Sulfonyl chromen-4-ones (CHW09) shows an additive effect to inhibit cell growth of X-ray irradiated oral cancer cells, involving apoptosis and ROS generation

References

• Ahire V, Kumar A, Mishra KP, Kulkarni G. 2017. Ellagic acid enhances apoptotic sensitivity of breast cancer cells to γ-Radiation. Nutr Cancer. 69:904–910.
   PubMed Web of Science ®Google Scholar
• Ahire V, Mishra K, Kulkarni G. 2016. Ellagic acid: a potent radio-sensitizer in cancer radiotherapy. Cancer Res Front. 2:141–155.
   Google Scholar
• Bando SI, Hatano O, Takemori H, Kubota N, Ohnishi K. 2017. Potentiality of syringetin for preferential radiosensitization to cancer cells. Int J Radiat Biol. 93:286–294.
   PubMed Web of Science ®Google Scholar
• Belletti B, Vaidya JS, D'Andrea S, Entschladen F, Roncadin M, Lovat F, Berton S, Perin T, Candiani E, Reccanello S, et al. 2008. Targeted intraoperative radiotherapy impairs the stimulation of breast cancer cell proliferation and invasion caused by surgical wounding. Clin Cancer Res. 14:1325–1332.
   PubMed Web of Science ®Google Scholar
• Bigdeli B, Goliaei B, Masoudi-Khoram N, Jooyan N, Nikoofar A, Rouhani M, Haghparast A, Mamashli F. 2016. Enterolactone: a novel radiosensitizer for human breast cancer cell lines through impaired DNA repair and increased apoptosis. Toxicol Appl Pharmacol. 313:180–194.
   PubMed Web of Science ®Google Scholar
• Carpi S, Fogli S, Romanini A, Pellegrino M, Adinolfi B, Podesta A, Costa B, Da Pozzo E, Martini C, Breschi MC, et al. 2015. AM251 induces apoptosis and G2/M cell cycle arrest in A375 human melanoma cells. Anticancer Drugs. 26:754–762.
   PubMed Web of Science ®Google Scholar
• Cerutti PA. 1985. Prooxidant states and tumor promotion. Science. 227:375–381.
   PubMed Web of Science ®Google Scholar
• Chang HW, Li RN, Wang HR, Liu JR, Tang JY, Huang HW, Chan YH, Yen CY. 2017. Withaferin A induces oxidative stress-mediated apoptosis and DNA damage in oral cancer cells. Front Physiol. 8:634.
   PubMed Web of Science ®Google Scholar
• Chang HW, Tang JY, Yen CY, Chang HS, Huang HW, Chung YA, Chen IS, Huang MY. 2016. Synergistic anti-oral cancer effects of UVC and methanolic extracts of Cryptocarya concinna roots via apoptosis, oxidative stress and DNA damage. Int J Radiat Biol. 92:263–272.
   PubMed Web of Science ®Google Scholar
• Chang YT, Wu CY, Tang JY, Huang CY, Liaw CC, Wu SH, Sheu JH, Chang HW. 2017. Sinularin induces oxidative stress-mediated G2/M arrest and apoptosis in oral cancer cells. Environ Toxicol. 32:2124–2132.
   PubMed Web of Science ®Google Scholar
• Chen BH, Chang HW, Huang HM, Chong IW, Chen JS, Chen CY, Wang HM. 2011. (-)Anonaine induces DNA damage and inhibits growth and migration of human lung carcinoma h1299 cells. J Agric Food Chem. 59:2284–2290.
   PubMed Web of Science ®Google Scholar
• Chen CY, Yen CY, Wang HR, Yang HP, Tang JY, Huang HW, Hsu SH, Chang HW. 2016. Tenuifolide B from Cinnamomum tenuifolium stem selectively inhibits proliferation of oral cancer cells via apoptosis, ROS generation, mitochondrial depolarization, and DNA damage. Toxins (Basel). 8:319.
   PubMed Web of Science ®Google Scholar
• Chen Y, Liu HR, Liu HS, Cheng M, Xia P, Qian K, Wu PC, Lai CY, Xia Y, Yang ZY, et al. 2012. Antitumor agents 292. Design, synthesis and pharmacological study of S- and O-substituted 7-mercapto- or hydroxy-coumarins and chromones as potent cytotoxic agents. Eur J Med Chem. 49:74–85.
   PubMed Web of Science ®Google Scholar
• Chen YC, Lu MC, El-Shazly M, Lai KH, Wu TY, Hsu YM, Lee YL, Liu YC. 2018. Breaking down leukemia walls: heteronemin, a sesterterpene derivative, induces apoptosis in leukemia Molt4 cells through oxidative stress, mitochondrial dysfunction and induction of talin Expression. Mar Drugs. 16:212.
   Web of Science ®Google Scholar
• Cheng CY, Liu CJ, Huang YC, Wu SH, Fang HW, Chen YJ. 2018. BI2536 induces mitotic catastrophe and radiosensitization in human oral cancer cells. Oncotarget. 9:21231–21243.
   PubMedGoogle Scholar
• Chiu CC, Haung JW, Chang FR, Huang KJ, Huang HM, Huang HW, Chou CK, Wu YC, Chang HW. 2013. Golden berry-derived 4beta-hydroxywithanolide E for selectively killing oral cancer cells by generating ROS, DNA damage, and apoptotic pathways. PLoS One. 8:e64739.
   PubMed Web of Science ®Google Scholar
• Choi C, Son A, Lee HS, Lee YJ, Park HC. 2018. Radiosensitization by marine sponge Agelas sp. extracts in hepatocellular carcinoma cells with autophagy induction. Sci Rep. 8:6317.
   PubMedGoogle Scholar
• da Costa Araldi IC, Bordin FPR, Cadona FC, Barbisan F, Azzolin VF, Teixeira CF, Baumhardt T, da Cruz IBM, Duarte M, Bauermann LF. 2018. The in vitro radiosensitizer potential of resveratrol on MCF-7 breast cancer cells. Chem Biol Interact. 282:85–92.
   PubMed Web of Science ®Google Scholar
• Dai XF, Ding J, Zhang RG, Ren JH, Ma CM, Wu G. 2013. Radiosensitivity enhancement of human hepatocellular carcinoma cell line SMMC-7721 by sorafenib through the MEK/ERK signal pathway. Int J Radiat Biol. 89:724–731.
   PubMed Web of Science ®Google Scholar
• Dayal R, Singh A, Pandey A, Mishra KP. 2014. Reactive oxygen species as mediator of tumor radiosensitivity. J Cancer Res Ther. 10:811–818.
   PubMed Web of Science ®Google Scholar
• Ewing D, Jones SR. 1987. Superoxide removal and radiation protection in bacteria. Arch Biochem Biophys. 254:53–62.
   PubMed Web of Science ®Google Scholar
• Farooqi AA, Fayyaz S, Hou MF, Li KT, Tang JY, Chang HW. 2014. Reactive oxygen species and autophagy modulation in non-marine drugs and marine drugs. Mar Drugs. 12:5408–5424.
   PubMed Web of Science ®Google Scholar
• Farooqi AA, Li KT, Fayyaz S, Chang YT, Ismail M, Liaw CC, Yuan SS, Tang JY, Chang HW. 2015. Anticancer drugs for the modulation of endoplasmic reticulum stress and oxidative stress. Tumour Biol. 36:5743–5752.
   PubMed Web of Science ®Google Scholar
• Gaspar A, Matos MJ, Garrido J, Uriarte E, Borges F. 2014. Chromone: a valid scaffold in medicinal chemistry. Chem Rev. 114:4960–4992.
   PubMed Web of Science ®Google Scholar
• Gomes A, Fernandes E, Silva AM, Pinto DC, Santos CM, Cavaleiro JA, Lima JL. 2009. Anti-inflammatory potential of 2-styrylchromones regarding their interference with arachidonic acid metabolic pathways. Biochem Pharmacol. 78:171–177.
   PubMed Web of Science ®Google Scholar
• Gong C, Yang Z, Zhang L, Wang Y, Gong W, Liu Y. 2018. Quercetin suppresses DNA double-strand break repair and enhances the radiosensitivity of human ovarian cancer cells via p53-dependent endoplasmic reticulum stress pathway. Onco Targets Ther. 11:17–27.
   PubMed Web of Science ®Google Scholar
• Guo HR, Chen CH, Ho SY, Ho YS, Chen RJ, Wang YJ. 2006. Staurosporine modulates radiosensitivity and radiation-induced apoptosis in U937 cells. Int J Radiat Biol. 82:97–109.
   PubMed Web of Science ®Google Scholar
• Gupte A, Mumper RJ. 2009. Elevated copper and oxidative stress in cancer cells as a target for cancer treatment. Cancer Treat Rev. 35:32–46.
   PubMed Web of Science ®Google Scholar
• Hartner L. 2018. Chemotherapy for oral cancer. Dent Clin North Am. 62:87–97.
   PubMedGoogle Scholar
• Herskind C, Wenz F, Giordano FA. 2017. Immunotherapy combined with large fractions of radiotherapy: stereotactic radiosurgery for brain metastases-implications for intraoperative radiotherapy after resection. Front Oncol. 7:147.
   PubMed Web of Science ®Google Scholar
• Hong WG, Kim JY, Cho JH, Hwang SG, Song JY, Lee E, Chang TS, Um HD, Park JK. 2017. AMRI-59 functions as a radiosensitizer via peroxiredoxin I-targeted ROS accumulation and apoptotic cell death induction. Oncotarget. 8:114050–114064.
   PubMedGoogle Scholar
• Huang HW, Tang JY, Ou-Yang F, Wang HR, Guan PY, Huang CY, Chen CY, Hou MF, Sheu JH, Chang HW. 2018. Sinularin selectively kills breast cancer cells showing G2/M arrest, apoptosis, and oxidative DNA damage. Molecules. 23:849.
   Web of Science ®Google Scholar
• Indo HP, Inanami O, Koumura T, Suenaga S, Yen HC, Kakinuma S, Matsumoto K, Nakanishi I, St Clair W, St Clair DK, et al. 2012. Roles of mitochondria-generated reactive oxygen species on X-ray-induced apoptosis in a human hepatocellular carcinoma cell line, HLE. Free Radic Res. 46:1029–1043.
   PubMed Web of Science ®Google Scholar
• Jayakumar S, Patwardhan RS, Pal D, Sharma D, Sandur SK. 2016. Dimethoxycurcumin, a metabolically stable analogue of curcumin enhances the radiosensitivity of cancer cells: possible involvement of ROS and thioredoxin reductase. Biochem Biophys Res Commun. 478:446–454.
   PubMed Web of Science ®Google Scholar
• Kello M, Drutovic D, Pilatova MB, Tischlerova V, Perjesi P, Mojzis J. 2016. Chalcone derivatives cause accumulation of colon cancer cells in the G2/M phase and induce apoptosis. Life Sci. 150:32–38.
   PubMed Web of Science ®Google Scholar
• Keri RS, Budagumpi S, Pai RK, Balakrishna RG. 2014. Chromones as a privileged scaffold in drug discovery: a review. Eur J Med Chem. 78:340–374.
   PubMed Web of Science ®Google Scholar
• Krall JA, Reinhardt F, Mercury OA, Pattabiraman DR, Brooks MW, Dougan M, Lambert AW, Bierie B, Ploegh HL, Dougan SK, et al. 2018. The systemic response to surgery triggers the outgrowth of distant immune-controlled tumors in mouse models of dormancy. Sci Transl Med. 10:eaan3464.
   PubMed Web of Science ®Google Scholar
• Kuefner MA, Brand M, Engert C, Schwab SA, Uder M. 2015. Radiation induced DNA double-strand breaks in radiology. Rofo. 187:872–878.
   PubMedGoogle Scholar
• Kumazawa Y, Takimoto H, Matsumoto T, Kawaguchi K. 2014. Potential use of dietary natural products, especially polyphenols, for improving type-1 allergic symptoms. Curr Pharm Des. 20:857–863.
   PubMed Web of Science ®Google Scholar
• Lee JC, Hou MF, Huang HW, Chang FR, Yeh CC, Tang JY, Chang HW. 2013. Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int. 13:55.
   PubMed Web of Science ®Google Scholar
• Lin A. 2018. Radiation therapy for oral cavity and oropharyngeal cancers. Dent Clin North Am. 62:99–109.
   PubMedGoogle Scholar
• Liu PF, Hsu CJ, Tsai WL, Cheng JS, Chen JJ, Huang IF, Tseng HH, Chang HW, Shu CW. 2017. Ablation of ATG4B suppressed autophagy and activated AMPK for cell cycle arrest in cancer cells. Cell Physiol Biochem. 44:728–740.
   PubMed Web of Science ®Google Scholar
• Liu Q, Schneider F, Ma L, Wenz F, Herskind C. 2013. Relative Biologic Effectiveness (RBE) of 50 kV X-rays measured in a phantom for intraoperative tumor-bed irradiation. Int J Radiat Oncol Biol Phys. 85:1127–1133.
   PubMed Web of Science ®Google Scholar
• Mates JM, Segura JA, Alonso FJ, Marquez J. 2012. Oxidative stress in apoptosis and cancer: an update. Arch Toxicol. 86:1649–1665.
   PubMed Web of Science ®Google Scholar
• Nambiar DK, Rajamani P, Deep G, Jain AK, Agarwal R, Singh RP. 2015. Silibinin preferentially radiosensitizes prostate cancer by inhibiting DNA repair signaling. Mol Cancer Ther. 14:2722–2734.
   PubMed Web of Science ®Google Scholar
• Niroomand-Rad A, Blackwell CR, Coursey BM, Gall KP, Galvin JM, McLaughlin WL, Meigooni AS, Nath R, Rodgers JE, Soares CG. 1998. Radiochromic film dosimetry: recommendations of AAPM Radiation Therapy Committee Task Group 55. American Association of Physicists in Medicine. Med Phys. 25:2093–2115.
   PubMed Web of Science ®Google Scholar
• Nishida N, Yasui H, Nagane M, Yamamori T, Inanami O. 2014. 3-Methyl pyruvate enhances radiosensitivity through increasing mitochondria-derived reactive oxygen species in tumor cell lines. J Radiat Res. 55:455–463.
   PubMed Web of Science ®Google Scholar
• Oike T, Ogiwara H, Torikai K, Nakano T, Yokota J, Kohno T. 2012. Garcinol, a histone acetyltransferase inhibitor, radiosensitizes cancer cells by inhibiting non-homologous end joining. Int J Radiat Oncol Biol Phys. 84:815–821.
   PubMed Web of Science ®Google Scholar
• Pan Y, Wang M, Bu X, Zuo Y, Wang S, Wang D, Liu Q, Su B, Xu T, Wang C, et al. 2013. Curcumin analogue T83 exhibits potent antitumor activity and induces radiosensitivity through inactivation of Jab1 in nasopharyngeal carcinoma. BMC Cancer. 13:323.
   PubMed Web of Science ®Google Scholar
• Park H, Jeong YJ, Han NK, Kim JS, Lee HJ. 2018. Oridonin enhances radiation-induced cell death by promoting DNA damage in non-small cell lung cancer cells. IJMS. 19:2378.
   Google Scholar
• Rakesh KP, Wang SM, Leng J, Ravindar L, Asiri AM, Marwani HM, Qin HL. 2018. Recent development of sulfonyl or sulfonamide hybrids as potential anticancer agents: a key review. Anticancer Agents Med Chem. 18:488–505.
   PubMed Web of Science ®Google Scholar
• Roszkowski K, Jozwicki W, Blaszczyk P, Mucha-Malecka A, Siomek A. 2011. Oxidative damage DNA: 8-oxoGua and 8-oxodG as molecular markers of cancer. Med Sci Monit. 17:CR329–CR333.
   PubMed Web of Science ®Google Scholar
• Santos CMM, Silva A. 2017. An overview of 2-styrylchromones: natural occurrence, synthesis, reactivity and biological properties. Eur J Org Chem. 2017:3115–3133.
   Google Scholar
• Song CW, Glatstein E, Marks LB, Emami B, Grimm J, Sperduto PW, Kim MS, Hui S, Dusenbery KE, Cho LC. 2019. Biological principles of stereotactic body radiation therapy (SBRT) and stereotactic radiation surgery (SRS): indirect cell death. Int J Radiat Oncol Biol Phys. In press [PMID: 30836165].
   Google Scholar
• Song CW, Kim MS, Cho LC, Dusenbery K, Sperduto PW. 2014. Radiobiological basis of SBRT and SRS. Int J Clin Oncol. 19:570–578.
   PubMed Web of Science ®Google Scholar
• Sun X, Wang Q, Wang Y, Du L, Xu C, Liu Q. 2016. Brusatol enhances the radiosensitivity of A549 cells by promoting ROS production and enhancing DNA damage. Int J Mol Sci. 17:997.
   Web of Science ®Google Scholar
• Supuran CT, Casini A, Scozzafava A. 2003. Protease inhibitors of the sulfonamide type: anticancer, antiinflammatory, and antiviral agents. Med Res Rev. 23:535–558.
   PubMed Web of Science ®Google Scholar
• Takemura T, Shinomiya N, Rokutanda M. 1998. G2/M is a critical phase to regulate X-ray-induced apoptosis in EL-4 mouse lymphoma cells. Ann Cancer Res Ther. 7:101–107.
   Google Scholar
• Tang JY, Wu CY, Shu CW, Wang SC, Chang MY, Chang HW. 2018. A novel sulfonyl chromen-4-ones (CHW09) preferentially kills oral cancer cells showing apoptosis, oxidative stress, and DNA damage. Environ Toxicol. 33:1195–1203.
   PubMed Web of Science ®Google Scholar
• Tiwari P, Kumar A, Balakrishnan S, Kushwaha HS, Mishra KP. 2011. Silibinin-induced apoptosis in MCF7 and T47D human breast carcinoma cells involves caspase-8 activation and mitochondrial pathway. Cancer Invest. 29:12–20.
   PubMed Web of Science ®Google Scholar
• Trachootham D, Alexandre J, Huang P. 2009. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov. 8:579–591.
   PubMed Web of Science ®Google Scholar
• Vaidya JS, Wenz F, Bulsara M, Tobias JS, Joseph DJ, Keshtgar M, Flyger HL, Massarut S, Alvarado M, Saunders C, group Tt, et al. 2014. Risk-adapted targeted intraoperative radiotherapy versus whole-breast radiotherapy for breast cancer: 5-year results for local control and overall survival from the TARGIT-A randomised trial. Lancet. 383:603–613.
   PubMed Web of Science ®Google Scholar
• Valdameri G, Genoux-Bastide E, Peres B, Gauthier C, Guitton J, Terreux R, Winnischofer SM, Rocha ME, Boumendjel A, Di Pietro A. 2012. Substituted chromones as highly potent nontoxic inhibitors, specific for the breast cancer resistance protein. J Med Chem. 55:966–970.
   PubMed Web of Science ®Google Scholar
• Vignon C, Debeissat C, Georget MT, Bouscary D, Gyan E, Rosset P, Herault O. 2013. Flow cytometric quantification of all phases of the cell cycle and apoptosis in a two-color fluorescence plot. PLoS One. 8:e68425.
   PubMed Web of Science ®Google Scholar
• Von Sonntag C. 1987. The chemical basis of radiation biology. London: Taylor & Francis.
   Google Scholar
• Wlodkowic D, Skommer J, Darzynkiewicz Z. 2009. Flow cytometry-based apoptosis detection. Methods Mol Biol. 559:19–32.
   PubMedGoogle Scholar
• Yamamori T, Yasui H, Yamazumi M, Wada Y, Nakamura Y, Nakamura H, Inanami O. 2012. Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med. 53:260–270.
   PubMed Web of Science ®Google Scholar
• Yang ES, Choi MJ, Kim JH, Choi KS, Kwon TK. 2011. Combination of withaferin A and X-ray irradiation enhances apoptosis in U937 cells. Toxicol in Vitro. 25:1803–1810.
   PubMed Web of Science ®Google Scholar
• Yeh CC, Tseng CN, Yang JI, Huang HW, Fang Y, Tang JY, Chang FR, Chang HW. 2012. Antiproliferation and induction of apoptosis in Ca9-22 oral cancer cells by ethanolic extract of Gracilaria tenuistipitata. Molecules. 17:10916–10927.
   PubMed Web of Science ®Google Scholar
• Yeh CC, Yang JI, Lee JC, Tseng CN, Chan YC, Hseu YC, Tang JY, Chuang LY, Huang HW, Chang FR, et al. 2012. Anti-proliferative effect of methanolic extract of Gracilaria tenuistipitata on oral cancer cells involves apoptosis, DNA damage, and oxidative stress. BMC Complement Altern Med. 12:142.
   PubMed Web of Science ®Google Scholar
• Yen CY, Chiu CC, Haung RW, Yeh CC, Huang KJ, Chang KF, Hseu YC, Chang FR, Chang HW, Wu YC. 2012. Antiproliferative effects of goniothalamin on Ca9-22 oral cancer cells through apoptosis, DNA damage and ROS induction. Mutat Res. 747:253–258.
   PubMed Web of Science ®Google Scholar
• Yen CY, Hou MF, Yang ZW, Tang JY, Li KT, Huang HW, Huang YH, Lee SY, Fu TF, Hsieh CY, et al. 2015. Concentration effects of grape seed extracts in anti-oral cancer cells involving differential apoptosis, oxidative stress, and DNA damage. BMC Complement Altern Med. 15:94.
   PubMed Web of Science ®Google Scholar
• Yen YH, Farooqi AA, Li KT, Butt G, Tang JY, Wu CY, Cheng YB, Hou MF, Chang HW. 2014. Methanolic extracts of Solieria robusta inhibits proliferation of oral cancer Ca9-22 cells via apoptosis and oxidative stress. Molecules. 19:18721–18732.
   PubMed Web of Science ®Google Scholar
• Zhao H, Zhuang Y, Li R, Liu Y, Mei Z, He Z, Zhou F, Zhou Y. 2019. Effects of different doses of X-ray irradiation on cell apoptosis, cell cycle, DNA damage repair and glycolysis in HeLa cells. Oncol Lett. 17:42–54.
   PubMed Web of Science ®Google Scholar
• Zou ZW, Liu T, Li Y, Chen P, Peng X, Ma C, Zhang WJ, Li PD. 2018. Melatonin suppresses thyroid cancer growth and overcomes radioresistance via inhibition of p65 phosphorylation and induction of ROS. Redox Biol. 16:226–236.
   PubMed Web of Science ®Google Scholar