sun H, Wang J, Cui G, Cai L, Dong X. Tea polyphenols induced apoptosis of breast cancer cells by suppressing the expression of Survivin. Sci Rep. 2014;4:4416. doi:10.1038/srep04416
  • Tian W, Deng Y, Li L, He H, Sun J, Xu D. Honokiol synergizes chemotherapy drugs in multidrug resistant breast cancer cells via enhanced apoptosis and additional programmed necrotic ed necrotic death. Int J Oncol. 2013;42(2):721–732. doi:10.3892/ijo.2012.1739
  • Siemens H, Jackstadt R, Hünten S, Kaller M, Menssen A, Götz U, Hermeking H. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions. Cell Cycle. 2011;10(24):4256–4271. doi:10.4161/cc.10.24.18552
  • Avtanski DB, Nagalingam A, Kuppusamy P, Bonner MY, Arbiser JL, Saxena NK, Sharma D. Honokiol abrogates leptin-induced tumor progression by inhibiting Wnt1-MTA1-β-catenin signaling axis in a microRNA-34a dependent manner. Oncotarget. 2015;6(18):16396–16410. doi:10.18632/oncotarget.3844
  • Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell. 2009;137(4):647–658. doi:10.1016/j.cell.2009.02.038
  • Sánchez‐Peris M, Murga J, Falomir E, Carda M, Marco JA. Synthesis of honokiol analogues and evaluation of their modulating action on VEGF protein secretion and telomerase-related gene expressions. Chem Biol Drug Des. 2017;89(4):577–584. doi:10.1111/cbdd.12880
  • Masuda M, Suzui M, Weinstein IB. Effects of epigallocatechin-3-gallate on growth, epidermal growth factor receptor signaling pathways, gene expression, and chemosensitivity in human head and neck squamous cell carcinoma cell lines. Clin Cancer Res. 2001;7(12):4220–4229.
  • Gao S-Y, Li E-M, Cui L, Lu X-F, Meng L-Y, Yuan H-M, Xie J-J, Du Z-P, Pang J-X, Xu L-Y, et al. Sp1 and AP-1 regulate expression of the human gene VIL2 in esophageal carcinoma cells. J Biol Chem. 2009;284(12):7995–8004. doi:10.1074/jbc.M809734200
  • Kang L, Mao J, Tao Y, Song B, Ma W, Lu Y, Zhao L, Li J, Yang B, Li L, et al. MicroRNA-34a suppresses the breast cancer stem cell-like characteristics by downregulating Notch1 pathway. Cancer Sci. 2015;106(6):700–708. doi:10.1111/cas.12656
  • Averett C, Bhardwaj A, Arora S, Srivastava SK, Khan MA, Ahmad A, Singh S, Carter JE, Khushman M, Singh AP, et al. Honokiol suppresses pancreatic tumor growth, metastasis and desmoplasia by interfering with tumor-stromal cross-talk. Carcinogenesis. 2016;37(11):1052–1061. doi:10.1093/carcin/bgw096
  • Singh AP, Arora S, Bhardwaj A, Srivastava SK, Kadakia MP, Wang B, Grizzle WE, Owen LB, Singh S. CXCL12/CXCR4 protein signaling axis induces sonic hedgehog expression in pancreatic cancer cells via extracellular regulated kinase- and akt kinase-mediated activation of nuclear factor κB: implications for bidirectional tumor-stromal interactions. J Biol Chem. 2012;287(46):39115–39124. doi:10.1074/jbc.M112.409581
  • Lin W, Tongyi S. Role of Bax/Bcl-2 family members in green tea polyphenol induced necroptosis of p53-deficient Hep3B cells. Tumour Biol. 2014;35(8):8065–8075. doi:10.1007/s13277-014-2064-0
  • Shammas MA, Neri P, Koley H, Batchu RB, Bertheau RC, Munshi V, Prabhala R, Fulciniti M, Tai YT, Treon SP, et al. Specific killing of multiple myeloma cells by (-)-epigallocatechin-3-gallate extracted from green tea: biologic activity and therapeutic implications. Blood. 2006;108(8):2804–2810. doi:10.1182/blood-2006-05-022814
  • Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM. p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell. 2012;149(7):1536–1548. doi:10.1016/j.cell.2012.05.014

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.