Combined Treatment (Ultraviolet-C/Physapruin A) Enhances Antiproliferation and Oxidative-Stress-Associated Mechanism in Oral Cancer Cells
Abstract
:1. Introduction
2. Materials and Methods
2.1. Cell Culture
2.2. UVC Irradiation and Drug Treatments
2.3. Cell Survival and Cell Number Assays and Synergy Determination
2.4. Cell Cycle Assays
2.5. Annexin V Assay and Caspase 3/7 (Cas 3/7) Activity
2.6. ROS and Mitochondrial Superoxide (MitoSOX) Assays
2.7. Mitochondrial Membrane Potential (MitoMP) Assays
2.8. γH2AX and 8-Hydroxyl-2’-Deoxyguanosine (8-OHdG) Assays
2.9. Statistics
3. Results
3.1. Proliferation-Modulating Effects of UVC/PHA
3.2. Cell-Cycle-Modulating Effects of UVC/PHA
3.3. Apoptosis-Modulating Effects of UVC/PHA
3.4. ROS-Modulating Effects of UVC/PHA
3.5. MitoSOX-Modulating Effects of UVC/PHA
3.6. MitoMP-Modulating Effects of UVC/PHA
3.7. DNA-Damage-Modulating Effects of UVC/PHA
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics, 2021. CA Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef] [PubMed]
- Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; 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, 394–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miranda-Galvis, M.; Loveless, R.; Kowalski, L.P.; Teng, Y. Impacts of environmental factors on head and neck cancer pathogenesis and progression. Cells 2021, 10, 389. [Google Scholar] [CrossRef]
- Huang, S.H.; O’Sullivan, B. Oral cancer: Current role of radiotherapy and chemotherapy. Med. Oral Patol. Oral Cir. Bucal 2013, 18, e233–e240. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Mu, X.; He, H.; Zhang, X.D. Cancer radiosensitizers. Trends Pharmacol. Sci. 2018, 39, 24–48. [Google Scholar] [CrossRef] [PubMed]
- Moeller, B.J.; Richardson, R.A.; Dewhirst, M.W. Hypoxia and radiotherapy: Opportunities for improved outcomes in cancer treatment. Cancer Metastasis Rev. 2007, 26, 241–248. [Google Scholar] [CrossRef]
- Bentzen, S.M. Preventing or reducing late side effects of radiation therapy: Radiobiology meets molecular pathology. Nat. Rev. Cancer 2006, 6, 702–713. [Google Scholar] [CrossRef]
- Oun, R.; Moussa, Y.E.; Wheate, N.J. The side effects of platinum-based chemotherapy drugs: A review for chemists. Dalton Trans. 2018, 47, 6645–6653. [Google Scholar] [CrossRef]
- Gong, L.; Zhang, Y.; Liu, C.; Zhang, M.; Han, S. Application of radiosensitizers in cancer radiotherapy. Int. J. Nanomed. 2021, 16, 1083–1102. [Google Scholar] [CrossRef]
- Nisar, S.; Masoodi, T.; Prabhu, K.S.; Kuttikrishnan, S.; Zarif, L.; Khatoon, S.; Ali, S.; Uddin, S.; Akil, A.A.; Singh, M.; et al. Natural products as chemo-radiation therapy sensitizers in cancers. Biomed. Pharmacother. 2022, 154, 113610. [Google Scholar] [CrossRef]
- Akter, R.; Najda, A.; Rahman, M.H.; Shah, M.; Wesolowska, S.; Hassan, S.S.U.; Mubin, S.; Bibi, P.; Saeeda, S. Potential role of natural products to combat radiotherapy and their future perspectives. Molecules 2021, 26, 5997. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.Y.; Wang, F.X.; Jia, K.K.; Kong, L.D. Natural product interventions for chemotherapy and radiotherapy-induced side effects. Front. Pharmacol. 2018, 9, 1253. [Google Scholar] [CrossRef] [Green Version]
- He, M.; Wang, N.; Zheng, W.; Cai, X.; Qi, D.; Zhang, Y.; Han, C. Ameliorative effects of ginsenosides on myelosuppression induced by chemotherapy or radiotherapy. J. Ethnopharmacol. 2021, 268, 113581. [Google Scholar] [CrossRef]
- Yamauchi, T.; Adachi, S.; Yasuda, I.; Nakashima, M.; Kawaguchi, J.; Yoshioka, T.; Hirose, Y.; Kozawa, O.; Moriwaki, H. Ultra-violet irradiation induces apoptosis via mitochondrial pathway in pancreatic cancer cells. Int. J. Oncol. 2011, 39, 1375–1380. [Google Scholar]
- Adachi, S.; Yasuda, I.; Nakashima, M.; Yamauchi, T.; Kawaguchi, J.; Shimizu, M.; Itani, M.; Nakamura, M.; Nishii, Y.; Yoshioka, T.; et al. Ultraviolet irradiation can induce evasion of colon cancer cells from stimulation of epidermal growth factor. J. Biol. Chem. 2011, 286, 26178–26187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peng, S.Y.; Tang, J.Y.; Li, R.N.; Huang, H.W.; Wu, C.Y.; Chiu, C.C.; Chang, F.R.; Zhang, H.W.; Lee, Y.J.; Sheu, J.H.; et al. Oxidative stress-dependent synergistic antiproliferation, apoptosis, and DNA damage of ultraviolet-C and coral-derived sinularin combined treatment for oral cancer cells. Cancers 2021, 13, 2450. [Google Scholar] [CrossRef] [PubMed]
- Pronin, S.; Koh, C.H.; Hughes, M. Cytotoxicity of ultraviolet-C radiation on a heterogeneous population of human glioblastoma multiforme cells: Meta-analysis. Photodiagnosis Photodyn. Ther. 2018, 24, 158–163. [Google Scholar] [CrossRef]
- Kawaguchi, J.; Adachi, S.; Yasuda, I.; Yamauchi, T.; Nakashima, M.; Ohno, T.; Shimizu, M.; Yoshioka, T.; Itani, M.; Kozawa, O.; et al. Cisplatin and ultra-violet-C synergistically down-regulate receptor tyrosine kinases in human colorectal cancer cells. Mol. Cancer 2012, 11, 45. [Google Scholar] [CrossRef] [Green Version]
- Murray, D.; Mirzayans, R. Cellular responses to platinum-based anticancer drugs and UVC: Role of p53 and implications for cancer therapy. Int. J. Mol. Sci. 2020, 21, 5766. [Google Scholar] [CrossRef]
- Chuang, Y.T.; Shiau, J.P.; Yen, C.Y.; Hou, M.F.; Jeng, J.H.; Tang, J.Y.; Chang, H.W. Fucoidan/UVC combined treatment exerts preferential antiproliferation in oral cancer cells but not normal cells. Antioxidants 2022, 11, 1797. [Google Scholar] [CrossRef]
- Xu, Y.M.; Wijeratne, E.M.K.; Babyak, A.L.; Marks, H.R.; Brooks, A.D.; Tewary, P.; Xuan, L.J.; Wang, W.Q.; Sayers, T.J.; Gunatilaka, A.A.L. Withanolides from aeroponically grown Physalis peruviana and their selective cytotoxicity to prostate cancer and renal carcinoma cells. J. Nat. Prod. 2017, 80, 1981–1991. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.X.; He, H.; Qiu, F. Natural withanolides: An overview. Nat. Prod. Rep. 2011, 28, 705–740. [Google Scholar] [CrossRef] [PubMed]
- Widodo, N.; Priyandoko, D.; Shah, N.; Wadhwa, R.; Kaul, S.C. Selective killing of cancer cells by Ashwagandha leaf extract and its component Withanone involves ROS signaling. PLoS ONE 2010, 5, e13536. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Royston, K.J.; Paul, B.; Nozell, S.; Rajbhandari, R.; Tollefsbol, T.O. Withaferin A and sulforaphane regulate breast cancer cell cycle progression through epigenetic mechanisms. Exp. Cell Res. 2018, 368, 67–74. [Google Scholar] [CrossRef] [PubMed]
- Peng, C.Y.; You, B.J.; Lee, C.L.; Wu, Y.C.; Lin, W.H.; Lu, T.L.; Chang, F.C.; Lee, H.Z. The roles of 4beta-hydroxywithanolide E from Physalis peruviana on the Nrf2-anti-oxidant system and the cell cycle in breast cancer cells. Am. J. Chin. Med. 2016, 44, 617–636. [Google Scholar] [CrossRef] [PubMed]
- Machin, R.P.; Veleiro, A.S.; Nicotra, V.E.; Oberti, J.C.; Padrón, J.M. Antiproliferative activity of withanolides against human breast cancer cell lines. J. Nat. Prod. 2010, 73, 966–968. [Google Scholar] [CrossRef]
- Yu, T.J.; Yen, C.Y.; Cheng, Y.B.; Yen, C.H.; Jeng, J.H.; Tang, J.Y.; Chang, H.W. Physapruin A enhances DNA damage and inhibits DNA repair to suppress oral cancer cell proliferation. Int. J. Mol. Sci. 2022, 23, 8839. [Google Scholar] [CrossRef]
- Yu, T.J.; Cheng, Y.B.; Lin, L.C.; Tsai, Y.H.; Yao, B.Y.; Tang, J.Y.; Chang, F.R.; Yen, C.H.; Ou-Yang, F.; Chang, H.W. Physalis peruviana-derived physapruin A (PHA) inhibits breast cancer cell proliferation and induces oxidative-stress-mediated apoptosis and DNA damage. Antioxidants 2021, 10, 393. [Google Scholar] [CrossRef]
- de Jager, T.L.; Cockrell, A.E.; Du Plessis, S.S. Ultraviolet light induced generation of reactive oxygen species. Adv. Exp. Med. Biol. 2017, 996, 15–23. [Google Scholar]
- Wang, S.C.; Wang, Y.Y.; Lin, L.C.; Chang, M.Y.; Yuan, S.F.; Tang, J.Y.; Chang, H.W. Combined treatment of sulfonyl chromen-4-ones (CHW09) and ultraviolet-C (UVC) enhances proliferation inhibition, apoptosis, oxidative stress, and DNA damage against oral cancer cells. Int. J. Mol. Sci. 2020, 21, 6443. [Google Scholar] [CrossRef]
- Kasten, F.H.; Pineda, L.F.; Schneider, P.E.; Rawls, H.R.; Foster, T.A. Biocompatibility testing of an experimental fluoride releasing resin using human gingival epithelial cells in vitro. In Vitro Cell Dev. Biol. 1989, 25, 57–62. [Google Scholar] [CrossRef] [PubMed]
- Kasten, F.H.; Soileau, K.; Meffert, R.M. Quantitative evaluation of human gingival epithelial cell attachment to implant surfaces in vitro. Int. J. Periodontics Restor. Dent. 1990, 10, 68–79. [Google Scholar]
- Hsieh, P.L.; Liao, Y.W.; Hsieh, C.W.; Chen, P.N.; Yu, C.C. Soy isoflavone genistein impedes cancer stemness and mesenchymal transition in head and neck cancer through activating miR-34a/RTCB axis. Nutrients 2020, 12, 1924. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.Y.; Chang, Y.L.; Liu, S.T.; Chen, G.S.; Lee, S.P.; Huang, S.M. Differential cytotoxicity mechanisms of copper complexed with disulfiram in oral cancer cells. Int. J. Mol. Sci. 2021, 22, 3711. [Google Scholar] [CrossRef] [PubMed]
- Chan, W.H.; Shiao, N.H.; Lu, P.Z. CdSe quantum dots induce apoptosis in human neuroblastoma cells via mitochondrial-dependent pathways and inhibition of survival signals. Toxicol. Lett. 2006, 167, 191–200. [Google Scholar] [CrossRef]
- Hung, J.H.; Chen, C.Y.; Omar, H.A.; Huang, K.Y.; Tsao, C.C.; Chiu, C.C.; Chen, Y.L.; Chen, P.H.; Teng, Y.N. Reactive oxygen species mediate Terbufos-induced apoptosis in mouse testicular cell lines via the modulation of cell cycle and pro-apoptotic proteins. Environ. Toxicol. 2016, 31, 1888–1898. [Google Scholar] [CrossRef]
- Huang, C.H.; Yeh, J.M.; Chan, W.H. Hazardous impacts of silver nanoparticles on mouse oocyte maturation and fertilization and fetal development through induction of apoptotic processes. Environ. Toxicol. 2018, 33, 1039–1049. [Google Scholar] [CrossRef]
- Wang, T.S.; Lin, C.P.; Chen, Y.P.; Chao, M.R.; Li, C.C.; Liu, K.L. CYP450-mediated mitochondrial ROS production involved in arecoline N-oxide-induced oxidative damage in liver cell lines. Environ. Toxicol. 2018, 33, 1029–1038. [Google Scholar] [CrossRef]
- Yu, T.J.; Tang, J.Y.; Shiau, J.P.; Hou, M.F.; Yen, C.H.; Ou-Yang, F.; Chen, C.Y.; Chang, H.W. Gingerenone A induces antiproliferation and senescence of breast cancer cells. Antioxidants 2022, 11, 587. [Google Scholar] [CrossRef]
- Peng, S.Y.; Wang, Y.Y.; Lan, T.H.; Lin, L.C.; Yuan, S.F.; Tang, J.Y.; Chang, H.W. Low dose combined treatment with ultraviolet-C and withaferin a enhances selective killing of oral cancer cells. Antioxidants 2020, 9, 1120. [Google Scholar] [CrossRef]
- Vignon, C.; Debeissat, C.; Georget, M.T.; Bouscary, D.; Gyan, E.; Rosset, P.; Herault, O. Flow cytometric quantification of all phases of the cell cycle and apoptosis in a two-color fluorescence plot. PLoS ONE 2013, 8, e68425. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fan, H.C.; Hsieh, Y.C.; Li, L.H.; Chang, C.C.; Janouskova, K.; Ramani, M.V.; Subbaraju, G.V.; Cheng, K.T.; Chang, C.C. Dehydroxyhispolon methyl ether, a hispolon derivative, inhibits WNT/beta-catenin signaling to elicit human colorectal carcinoma cell apoptosis. Int. J. Mol. Sci. 2020, 21, 8839. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.F.; Lee, M.G.; El-Shazly, M.; Lai, K.H.; Ke, S.C.; Su, C.W.; Shih, S.P.; Sung, P.J.; Hong, M.C.; Wen, Z.H.; et al. Isoaaptamine induces T-47D cells apoptosis and autophagy via oxidative stress. Mar. Drugs 2018, 16, 18. [Google Scholar] [CrossRef] [PubMed]
- Shih, S.P.; Lu, M.C.; El-Shazly, M.; Lin, Y.H.; Chen, C.L.; Yu, S.S.F.; Liu, Y.C. The antileukemic and anti-prostatic effect of aeroplysinin-1 is mediated through ROS-induced apoptosis via NOX activation and inhibition of HIF-1a activity. Life 2022, 12, 687. [Google Scholar] [CrossRef]
- Peng, S.Y.; Lin, L.C.; Yang, Z.W.; Chang, F.R.; Cheng, Y.B.; Tang, J.Y.; Chang, H.W. Combined treatment with low cytotoxic ethyl acetate Nepenthes extract and ultraviolet-C improves antiproliferation to oral cancer cells via oxidative stress. Antioxidants 2020, 9, 873. [Google Scholar] [CrossRef]
- Nasihun, T.; Widayati, E. Administration of purwoceng (Pimpinella alpina Molk) improves oxidative stress biomarker following UVC irradiation in spargue-dawley male rats. J. Nat. Remedies 2016, 16, 115–124. [Google Scholar] [CrossRef] [Green Version]
- Chan, W.H.; Yu, J.S. Inhibition of UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermal carcinoma A431 cells by genistein. J. Cell Biochem. 2000, 78, 73–84. [Google Scholar] [CrossRef]
- Chan, W.H.; Wu, C.C.; Yu, J.S. Curcumin inhibits UV irradiation-induced oxidative stress and apoptotic biochemical changes in human epidermoid carcinoma A431 cells. J. Cell Biochem. 2003, 90, 327–338. [Google Scholar] [CrossRef]
- Kashyap, D.; Sharma, A.; Garg, V.; Tuli, H.S.; Kumar, G.; Kumar, M.; Mukherjee, T. Reactive oxygen species (ROS): An activator of apoptosis and autophagy in cancer. J. Biol. Chem. Sci. 2016, 3, 256–264. [Google Scholar]
- Li, Z.; Yang, J.; Huang, H. Oxidative stress induces H2AX phosphorylation in human spermatozoa. FEBS Lett. 2006, 580, 6161–6168. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Peng, S.-Y.; Yen, C.-Y.; Lan, T.-H.; Jeng, J.-H.; Tang, J.-Y.; Chang, H.-W. Combined Treatment (Ultraviolet-C/Physapruin A) Enhances Antiproliferation and Oxidative-Stress-Associated Mechanism in Oral Cancer Cells. Antioxidants 2022, 11, 2227. https://doi.org/10.3390/antiox11112227
Peng S-Y, Yen C-Y, Lan T-H, Jeng J-H, Tang J-Y, Chang H-W. Combined Treatment (Ultraviolet-C/Physapruin A) Enhances Antiproliferation and Oxidative-Stress-Associated Mechanism in Oral Cancer Cells. Antioxidants. 2022; 11(11):2227. https://doi.org/10.3390/antiox11112227
Chicago/Turabian StylePeng, Sheng-Yao, Ching-Yu Yen, Ting-Hsun Lan, Jiiang-Huei Jeng, Jen-Yang Tang, and Hsueh-Wei Chang. 2022. "Combined Treatment (Ultraviolet-C/Physapruin A) Enhances Antiproliferation and Oxidative-Stress-Associated Mechanism in Oral Cancer Cells" Antioxidants 11, no. 11: 2227. https://doi.org/10.3390/antiox11112227