Corilagin induces apoptosis and autophagy in NRF2‑addicted U251 glioma cell line
- Authors:
- Jilan Liu
- Xianyun Qin
- Wenyuan Ma
- Shu Jia
- Xiaobei Zhang
- Xinlin Yang
- Dongfeng Pan
- Feng Jin
-
Affiliations: Department of Central Laboratory, Affiliated Hospital of Jining Medical University, Jining, Shandong 272029, P.R. China, Department of Neurosurgery, Affiliated Hospital of Jining Medical University, Jining, Shandong 272029, P.R. China, Department of Orthopaedic Surgery, Orthopaedic Research Labs, University of Virginia, Charlottesville, VA 22908, USA, Department of Radiology and Medical Imaging, University of Virginia, Charlottesville, VA 22908, USA - Published online on: March 5, 2021 https://doi.org/10.3892/mmr.2021.11959
- Article Number: 320
-
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Chen R, Smith-Cohn M, Cohen AL and Colman H: Glioma subclassifications and their clinical significance. Neurotherapeutics. 14:284–297. 2017. View Article : Google Scholar : PubMed/NCBI | |
Delgado-Lopez PD, Corrales-Garcia EM, Martino J, Lastra-Aras E and Duenas-Polo MT: Diffuse low-grade glioma: A review on the new molecular classification, natural history and current management strategies. Clin Transl Oncol. 19:931–944. 2017. View Article : Google Scholar : PubMed/NCBI | |
Duffau H and Taillandier L: New concepts in the management of diffuse low-grade glioma: Proposal of a multistage and individualized therapeutic approach. Neuro Oncol. 17:332–342. 2015.PubMed/NCBI | |
Chen X, Zhang M, Gan H, Wang H, Lee JH, Fang D, Kitange GJ, He L, Hu Z, Parney IF, et al: A novel enhancer regulates MGMT expression and promotes temozolomide resistance in glioblastoma. Nat Commun. 9:29492018. View Article : Google Scholar : PubMed/NCBI | |
Schmidt OT and Lademann R: Corilagin, ein weiterer kristallisierter Gerbstoff aus Dividivi. X. Mitteilung über natürliche Gerbstoffe. Justus Liebigs Ann Chem. 571:232–237. 1951. View Article : Google Scholar | |
Kakiuchi N, Hattori M, Namba T, Nishizawa M, Yamagishi T and Okuda T: Inhibitory effect of tannins on reverse transcriptase from RNA tumor virus. J Nat Prod. 48:614–621. 1985. View Article : Google Scholar : PubMed/NCBI | |
Qiu F, Liu L, Lin Y, Yang Z and Qiu F: Corilagin inhibits esophageal squamous cell carcinoma by inducing DNA damage and down-regulation of RNF8. Anticancer Agents Med Chem. 19:1021–1028. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ding Y, Ren D, Xu H, Liu W, Liu T, Li L, Li J, Li Y and Wen A: Antioxidant and pro-angiogenic effects of corilagin in rat cerebral ischemia via Nrf2 activation. Oncotarget. 8:114816–114828. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu FC, Chaudry IH and Yu HP: Hepatoprotective effects of corilagin following hemorrhagic shock are through akt-dependent pathway. Shock. 47:346–345. 2017. View Article : Google Scholar : PubMed/NCBI | |
Guo S, Fu Y, Xiong S and Lv J: Corilagin protects the acute lung injury by ameliorating the apoptosis pathway. Biomed Pharmacother. 95:1743–1748. 2017. View Article : Google Scholar : PubMed/NCBI | |
Li HR, Liu J, Zhang SL, Luo T, Wu F, Dong JH, Guo YJ and Zhao L: Corilagin ameliorates the extreme inflammatory status in sepsis through TLR4 signaling pathways. BMC Complement Altern Med. 17:182017. View Article : Google Scholar : PubMed/NCBI | |
Xu J, Zhang G, Tong Y, Yuan J, Li Y and Song G: Corilagin induces apoptosis, autophagy and ROS generation in gastric cancer cells in vitro. Int J Mol Med. 43:967–979. 2019.PubMed/NCBI | |
Deng Y, Li X, Li X, Zheng Z, Huang W, Chen L, Tong Q and Ming Y: Corilagin induces the apoptosis of hepatocellular carcinoma cells through the mitochondrial apoptotic and death receptor pathways. Oncol Rep. 39:2545–2552. 2018.PubMed/NCBI | |
Tong Y, Zhang G, Li Y, Xu J, Yuan J, Zhang B, Hu T and Song G: Corilagin inhibits breast cancer growth via reactive oxygen species-dependent apoptosis and autophagy. J Cell Mol Med Jun. 22:3795–3807. 2018. View Article : Google Scholar | |
Li N, Lin Z, Chen W, Zheng Y, Ming Y, Zheng Z, Huang W, Chen L, Xiao J and Lin H: Corilagin from longan seed: Identification, quantification, and synergistic cytotoxicity on SKOv3ip and hey cells with ginsenoside Rh2 and 5-fluorouracil. Food Chem Toxicol. 119:133–140. 2018. View Article : Google Scholar : PubMed/NCBI | |
Milani R, Brognara E, Fabbri E, Finotti A, Borgatti M, Lampronti I, Marzaro G, Chilin A, Lee KK, Kok SH, et al: Corilagin induces high levels of apoptosis in the temozolomide-resistant T98G glioma cell line. Oncol Res. 26:1307–1315. 2018. View Article : Google Scholar : PubMed/NCBI | |
Noguchi M, Hirata N, Tanaka T, Suizu F, Nakajima H and Chiorini JA: Autophagy as a modulator of cell death machinery. Cell Death Dis. 11:5172020. View Article : Google Scholar : PubMed/NCBI | |
Choi AM, Ryter SW and Levine B: Autophagy in human health and disease. N Engl J Med. 368:651–662. 2013. View Article : Google Scholar : PubMed/NCBI | |
Baechler BL, Bloemberg D and Quadrilatero J: Mitophagy regulates mitochondrial network signaling, oxidative stress, and apoptosis during myoblast differentiation. Autophagy. 15:1606–1619. 2019. View Article : Google Scholar : PubMed/NCBI | |
Jiang P and Mizushima N: LC3- and p62-based biochemical methods for the analysis of autophagy progression in mammalian cells. Methods. 75:13–18. 2015. View Article : Google Scholar : PubMed/NCBI | |
He F, Ru X and Wen T: NRF2, a transcription factor for stress response and beyond. Int J Mol Sci. 21:47772020. View Article : Google Scholar | |
Baird L and Yamamoto M: The molecular mechanisms regulating the KEAP1-NRF2 pathway. Mol Cell Biol. 40:e00099-20. 2020. View Article : Google Scholar | |
Unoki T, Akiyama M and Kumagai Y: Nrf2 activation and its coordination with the protective defense systems in response to electrophilic stress. Int J Mol Sci. 21:5452020. View Article : Google Scholar | |
Menegon S, Columbano A and Giordano S: The dual roles of NRF2 in cancer. Trends Mol Med. 22:578–593. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhao Q, Mao A, Yan J, Sun C, Di C, Zhou X, Li H, Guo R and Zhang H: Downregulation of Nrf2 promotes radiation-induced apoptosis through Nrf2 mediated Notch signaling in non-small cell lung cancer cells. Int J Oncol. 48:765–773. 2016. View Article : Google Scholar : PubMed/NCBI | |
Meng QT, Chen R, Chen C, Su K, Li W, Tang LH, Liu HM, Xue R, Sun Q, Leng Y, et al: Transcription factors Nrf2 and NF-kappaB contribute to inflammation and apoptosis induced by intestinal ischemia-reperfusion in mice. Int J Mol Med. 40:1731–1740. 2017.PubMed/NCBI | |
Wan ZH, Jiang TY, Shi YY, Pan YF, Lin YK, Ma YH, Yang C, Feng XF, Huang LF, Kong XN, et al: RPB5-mediating protein promotes cholangiocarcinoma tumorigenesis and drug resistance by competing with NRF2 for KEAP1 binding. Hepatology. 71:2005–2022. 2020. View Article : Google Scholar : PubMed/NCBI | |
Kitamura H and Motohashi H: NRF2 addiction in cancer cells. Cancer Sci. 109:900–911. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ji XJ, Chen SH, Zhu L, Pan H, Zhou Y, Li W, You WC, Gao CC, Zhu JH, Jiang K, et al: Knockdown of NF-E2-related factor 2 inhibits the proliferation and growth of U251MG human glioma cells in a mouse xenograft model. Oncol Rep. 30:157–164. 2013. View Article : Google Scholar : PubMed/NCBI | |
Taguchi K and Yamamoto M: The KEAP1-NRF2 System in Cancer. Front Oncol. 7:852017. View Article : Google Scholar : PubMed/NCBI | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
Tang Z, Li C, Kang B, Gao G, Li C and Zhang Z: GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 45:W98–W102. 2017. View Article : Google Scholar : PubMed/NCBI | |
Yang WT, Li GH, Li ZY, Feng S, Liu XQ, Han GK, Zhang H, Qin XY, Zhang R, Nie QM, et al: Effect of corilagin on the proliferation and NF-κB in U251 glioblastoma cells and U251 glioblastoma stem-like cells. Evid Based Complement Alternat Med. 2016:14183092016. View Article : Google Scholar : PubMed/NCBI | |
Basso J, Miranda A, Sousa J, Pais A and Vitorino C: Repurposing drugs for glioblastoma: From bench to bedside. Cancer Lett. 428:173–183. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hau DK, Zhu GY, Leung AK, Wong RS, Cheng GY, Lai PB, Tong SW, Lau FY, Chan KW, Wong WY, et al: In vivo anti-tumour activity of corilagin on Hep3B hepatocellular carcinoma. Phytomedicine. 18:11–15. 2010. View Article : Google Scholar : PubMed/NCBI | |
Pham AT, Malterud KE, Paulsen BS, Diallo D and Wangensteen H: DPPH radical scavenging and xanthine oxidase inhibitory activity of Terminalia macroptera leaves. Nat Prod Commun. 6:1125–1128. 2011.PubMed/NCBI | |
Gaudreault R and Mousseau N: Mitigating Alzheimer's disease with natural polyphenols: A review. Curr Alzheimer Res. 16:529–543. 2019. View Article : Google Scholar : PubMed/NCBI | |
Moraes LS, Donza MR, Rodrigues AP, Silva BJ, Brasil DS, Zoghbi M, Andrade EH, Guilhon GM and Silva EO: Leishmanicidal activity of (+)-phyllanthidine and the phytochemical profile of Margaritaria nobilis (Phyllanthaceae). Molecules. 20:22157–22169. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Xu D, Sun A, Ho SL, Poon CY, Chan HN, Ng OT, Yung KK, Yan H, Li HW, et al: Fluoro-substituted cyanine for reliable in vivo labelling of amyloid-β oligomers and neuroprotection against amyloid-β induced toxicity. Chem Sci. 8:8279–8284. 2017. View Article : Google Scholar : PubMed/NCBI | |
Adesina SK, Idowu O, Ogundaini AO, Oladimeji H, Olugbade TA, Onawunmi GO and Pais M: Antimicrobial constituents of the leaves of Acalypha wilkesiana and Aacalypha hispida. Phytother Res. 14:371–374. 2000. View Article : Google Scholar : PubMed/NCBI | |
Yeo SG, Song JH, Hong EH, Lee BR, Kwon YS, Chang SY, Kim SH, Lee SW, Park JH and Ko HJ: Antiviral effects of Phyllanthus urinaria containing corilagin against human enterovirus 71 and Coxsackievirus A16 in vitro. Arch Pharm Res. 38:193–202. 2015. View Article : Google Scholar : PubMed/NCBI | |
Burapadaja S and Bunchoo A: Antimicrobial activity of tannins from Terminalia citrina. Planta Med. 61:365–366. 1995. View Article : Google Scholar : PubMed/NCBI | |
Teodoro GR, Brighenti FL, Delbem AC, Delbem ÁC, Khouri S, Gontijo AV, Pascoal AC, Salvador MJ and Koga-Ito CY: Antifungal activity of extracts and isolated compounds from Buchenavia tomentosa on Candida albicans and non-albicans. Future Microbiol. 10:917–927. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li X, Deng Y, Zheng Z, Huang W, Chen L, Tong Q and Ming Y: Corilagin, a promising medicinal herbal agent. Biomed Pharmacother. 99:43–50. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guo YJ, Luo T, Wu F, Liu H, Li HR, Mei YW, Zhang SL, Tao JY, Dong JH, Fang Y, et al: Corilagin protects against HSV1 encephalitis through inhibiting the TLR2 signaling pathways in vivo and in vitro. Mol Neurobiol. 52:1547–1560. 2015. View Article : Google Scholar : PubMed/NCBI | |
Komori A, Yatsunami J, Suganuma M, Okabe S, Abe S, Sakai A, Sasaki K and Fujiki H: Tumor necrosis factor acts as a tumor promoter in BALB/3T3 cell transformation. Cancer Res. 53:1982–1985. 1993.PubMed/NCBI | |
Okabe S, Suganuma M, Imayoshi Y, Taniguchi S, Yoshida T and Fujiki H: New TNF-alpha releasing inhibitors, geraniin and corilagin, in leaves of Acer nikoense, Megusurino-ki. Biol Pharm Bull. 24:1145–1148. 2001. View Article : Google Scholar : PubMed/NCBI | |
Tong F, Zhang J, Liu L, Gao X, Cai Q, Wei C, Dong J, Hu Y, Wu G and Dong X: Corilagin attenuates radiation-induced brain injury in mice. Mol Neurobiol. 53:6982–6996. 2016. View Article : Google Scholar : PubMed/NCBI | |
Lu MC, Ji JA, Jiang ZY and You QD: The Keap1-Nrf2-ARE pathway as a potential preventive and therapeutic target: An update. Med Res Rev. 36:924–963. 2016. View Article : Google Scholar : PubMed/NCBI | |
Chen HH, Chang HH, Chang JY, Tang YC, Cheng YC, Lin LM, Cheng SY, Huang CH, Sun MW, Chen CT, et al: Enhanced B-Raf-mediated NRF2 gene transcription and HATs-mediated NRF2 protein acetylation contributes to ABCC1-mediated chemoresistance and glutathione-mediated survival in acquired topoisomerase II poison-resistant cancer cells. Free Radic Biol Med. 113:505–518. 2017. View Article : Google Scholar : PubMed/NCBI | |
Beidler DR, Chang JY, Zhou BS and Cheng YC: Camptothecin resistance involving steps subsequent to the formation of protein-linked DNA breaks in human camptothecin-resistant KB cell lines. Cancer Res. 56:345–353. 1996.PubMed/NCBI | |
Ferguson PJ, Fisher MH, Stephenson J, Li DH, Zhou BS and Cheng YC: Combined modalities of resistance in etoposide-resistant human KB cell lines. Cancer Res. 48:5956–5964. 1988.PubMed/NCBI | |
Xu B, Wang S, Li R, Chen K, He L, Deng M, Kannappan V, Zha J, Dong H and Wang W: Disulfiram/copper selectively eradicates AML leukemia stem cells in vitro and in vivo by simultaneous induction of ROS-JNK and inhibition of NF-κB and Nrf2. Cell Death Dis. 8:e27972017. View Article : Google Scholar : PubMed/NCBI | |
Yang F, Wang Y, Xue J, Ma Q, Zhang J, Chen YF, Shang ZZ, Li QQ, Zhang SL and Zhao L: Effect of Corilagin on the miR-21/smad7/ERK signaling pathway in a schistosomiasis-induced hepatic fibrosis mouse model. Parasitol Int. 65:308–315. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhou X, Xiong J, Lu S, Luo L, Chen ZL, Yang F, Jin F, Wang Y, Ma Q, Luo YY, et al: Inhibitory effect of corilagin on miR-21-regulated hepatic fibrosis signaling pathway. Am J Chin Med. 47:1541–1569. 2019. View Article : Google Scholar : PubMed/NCBI | |
Rami A and Kögel D: Apoptosis meets autophagy-like cell death in the ischemic penumbra: Two sides of the same coin? Autophagy. 4:422–426. 2008. View Article : Google Scholar : PubMed/NCBI | |
Siddiqui WA, Ahad A and Ahsan H: The mystery of BCL2 family: Bcl-2 proteins and apoptosis: an update. Arch Toxicol. 89:289–317. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yousefi S, Perozzo R, Schmid I, Ziemiecki A, Schaffner T, Scapozza L, Brunner T and Simon HU: Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat Cell Biol. 8:1124–1132. 2006. View Article : Google Scholar : PubMed/NCBI | |
Booth LA, Tavallai S, Hamed HA, Cruickshanks N and Dent P: The role of cell signalling in the crosstalk between autophagy and apoptosis. Cell Signal. 26:549–555. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang Z and Guo S: Nrf2/HO-1 mediates the neuroprotective effect of mangiferin on early brain injury after subarachnoid hemorrhage by attenuating mitochondria-related apoptosis and neuroinflammation. Sci Rep. 7:118832017. View Article : Google Scholar : PubMed/NCBI | |
Wu J, Zhang L, Li H, Wu S and Liu Z: Nrf2 induced cisplatin resistance in ovarian cancer by promoting CD99 expression. Biochem Biophys Res Commun. 518:698–705. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liu P, Rojo de la Vega M, Sammani S, Mascarenhas JB, Kerins M, Dodson M, Sun X, Wang T, Ooi A, Garcia JG, et al: RPA1 binding to NRF2 switches ARE-dependent transcriptional activation to ARE-NRE-dependent repression. Proc Natl Acad Sci USA. 115:E10352–E10361. 2018. View Article : Google Scholar : PubMed/NCBI | |
Buendia I, Michalska P, Navarro E, Gameiro I, Egea J and León R: Nrf2-ARE pathway: An emerging target against oxidative stress and neuroinflammation in neurodegenerative diseases. Pharmacol Ther. 157:84–104. 2016. View Article : Google Scholar : PubMed/NCBI | |
Shaw P and Chattopadhyay A: Nrf2-ARE signaling in cellular protection: Mechanism of action and the regulatory mechanisms. J Cell Physiol. 235:3119–3130. 2020. View Article : Google Scholar : PubMed/NCBI | |
Jiang T, Harder B, Rojo de la Vega M, Wong PK, Chapman E and Zhang DD: p62 links autophagy and Nrf2 signaling. Free Radic Biol Med. 88:199–204. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chen RH, Chen YH and Huang TY: Ubiquitin-mediated regulation of autophagy. J Biomed Sci. 26:802019. View Article : Google Scholar : PubMed/NCBI | |
Narayanan S, Cai CY, Assaraf YG, Guo HQ, Cui Q, Wei L, Huang JJ, Ashby CR Jr and Chen ZS: Targeting the ubiquitin-proteasome pathway to overcome anti-cancer drug resistance. Drug Resist Updat. 48:1006632020. View Article : Google Scholar : PubMed/NCBI | |
Im E, Yoon JB, Lee HW and Chung KC: Human telomerase reverse transcriptase (hTERT) positively regulates 26S proteasome activity. J Cell Physiol. 232:2083–2093. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lokireddy S, Kukushkin NV and Goldberg AL: cAMP-induced phosphorylation of 26S proteasomes on Rpn6/PSMD11 enhances their activity and the degradation of misfolded proteins. Proc Natl Acad Sci USA. 112:E7176–E7185. 2015. View Article : Google Scholar : PubMed/NCBI | |
Roh JL, Kim EH, Jang H and Shin D: Nrf2 inhibition reverses the resistance of cisplatin-resistant head and neck cancer cells to artesunate-induced ferroptosis. Redox Biol. 11:254–262. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Mandal AK, Son YO, Pratheeshkumar P, Wise JT, Wang L, Zhang Z, Shi X and Chen Z: Roles of ROS, Nrf2, and autophagy in cadmium-carcinogenesis and its prevention by sulforaphane. Toxicol Appl Pharmacol. 353:23–30. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kovac S, Angelova PR, Holmström KM, Zhang Y, Dinkova-Kostova AT and Abramov AY: Nrf2 regulates ROS production by mitochondria and NADPH oxidase. Biochim Biophys Acta. 1850:794–801. 2015. View Article : Google Scholar : PubMed/NCBI |