Antitumor Activity of Berberine by Activating Autophagy and Apoptosis in CAL-62 and BHT-101 Anaplastic Thyroid Carcinoma Cell Lines

References

• Chen W, Zheng R, Zhang S, et al. Cancer incidence and mortality in China in 2013: an analysis based on urbanization level. Chin J Cancer Res. 2017;29(1):1–10.
   PubMed Web of Science ®Google Scholar
• Deeken-Draisey A, Yang GY, Gao J, Alexiev BA. Anaplastic thyroid carcinoma: an epidemiologic, histologic, immunohistochemical, and molecular single-institution study. Hum Pathol. 2018;82:140–148.
   PubMed Web of Science ®Google Scholar
• Kim JH, Leeper RD. Treatment of anaplastic giant and spindle cell carcinoma of the thyroid gland with combination Adriamycin and radiation therapy. A new approach. Cancer. 1983;52(6):954–957.
   PubMed Web of Science ®Google Scholar
• Ranganath R, Shah MA, Shah AR. Anaplastic thyroid cancer, Current opinion in endocrinology. Diabetes Obes. 2015;22(5):387–391.
   Google Scholar
• Liu C, Yang S, Wang K, et al. Alkaloids from traditional Chinese medicine against hepatocellular carcinoma. Biomed Pharmacother. 2019;120:109543.
   PubMed Web of Science ®Google Scholar
• Qi F, Zhao L, Zhou A, et al. The advantages of using traditional Chinese medicine as an adjunctive therapy in the whole course of cancer treatment instead of only terminal stage of cancer. Biosci Trends. 2015;9:16–34.
   PubMed Web of Science ®Google Scholar
• Tan HL, Chan KG, Pusparajah P, et al. Rhizoma coptidis: a potential cardiovascular protective agent. FronPharmacol. 2016;7:362.
   Google Scholar
• Tabeshpour J, Imenshahidi M, Hosseinzadeh H. A review of the effects of Berberis vulgaris and its major component, berberine, in metabolic syndrome. Iran J Basic Med Sci. 2017;20(5):557–568.
   PubMed Web of Science ®Google Scholar
• Zou K, Li Z, Zhang Y, et al. Advances in the study of berberine and its derivatives: a focus on anti-inflammatory and anti-tumor effects in the digestive system. Acta Pharmacol Sin. 2017;38(2):157–167.
   PubMed Web of Science ®Google Scholar
• Gong C, Hu X, Xu Y, et al. Berberine inhibits proliferation and migration of colorectal cancer cells by downregulation of GRP78. Anticancer Drugs. 2020;31:141–149.
   PubMed Web of Science ®Google Scholar
• Li D, Zhang Y, Liu K, et al. Berberine inhibits colitis-associated tumorigenesis via suppressing inflammatory responses and the consequent EGFR signaling-involved tumor cell growth. Lab Invest. 2017;97(1):1343–1353.
   PubMedGoogle Scholar
• Li L, Wang X, Sharvan R, Gao J, Qu S. Berberine could inhibit thyroid carcinoma cells by inducing mitochondrial apoptosis, G0/G1 cell cycle arrest and suppressing migration via PI3K-AKT and MAPK signaling pathways. Biomed Pharmacother. 2017;95:1225–1231.
   PubMed Web of Science ®Google Scholar
• Park KS, Kim JB, Bae J, et al. Berberine inhibited the growth of thyroid cancer cell lines 8505C and TPC1. Yonsei Med J. 2012;53(2):346–351.
   PubMed Web of Science ®Google Scholar
• Levy JMM, Towers CG, Thorburn A. Targeting autophagy in cancer. Nat Rev Cancer. 2017;17(9):528–542.
   PubMed Web of Science ®Google Scholar
• Singh SS, Vats S, Chia AY, et al. Dual role of autophagy in hallmarks of cancer. Oncogene. 2018;37(9):1142–1158.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Wang X, Cao S, et al. Berberine represses human gastric cancer cell growth in vitro and in vivo by inducing cytostatic autophagy via inhibition of MAPK/mTOR/p70S6K and Akt signaling pathways. Biomed Pharmacother. 2020;128:110245.
   PubMed Web of Science ®Google Scholar
• Liu J, Liu P, Xu T, et al. Berberine induces autophagic cell death in acute lymphoblastic leukemia by inactivating AKT/mTORC1 signaling. Drug Des Devel Ther. 2020;14:1813–1823.
   PubMed Web of Science ®Google Scholar
• Wang Y, Liu Y, Du X, Ma H, Yao J. Berberine reverses doxorubicin resistance by inhibiting autophagy through the PTEN/Akt/mTOR signaling pathway in breast cancer. Onco Targets Ther. 2020;13:1909–1919.
   PubMed Web of Science ®Google Scholar
• Wang H, Dong R, Fan WW, Zheng XC, Li AM, Wang WD. Timosaponin A-III induces autophagy of T-cell acute lymphoblastic leukemia Jurkat cells via inhibition of the PI3K/Akt/mTOR pathway. Oncol Rep. 2019;41(5):2937–2944.
   PubMed Web of Science ®Google Scholar
• Fan XJ, Wang Y, Wang L, Zhu M. Salidroside induces apoptosis and autophagy in human colorectal cancer cells through inhibition of PI3K/Akt/mTOR pathway. Oncol Rep. 2016;36(6):3559–3567.
   PubMed Web of Science ®Google Scholar
• Saji M, Ringel MD. The PI3K-Akt-mTOR pathway in initiation and progression of thyroid tumors. Mol Cell Endocrinol. 2010;321(1):20–28.
   PubMed Web of Science ®Google Scholar
• Petrulea MS, Plantinga TS, Smit JW, Georgescu CE, Netea-Maier RT. PI3K/Akt/mTOR: a promising therapeutic target for non-medullary thyroid carcinoma. Cancer Treat Rev. 2015;41(8):707–713.
   PubMed Web of Science ®Google Scholar
• Haddad RI, Lydiatt WM, Ball DW, et al. Anaplastic thyroid carcinoma, version 2.2015. J Natl Compr Can Netw. 2015;13(9):1140–1150.
   PubMed Web of Science ®Google Scholar
• Mittal A, Tabasum S, Singh RP. Berberine in combination with doxorubicin suppresses growth of murine melanoma B16F10 cells in culture and xenograft. Phytomedicine. 2014;21(3):340–347.
   PubMed Web of Science ®Google Scholar
• Tong N, Zhang J, Chen Y, et al. Berberine sensitizes multiple human cancer cells to the anticancer effects of doxorubicin in vitro. Oncol Lett. 2012;3(6):1263–1267.
   PubMed Web of Science ®Google Scholar
• Xiong C, Wu YZ, Zhang Y, et al. Protective effect of berberine on acute cardiomyopathy associated with doxorubicin treatment. Oncol Lett. 2018;15(4):5721–5729.
   PubMed Web of Science ®Google Scholar
• Wu YZ, Zhang L, Wu ZX, Shan TT, Xiong C. Berberine ameliorates doxorubicin-induced cardiotoxicity via a SIRT1/p66Shc-mediated pathway. Oxid Med Cell Longev. 2019;2019:2150394.
   PubMed Web of Science ®Google Scholar
• Cohen GM. Caspases: the executioners of apoptosis. Biochem J. 1997;326(Pt 1):1–16.
   PubMed Web of Science ®Google Scholar
• Mohammadinejad R, Ahmadi Z, Tavakol S, Ashrafizadeh M. Berberine as a potential autophagy modulator. J Cell Physiol. 2019;2019:1.
   Google Scholar
• Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1. Autophagy. 2021;17(1):1–382.
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282(33):24131–24145.
   PubMed Web of Science ®Google Scholar
• Wan X, Harkavy B, Shen N, Grohar P, Helman LJ. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene. 2007;26:1932–1940.
   PubMed Web of Science ®Google Scholar
• Fang J, Huang X, Yang Y, Wang X, Liang X, Liu J. Berberine-photodynamic induced apoptosis by activating endoplasmic reticulum stress-autophagy pathway involving CHOP in human malignant melanoma cells. Biochem Biophys Res Commun. 2021;552:183–190.
   PubMed Web of Science ®Google Scholar
• Kim SY, Hwangbo H, Kim MY, et al. Coptisine induces autophagic cell death through down-regulation of PI3K/Akt/mTOR signaling pathway and up-regulation of ROS-mediated mitochondrial dysfunction in hepatocellular carcinoma Hep3B cells. Arch Biochem Biophys. 2021;697:108688.
   PubMed Web of Science ®Google Scholar
• Liu JZ, Hu YL, Feng Y, et al. BDH2 triggers ROS-induced cell death and autophagy by promoting Nrf2 ubiquitination in gastric cancer. J Exp Clin Cancer Res. 2020;39(1):123.
   PubMed Web of Science ®Google Scholar
• Wen C, Wang H, Wu X, et al. ROS-mediated inactivation of the PI3K/AKT pathway is involved in the antigastric cancer effects of thioredoxin reductase-1 inhibitor chaetocin. Cell Death Dis. 2019;10(11):809.
   PubMedGoogle Scholar
• Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul. 1984;22:27–55.
   PubMedGoogle Scholar
• Liu D, Meng X, Wu D, Qiu Z, Luo H. Anaturalisoquinolinealkaloidwith antitumor activity: studies of the biological activities of berberine. FrontPharmacol. 2019;10:9.
   Google Scholar
• Gao X, Wang J, Li M, et al. Berberine attenuates XRCC1-mediated base excision repair and sensitizes breast cancer cells to the chemotherapeutic drugs. J Cell Mol Med. 2019;23(10):6797–6804.
   PubMed Web of Science ®Google Scholar
• Palmieri A, Iapichino A, Cura F, et al. Pre-treatment with berberine enhances effect of 5-fluorouracil and cisplatin in HEP2 laryngeal cancer cell line. J Biol Regul Homeost Agents. 2018;32(2 Suppl. 1):167–177.
   PubMed Web of Science ®Google Scholar
• Kumar A, Chopra K, Mukherjee M, Pottabathini R, Dhull DK. Current knowledge and pharmacological profile of berberine: an update. Eur J Pharmacol. 2015;761:288–297.
   PubMed Web of Science ®Google Scholar
• Wang K, Zhang C, Bao J, et al. Synergistic chemopreventive effects of curcumin and berberine on human breast cancer cells through induction of apoptosis and autophagic cell death. Sci Rep. 2016;6:26064.
   PubMed Web of Science ®Google Scholar
• Meng M, Geng S, Du Z, et al. Berberine and cinnamaldehyde together prevent lung carcinogenesis. Oncotarget. 2017;8(44):76385–76397.
   PubMedGoogle Scholar
• Moscat J, Karin M, Diaz-Meco MT. p62 in cancer: signaling adaptor beyond autophagy. Cell. 2016;167(3):606–609.
   PubMed Web of Science ®Google Scholar
• Pan T, Rawal P, Wu Y, Xie W, Jankovic J, Le W. Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience. 2009;164(2):541–551.
   PubMed Web of Science ®Google Scholar
• Xing M. Genetic alterations in the phosphatidylinositol-3 kinase/Akt pathway in thyroid cancer. Thyroid. 2010;20(7):697–706.
   PubMed Web of Science ®Google Scholar
• Hyun MS, Hur JM, Mun YJ, Kim D, Woo WH. BBR induces apoptosis in HepG2 cell through an Akt-ASK1-ROS-p38MAPKs-linked cascade. J Cell Biochem. 2010;109(2):329–338.
   PubMed Web of Science ®Google Scholar
• Eo SH, Kim JH, Kim SJ. Induction of G(2)/M arrest by berberine via activation of PI3K/Akt and p38 in human chondrosarcoma cell line. Oncol Res. 2014;22(3):147–157.
   PubMed Web of Science ®Google Scholar
• Smallridge RC, Ain KB, Asa SL, et al. American thyroid association guidelines for management of patients with anaplastic thyroid cancer. Thyroid. 2012;22(11):1104–1139.
   PubMed Web of Science ®Google Scholar
• Almatroodi SA, Alsahli MA, Rahmani AH. Berberine: an important emphasis on its anticancer effects through modulation of various cell signaling pathways. Molecules. 2022;27:5889.
   PubMed Web of Science ®Google Scholar
• Yi T, Zhuang L, Song G, Zhang B, Li G, Hu T. Akt signaling is associated with the berberine-induced apoptosis of human gastric cancer cells. Nutr Cancer. 2015;67:523–531.
   PubMed Web of Science ®Google Scholar
• Kim HS, Kim MJ, Kim EJ, Yang Y, Lee MS, Lim JS. Berberine-induced AMPK activation inhibits the metastatic potential of melanoma cells via reduction of ERK activity and COX-2 protein expression. Biochem Pharmacol. 2012;83:385–394.
   PubMed Web of Science ®Google Scholar
• Sun S, Zhang X, Xu M, et al. Berberine downregulates CDC6and inhibits proliferation via targeting JAK-STAT3 signaling in keratinocytes. Cell Death Dis. 2019;10:274.
   PubMed Web of Science ®Google Scholar