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Resveratrol inhibits cell growth via targeting the Bmi-1 pathway in YD-10B human oral squamous cell carcinoma cells

  • Park, Kyoung-Eun (Department of Dental Pharmacology, School of Dentistry, Pusan National University) ;
  • Ok, Chang Youp (Department of Dental Pharmacology, School of Dentistry, Pusan National University) ;
  • Jang, Hye-Ock (Department of Dental Pharmacology, School of Dentistry, Pusan National University) ;
  • Bae, Moon-Kyoung (Periodontal Disease Signaling Network Research Center, School of Dentistry, Pusan National University) ;
  • Bae, Soo-Kyung (Department of Dental Pharmacology, School of Dentistry, Pusan National University)
  • Received : 2020.08.07
  • Accepted : 2020.08.26
  • Published : 2020.09.30

Abstract

Resveratrol has been reported to exert anticancer activity via modulation of multiple pathways and genes. In this study, we examined the effect of resveratrol on YD-10B human oral squamous cell carcinoma cells and its molecular mechanisms of action. We found that resveratrol inhibited the proliferation of YD-10B cells in a dose- and time-dependent manner. The suppressive effect of resveratrol was accompanied by a reduction in Bmi-1 gene expression. We observed that silencing the Bmi-1 gene by small interfering RNA effectively downregulated the levels of GLUT1 mRNA and protein, which were also repressed by resveratrol. Bmi-1 silencing increased the number of YD-10B cells in S-phase arrest by approximately 2.3-fold compared with the control. In conclusion, the results of the present study demonstrate, for the first time, that resveratrol suppresses Bmi-1-mediated GLUT1 expression in human oral squamous cell carcinoma cells and suggest that the specific molecular targeting of Bmi-1 and/or GLUT1 expression can be combined with a chemotherapeutic strategy to improve the response of oral cancer cells to resveratrol.

Keywords

References

  1. D'souza S, Addepalli V. Preventive measures in oral cancer: an overview. Biomed Pharmacother 2018;107:72-80. doi: 10.1016/j.biopha.2018.07.114.
  2. Mark AM. What you should know about oral cancer. J Am Dent Assoc 2016;147:312. doi: 10.1016/j.adaj.2016.02.001.
  3. Rivera C. Essentials of oral cancer. Int J Clin Exp Pathol 2015;8:11884-94.
  4. Grafton-Clarke C, Chen KW, Wilcock J. Diagnosis and referral delays in primary care for oral squamous cell cancer: a systematic review. Br J Gen Pract 2019;69:e112-26. doi: 10.3399/bjgp18X700205.
  5. Sasahira T, Kirita T. Hallmarks of cancer-related newly prognostic factors of oral squamous cell carcinoma. Int J Mol Sci 2018;19:2413. doi: 10.3390/ijms19082413.
  6. Sasahira T, Bosserhoff AK, Kirita T. The importance of melanoma inhibitory activity gene family in the tumor progression of oral cancer. Pathol Int 2018;68:278-86. doi: 10.1111/pin.12672.
  7. Cal C, Garban H, Jazirehi A, Yeh C, Mizutani Y, Bonavida B. Resveratrol and cancer: chemoprevention, apoptosis, and chemo- immunosensitizing activities. Curr Med Chem Anticancer Agents 2003;3:77-93. doi: 10.2174/1568011033353443.
  8. Bostanghadiri N, Pormohammad A, Chirani AS, Pouriran R, Erfanimanesh S, Hashemi A. Comprehensive review on the antimicrobial potency of the plant polyphenol resveratrol. Biomed Pharmacother 2017;95:1588-95. doi: 10.1016/j.biopha.2017.09.084.
  9. Fremont L. Biological effects of resveratrol. Life Sci 2000;66:663-73. doi: 10.1016/s0024-3205(99)00410-5.
  10. Pervaiz S, Holme AL. Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal 2009;11:2851-97. doi: 10.1089/ars.2008.2412.
  11. Sinha D, Sarkar N, Biswas J, Bishayee A. Resveratrol for breast cancer prevention and therapy: preclinical evidence and molecular mechanisms. Semin Cancer Biol 2016;40-41:209-32. doi: 10.1016/j.semcancer.2015.11.001.
  12. Aluyen JK, Ton QN, Tran T, Yang AE, Gottlieb HB, Bellanger RA. Resveratrol: potential as anticancer agent. J Diet Suppl 2012;9:45-56. doi: 10.3109/19390211.2011.650842.
  13. Liu Y, Wu X, Hu X, Chen Z, Liu H, Takeda S, Qing Y. Multiple repair pathways mediate cellular tolerance to resveratrolinduced DNA damage. Toxicol In Vitro 2017;42:130-8. doi: 10.1016/j.tiv.2017.04.017.
  14. Takashina M, Inoue S, Tomihara K, Tomita K, Hattori K, Zhao QL, Suzuki T, Noguchi M, Ohashi W, Hattori Y. Different effect of resveratrol to induction of apoptosis depending on the type of human cancer cells. Int J Oncol 2017;50:787-97. doi: 10.3892/ijo.2017.3859.
  15. Chang CH, Lee CY, Lu CC, Tsai FJ, Hsu YM, Tsao JW, Juan YN, Chiu HY, Yang JS, Wang CC. Resveratrol-induced autophagy and apoptosis in cisplatin-resistant human oral cancer CAR cells: a key role of AMPK and Akt/mTOR signaling. Int J Oncol 2017;50:873-82. doi: 10.3892/ijo.2017.3866.
  16. Farhadnejad H, Emamat H, Zand H. The effect of resveratrol on cellular senescence in normal and cancer cells: focusing on cancer and age-related diseases. Nutr Cancer 2019;71:1175-80. doi: 10.1080/01635581.2019.1597907.
  17. Elattar TM, Virji AS. The effect of red wine and its components on growth and proliferation of human oral squamous carcinoma cells. Anticancer Res 1999;19:5407-14.
  18. ElAttar TM, Virji AS. Modulating effect of resveratrol and quercetin on oral cancer cell growth and proliferation. Anticancer Drugs 1999;10:187-93. doi: 10.1097/00001813-199902000-00007.
  19. Singh V, Singh R, Kujur PK, Singh RP. Combination of resveratrol and quercetin causes cell growth inhibition, DNA damage, cell cycle arrest, and apoptosis in oral cancer cells. Assay Drug Dev Technol 2020;18:226-38. doi: 10.1089/adt.2020.972.
  20. Pan J, Shen J, Si W, Du C, Chen D, Xu L, Yao M, Fu P, Fan W. Resveratrol promotes MICA/B expression and natural killer cell lysis of breast cancer cells by suppressing c-Myc/miR-17 pathway. Oncotarget 2017;8:65743-58. doi: 10.18632/oncotarget.19445.
  21. Benetatos L, Vartholomatos G, Hatzimichael E. Polycomb group proteins and MYC: the cancer connection. Cell Mol Life Sci 2014;71:257-69. doi: 10.1007/s00018-013-1426-x.
  22. Siddique HR, Saleem M. Role of BMI1, a stem cell factor, in cancer recurrence and chemoresistance: preclinical and clinical evidences. Stem Cells 2012;30:372-8. doi: 10.1002/stem.1035.
  23. Zheng X, Wang Y, Liu B, Liu C, Liu D, Zhu J, Yang C, Yan J, Liao X, Meng X, Yang H. Bmi-1-shRNA inhibits the proliferation of lung adenocarcinoma cells by blocking the G1/S phase through decreasing cyclin D1 and increasing p21/p27 levels. Nucleic Acid Ther 2014;24:210-6. doi: 10.1089/nat.2013.0459.
  24. Liu J, Luo B, Zhao M. Bmi‑1‑targeting suppresses osteosarcoma aggressiveness through the NF‑${\kappa}$B signaling pathway. Mol Med Rep 2017;16:7949-58. doi: 10.3892/mmr.2017.7660.
  25. Kang MK, Kim RH, Kim SJ, Yip FK, Shin KH, Dimri GP, Christensen R, Han T, Park NH. Elevated Bmi-1 expression is associated with dysplastic cell transformation during oral carcinogenesis and is required for cancer cell replication and survival. Br J Cancer 2007;96:126-33. doi: 10.1038/sj.bjc.6603529.
  26. Kalish JM, Tang XH, Scognamiglio T, Zhang T, Gudas LJ. Doxycycline-induced exogenous Bmi-1 expression enhances tumor formation in a murine model of oral squamous cell carcinoma. Cancer Biol Ther 2020;21:400-11. doi: 10.1080/15384047.2020.1720485.
  27. Chen YC, Chang CJ, Hsu HS, Chen YW, Tai LK, Tseng LM, Chiou GY, Chang SC, Kao SY, Chiou SH, Lo WL. Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral Oncol 2010;46:158-65. doi: 10.1016/j.oraloncology.2009.11.007.
  28. Murray JM, Carr AM. Integrating DNA damage repair with the cell cycle. Curr Opin Cell Biol 2018;52:120-5. doi: 10.1016/j.ceb.2018.03.006.
  29. Tchakarska G, Sola B. The double dealing of cyclin D1. Cell Cycle 2020;19:163-78. doi: 10.1080/15384101.2019.1706903.
  30. Joe AK, Liu H, Suzui M, Vural ME, Xiao D, Weinstein IB. Resveratrol induces growth inhibition, S-phase arrest, apoptosis, and changes in biomarker expression in several human cancer cell lines. Clin Cancer Res 2002;8:893-903.
  31. Park JW, Choi YJ, Jang MA, Lee YS, Jun DY, Suh SI, Baek WK, Suh MH, Jin IN, Kwon TK. Chemopreventive agent resveratrol, a natural product derived from grapes, reversibly inhibits progression through S and G2 phases of the cell cycle in U937 cells. Cancer Lett 2001;163:43-9. doi: 10.1016/s0304-3835(00)00658-3.
  32. Barron CC, Bilan PJ, Tsakiridis T, Tsiani E. Facilitative glucose transporters: Implications for cancer detection, prognosis and treatment. Metabolism 2016;65:124-39. doi: 10.1016/j.metabol.2015.10.007.
  33. Zambrano A, Molt M, Uribe E, Salas M. Glut 1 in Cancer Cells and the Inhibitory Action of Resveratrol as A Potential Therapeutic Strategy. Int J Mol Sci 2019;20:3374. doi: 10.3390/ijms20133374.
  34. Zhou J, Li Y, Li D, Liu Z, Zhang J. Oncoprotein LAMTOR5 activates GLUT1 via upregulating NF-${\kappa}$B in liver cancer. Open Med (Wars) 2019;14:264-70. doi: 10.1515/med-2019-0022.
  35. Salas M, Obando P, Ojeda L, Ojeda P, Perez A, Vargas-Uribe M, Rivas CI, Vera JC, Reyes AM. Resolution of the direct interaction with and inhibition of the human GLUT1 hexose transporter by resveratrol from its effect on glucose accumulation. Am J Physiol Cell Physiol 2013;305:C90-9. doi: 10.1152/ajpcell.00387.2012.
  36. Shibuya K, Okada M, Suzuki S, Seino M, Seino S, Takeda H, Kitanaka C. Targeting the facilitative glucose transporter GLUT1 inhibits the self-renewal and tumor-initiating capacity of cancer stem cells. Oncotarget 2015;6:651-61. doi: 10.18632/oncotarget.2892.
  37. Harshani JM, Yeluri S, Guttikonda VR. Glut-1 as a prognostic biomarker in oral squamous cell carcinoma. J Oral Maxillofac Pathol 2014;18:372-8. doi: 10.4103/0973-029X.151318.