International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
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Anticancer effects of Ulva compressa extracts on FaDu human hypopharangeal squamous carcinoma cells in vitro

  • Jang, Ji Yun (Department of Oral Biochemistry, College of Dentistry, Chosun University) ;
  • Jung, Seo Yun (Department of Oral Biochemistry, College of Dentistry, Chosun University) ;
  • Park, Bo-Ram (Department of Dental Hygiene, College of Health and Welfare, Kyungwoon University) ;
  • Lee, Seul Ah (Marine Healthcare Reaserch & Evaluation Center, Chosun University) ;
  • Kim, Chun Sung (Department of Oral Biochemistry, College of Dentistry, Chosun University)
  • Received : 2022.09.13
  • Accepted : 2022.09.22
  • Published : 2022.09.30
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Abstract

Ulva compressa Linnaeus (UCL) is a green algae seaweed that performs photosynthesis and is used as a food material in some Asian regions including Korea. It is known to be the dominant species in copper ion-contaminated seas, and many studies on copper ion resistant mechanisms have been reported. UCL is known to have an excellent antioxidant effect, but limited information is available regarding its other physiological activities. In this study, we investigated the anticancer activity of 30% prethanol extracts of Ulva compressa Linnaeus (30% PeUCL) and the underlying mechanisms of its activity on human FaDu hypopharyngeal squamous carcinoma cells. The 30% PeUCL extracts suppressed FaDu cell viability without affecting normal cells (L929), as determined by MTT and viability assays. Furthermore, the 30% PeUCL extracts induced apoptosis, as determined by DAPI staining. The 30% PeUCL extracts inhibited colony formation effectively as well as wound-healing of FaDu cells, even at noncytotoxic concentrations. In addition, 30% PeUCL extracts induced apoptosis significantly through proteolytic cleavage of caspase-3, -7, and -9, and poly (ADP-ribose) polymerase, and by downregulation of Bcl-2 and upregulation of Bax in FaDu cells, as determined by Western blot analysis. Collectively, these results suggest that the inhibitory effect of 30% PeUCL extracts on the growth of oral cancer cells, colony formation and wound-healing may be mediated by caspase- and mitochondrial-dependent apoptotic pathways in human FaDu hypopharyngeal squamous carcinoma cells. Therefore, 30% PeUCL extracts can be administered as a natural chemotherapeutic drug for the treatment of human oral cancers.

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References

  1. Ghantous Y, Abu Elnaaj I. [Global incidence and risk factors of oral cancer]. Harefuah 2017;156:645-9. Hebrew.
  2. Lee YC, Wong WT, Li LH, Chu LJ, Menon MP, Ho CL, Chernikov OV, Lee SL, Hua KF. Ginsenoside M1 induces apoptosis and inhibits the migration of human oral cancer cells. Int J Mol Sci 2020;21:9704. doi: 10.3390/ijms21249704.
  3. Wang Z, Lai ST, Xie L, Zhao JD, Ma NY, Zhu J, Ren ZG, Jiang GL. Metformin is associated with reduced risk of pancreatic cancer in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetes Res Clin Pract 2014;106: 19-26. doi: 10.1016/j.diabres.2014.04.007.
  4. Yin W, Liu Y, Liu X, Ma X, Sun B, Yu Z. Metformin inhibits epithelial-mesenchymal transition of oral squamous cell carcinoma via the mTOR/HIF-1α/PKM2/STAT3 pathway. Oncol Lett 2021;21:31. doi: 10.3892/ol.2020.12292.
  5. Shahid S. Review of hematological indices of cancer patients receiving combined chemotherapy & radiotherapy or receiving radiotherapy alone. Crit Rev Oncol Hematol 2016;105:145-55. doi: 10.1016/j.critrevonc.2016.06.001.
  6. Liang SY, Chang TT, Wu WW, Wang TJ. Caring for patients with oral cancer in Taiwan: the challenges faced by family caregivers. Eur J Cancer Care (Engl) 2019;28:e12891. doi: 10.1111/ecc.12891.
  7. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-57. doi: 10.1038/bjc.1972.33.
  8. Kerr JF. History of the events leading to the formulation of the apoptosis concept. Toxicology 2002;181-182:471-4. doi: 10.1016/s0300-483x(02)00457-2.
  9. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516. doi:10.1080/01926230701320337.
  10. Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 2001;41:367-401. doi: 10.1146/annurev.pharmtox.41.1.367.
  11. Smets LA. Programmed cell death (apoptosis) and response to anti-cancer drugs. Anticancer Drugs 1994;5:3-9. doi: 10.1097/00001813-199402000-00001.
  12. Mukherjee AK, Basu S, Sarkar N, Ghosh AC. Advances in cancer therapy with plant based natural products. Curr Med Chem 2001;8:1467-86. doi: 10.2174/0929867013372094.
  13. Shanab SM, Shalaby EA, El-Fayoumy EA. Enteromorpha compressa exhibits potent antioxidant activity. J Biomed Biotechnol 2011;2011:726405. doi: 10.1155/2011/726405.
  14. Cardozo KHM, Guaratini T, Barros MP, Falcao VR, Tonon AP, Lopes NP, Campos S, Torres MA, Souza AO, Colepicolo P, Pinto E. Metabolites from algae with economical impact. Comp Biochem Physiol C Toxicol Pharmacol 2007;146:60-78. doi: 10.1016/j.cbpc.2006.05.007.
  15. Moenne A, Gomez M, Laporte D, Espinoza D, S aez CA, Gonzalez A. Mechanisms of copper tolerance, accumulation, and detoxification in the marine macroalga Ulva compressa (Chlorophyta): 20 years of research. Plants (Basel) 2020;9:681. doi: 10.3390/plants9060681.
  16. Wang L, Kim HS, Je JG, Fu X, Huang C, Ahn G, Oh JY, Sanjeewa KKA, Xu J, Gao X, Yeo IK, Jeon YJ. In vitro and in vivo photoprotective effects of (-)-loliode isolated from the brown seaweed, Sargassum horneri. Molecules 2021;26:6898. doi:10.3390/molecules26226898.
  17. Pradhan B, Patra S, Behera C, Nayak R, Patil S, Bhutia SK, Jena M. Enteromorpha compressa extract induces anticancer activity through apoptosis and autophagy in oral cancer. Mol Biol Rep 2020;47:9567-78. doi: 10.1007/s11033-020-06010-4.
  18. Laporte D, Gonzalez A, Moenne A. Copper-induced activation of MAPKs, CDPKs and CaMKs triggers activation of hexoki- nase and inhibition of pyruvate kinase leading to increased synthesis of ASC, GSH and NADPH in Ulva compressa. Front Plant Sci 2020;11:990. doi: 10.3389/fpls.2020.00990.
  19. Gonzalez A, Laporte D, Moenne A. Cadmium accumulation involves synthesis of glutathione and phytochelatins, and activation of CDPK, CaMK, CBLPK, and MAPK signaling pathways in Ulva compressa. Front Plant Sci 2021;12:669096. doi:10.3389/fpls.2021.669096.
  20. Sharma H, Stephen NM, Gopal SS, Udayawara Rudresh D, Kavalappa YP, Haranahalli Shivarudrappa A, Gavirangappa H, Ponesakki G. Phenolic extract of seagrass, Halophila ovalis activates intrinsic pathway of apoptosis in human breast cancer (MCF-7) cells. Nutr Cancer 2021;73:307-17. doi: 10.1080/01635581.2020.1743874.
  21. Doan CC, Le TL, Ho NQC, Tran TLG, Le NTL, Vu QD, La THL, Nguyen VC, Nguyen TPT, Hoang NS. Investigation of bioactive chemical constituents and anti-cancer activity of ethanol extract of Curcuma singularis Gagnep rhizomes. Nat Prod Res 2022;36:4757-62. doi: 10.1080/14786419.2021.2005595.
  22. Ke W, Zhao X, Lu Z. Foeniculum vulgare seed extract induces apoptosis in lung cancer cells partly through the down-regulation of Bcl-2. Biomed Pharmacother 2021;135:111213. doi:10.1016/j.biopha.2020.111213.
  23. Nelson VK, Sahoo NK, Sahu M, Sudhan HH, Pullaiah CP, Muralikrishna KS. In vitro anticancer activity of Eclipta alba whole plant extract on colon cancer cell HCT-116. BMC Complement Med Ther 2020;20:355. doi: 10.1186/s12906-020-03118-9.
  24. Su Z, Yang Z, Xu Y, Chen Y, Yu Q. Apoptosis, autophagy, necroptosis, and cancer metastasis. Mol Cancer 2015;14:48. doi: 10.1186/s12943-015-0321-5.
  25. Xu X, Lai Y, Hua ZC. Apoptosis and apoptotic body: disease message and therapeutic target potentials. Biosci Rep 2019; 39:BSR20180992. doi: 10.1042/BSR20180992.
  26. Van Opdenbosch N, Lamkanfi M. Caspases in cell death, inflammation, and disease. Immunity 2019;50:1352-64. doi:10.1016/j.immuni.2019.05.020.
  27. Shi Y. Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002;9:459-70. doi: 10.1016/s1097-2765(02)00482-3.
  28. Sham N, Qin C, Zhu Z, Redington CG, Xiao H, Bai Q, Wakefield MR, Kou L, Fang Y. Raspberry extract with potential antitumor activity against cervical cancer. Anticancer Res 2021; 41:3343-8. doi: 10.21873/anticanres.15122.