Berberine Induces Autophagic Cell Death in Acute Lymphoblastic Leukemia by Inactivating AKT/mTORC1 Signaling

References

• JabbourE, O’BrienS, RavandiF, KantarjianH. Monoclonal antibodies in acute lymphoblastic leukemia. Blood. 2015;125(26):4010–4016. doi:10.1182/blood-2014-08-59640325999456
   PubMed Web of Science ®Google Scholar
• BhojwaniD, PuiCH. Relapsed childhood acute lymphoblastic leukaemia. Lancet Oncol. 2013;14(6):e205–e217. doi:10.1016/S1470-2045(12)70580-623639321
   PubMed Web of Science ®Google Scholar
• SimioniC, MartelliAM, ZauliG, MelloniE, NeriLM. Targeting mTOR in acute lymphoblastic leukemia. Cells. 2019;8(2):190. doi:10.3390/cells8020190
   PubMed Web of Science ®Google Scholar
• YilmazM, KantarjianH, JabbourE. Treatment of acute lymphoblastic leukemia in older adults: now and the future. Clin Adv Hematol Oncol. 2017;15(4):266–274.28591103
   PubMed Web of Science ®Google Scholar
• CrazzolaraR, BernhardD. CXCR4 chemokine receptors, histone deacetylase inhibitors and acute lymphoblastic leukemia. Leuk Lymphoma. 2005;46(11):1545–1551. doi:10.1080/1042819050021502716236608
   PubMed Web of Science ®Google Scholar
• InabaH, PuiCH. Glucocorticoid use in acute lymphoblastic leukaemia. Lancet Oncol. 2010;11(11):1096–1106. doi:10.1016/S1470-2045(10)70114-520947430
   PubMed Web of Science ®Google Scholar
• FengX, SuredaA, JafariS, et al. Berberine in cardiovascular and metabolic diseases: from mechanisms to therapeutics. Theranostics. 2019;9(7):1923–1951. doi:10.7150/thno.3078731037148
   PubMed Web of Science ®Google Scholar
• KongW, WeiJ, AbidiP, et al. Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med. 2004;10(12):1344–1351. doi:10.1038/nm113515531889
   PubMed Web of Science ®Google Scholar
• MisikV, BezakovaL, MalekovaL, KostalovaD. Lipoxygenase inhibition and antioxidant properties of protoberberine and aporphine alkaloids isolated from mahonia aquifolium. Planta Med. 1995;61(04):372–373. doi:10.1055/s-2006-9581077480190
   PubMed Web of Science ®Google Scholar
• LiangKW, TingCT, YinSC, et al. Berberine suppresses MEK/ERK-dependent Egr-1 signaling pathway and inhibits vascular smooth muscle cell regrowth after in vitro mechanical injury. Biochem Pharmacol. 2006;71(6):806–817. doi:10.1016/j.bcp.2005.12.02816448624
   PubMed Web of Science ®Google Scholar
• HuS, ChenCW, ChenST, et al. Inhibitory effect of berberine on interleukin-2 secretion from PHA-treated lymphocytic Jurkat cells. Int Immunopharmacol. 2019;66:267–273. doi:10.1016/j.intimp.2018.11.02030502647
   PubMed Web of Science ®Google Scholar
• LeeS, HallisSP, JungKA, RyuD, KwakMK. Impairment of HIF-1alpha-mediated metabolic adaption by NRF2-silencing in breast cancer cells. Redox Biol. 2019;24:101210. doi:10.1016/j.redox.2019.10121031078780
   PubMed Web of Science ®Google Scholar
• KumaA, HatanoM, MatsuiM, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004;432(7020):1032–1036. doi:10.1038/nature0302915525940
   PubMed Web of Science ®Google Scholar
• LiuX, ZhaoP, WangX, et al. Celastrol mediates autophagy and apoptosis via the ROS/JNK and Akt/mTOR signaling pathways in glioma cells. J Exp Clin Cancer Res. 2019;38(1):184. doi:10.1186/s13046-019-1173-431053160
   PubMed Web of Science ®Google Scholar
• BaiY, LiuX, QiX, et al. PDIA6 modulates apoptosis and autophagy of non-small cell lung cancer cells via the MAP4K1/JNK signaling pathway. EBioMedicine. 2019;42:311–325. doi:10.1016/j.ebiom.2019.03.04530922965
   PubMed Web of Science ®Google Scholar
• ZhangJ, ZhangN, LiangS, et al. The amounts and contributions of total drinking fluids and water from food to total water intake of young adults in Baoding, China. Eur J Nutr. 2018;58(7):2669–2677.30225629
   PubMed Web of Science ®Google Scholar
• WangH, DongR, FanWW, ZhengXC, LiAM, WangWD. Timosaponin AIII induces autophagy of Tcell acute lymphoblastic leukemia Jurkat cells via inhibition of the PI3K/Akt/mTOR pathway. Oncol Rep. 2019;41(5):2937–2944. doi:10.3892/or.2019.707230896824
   PubMed Web of Science ®Google Scholar
• LiZ, JiangT, LuQ, et al. Berberine attenuated the cytotoxicity induced by t-BHP via inhibiting oxidative stress and mitochondria dysfunction in PC-12 cells. Cell Mol Neurobiol. 2019:1–16.
   Web of Science ®Google Scholar
• ChenY, ChenY, LiangY, ChenH, JiX, HuangM. Berberine mitigates cognitive decline in an alzheimer’s disease mouse model by targeting both tau hyperphosphorylation and autophagic clearance. Biomed Pharmacother. 2020;121:109670. doi:10.1016/j.biopha.2019.10967031810131
   PubMed Web of Science ®Google Scholar
• ZengZ, PanY, WuW, et al. Myocardial hypertrophy is improved with berberine treatment via long non-coding RNA MIAT-mediated autophagy. J Pharm Pharmacol. 2019;71(12):1822–1831. doi:10.1111/jphp.1317031612504
   PubMed Web of Science ®Google Scholar
• LinYS, ChiuYC, TsaiYH, et al. Different mechanisms involved in the berberine-induced antiproliferation effects in triple-negative breast cancer cell lines. J Cell Biochem. 2019;120(8):13531–13544. doi:10.1002/jcb.2862830957305
   PubMed Web of Science ®Google Scholar
• ChenH, JiY, YanX, SuG, ChenL, XiaoJ. Berberine attenuates apoptosis in rat retinal Muller cells stimulated with high glucose via enhancing autophagy and the AMPK/mTOR signaling. Biomed Pharmacother. 2018;108:1201–1207. doi:10.1016/j.biopha.2018.09.14030372821
   PubMed Web of Science ®Google Scholar
• FanX, WangJ, HouJ, et al. Berberine alleviates ox-LDL induced inflammatory factors by up-regulation of autophagy via AMPK/mTOR signaling pathway. J Transl Med. 2015;13(1):92. doi:10.1186/s12967-015-0450-z25884210
   PubMed Web of Science ®Google Scholar
• SilvaA, YunesJA, CardosoBA, et al. PTEN posttranslational inactivation and hyperactivation of the PI3K/Akt pathway sustain primary T cell leukemia viability. J Clin Invest. 2008;118(11):3762–3774. doi:10.1172/JCI3461618830414
   PubMed Web of Science ®Google Scholar
• NishiokaC, IkezoeT, YangJ, KoefflerHP, YokoyamaA. Blockade of mTOR signaling potentiates the ability of histone deacetylase inhibitor to induce growth arrest and differentiation of acute myelogenous leukemia cells. Leukemia. 2008;22(12):2159–2168. doi:10.1038/leu.2008.24318784743
   PubMed Web of Science ®Google Scholar
• McCubreyJA, SteelmanLS, AbramsSL, et al. Targeting survival cascades induced by activation of Ras/Raf/MEK/ERK, PI3K/PTEN/Akt/mTOR and Jak/STAT pathways for effective leukemia therapy. Leukemia. 2008;22(4):708–722. doi:10.1038/leu.2008.2718337766
   PubMed Web of Science ®Google Scholar
• SteelmanLS, AbramsSL, WhelanJ, et al. Contributions of the Raf/MEK/ERK, PI3K/PTEN/Akt/mTOR and Jak/STAT pathways to leukemia. Leukemia. 2008;22:686–707.18337767
   PubMed Web of Science ®Google Scholar
• HeY, MoQ, LuoB, et al. Induction of apoptosis and autophagy via mitochondria- and PI3K/Akt/mTOR-mediated pathways by E. adenophorum in hepatocytes of saanen goat. Oncotarget. 2016;7(34):54537–54548. doi:10.18632/oncotarget.1040227391155
   PubMedGoogle Scholar
• YangJ, ChenQ, TianS, et al. The role of 1,25-dyhydroxyvitamin D3 in mouse liver ischemia reperfusion injury: regulation of autophagy through activation of MEK/ERK signaling and PTEN/PI3K/Akt/mTORC1 signaling. Am J Transl Res. 2015;7(12):2630–2645.26885262
   PubMed Web of Science ®Google Scholar
• LiuQ, MaH, SunX, et al. The regulatory ZFAS1/miR-150/ST6GAL1 crosstalk modulates sialylation of EGFR via PI3K/Akt pathway in T-cell acute lymphoblastic leukemia. J Exp Clin Cancer Res. 2019;38(1):199. doi:10.1186/s13046-019-1208-x31096997
   PubMed Web of Science ®Google Scholar
• TatsumiE, PiontekC, SugimotoT, MinatoK, MinowadaJ. Selective loss of the expression of OKT-4 or Leu-3A defined antigen by 12-0-tetradecanoylphorbol-13-acetate (TPA) in human lymphoid cells. Am J Hematol. 1984;17(3):287–294. doi:10.1002/ajh.28301703096475939
   PubMed Web of Science ®Google Scholar
• SerafinV, CapuzzoG, MilaniG, et al. Glucocorticoid resistance is reverted by LCK inhibition in pediatric T-cell acute lymphoblastic leukemia. Blood. 2017;130(25):2750–2761. doi:10.1182/blood-2017-05-78460329101238
   PubMed Web of Science ®Google Scholar
• MohammadiS, SeyedhoseiniFS, AsadiJ, YazdaniY. Effects of berberine on the secretion of cytokines and expression of genes involved in cell cycle regulation in THP-1 monocytic cell line. Iran J Basic Med Sci. 2017;20(5):530–537. doi:10.22038/IJBMS.2017.867728656088
   PubMed Web of Science ®Google Scholar
• SwaminathanS, KlemmL, ParkE, et al. Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia. Nat Immunol. 2015;16:766–774.25985233
   PubMed Web of Science ®Google Scholar
• LiH, MiyaharaT, TezukaY, TranQL, SetoH, KadotaS. Effect of berberine on bone mineral density in SAMP6 as a senile osteoporosis model. Biol Pharm Bull. 2003;26(1):110–111. doi:10.1248/bpb.26.11012520186
   PubMed Web of Science ®Google Scholar
• LiYH, ZhangM, FuHB, XiaoHT, BianZX. Pre-clinical toxicity of a combination of berberine and 5-aminosalicylic acid in mice. Food Chem Toxicol. 2016;97:150–158.27587080
   PubMed Web of Science ®Google Scholar
• ZhangX, GuL, LiJ, et al. Degradation of MDM2 by the interaction between berberine and DAXX leads to potent apoptosis in MDM2-overexpressing cancer cells. Cancer Res. 2010;70(23):9895–9904. doi:10.1158/0008-5472.CAN-10-154620935220
   PubMed Web of Science ®Google Scholar
• PengPL, KuoWH, TsengHC, ChouFP. Synergistic tumor-killing effect of radiation and berberine combined treatment in lung cancer: the contribution of autophagic cell death. Int J Radiat Oncol Biol Phys. 2008;70(2):529–542. doi:10.1016/j.ijrobp.2007.08.03418207031
   PubMed Web of Science ®Google Scholar
• LampadaA, O’PreyJ, SzabadkaiG, RyanKM, HochhauserD, SalomoniP. mTORC1-independent autophagy regulates receptor tyrosine kinase phosphorylation in colorectal cancer cells via an mTORC2-mediated mechanism. Cell Death Differ. 2017;24(6):1045–1062. doi:10.1038/cdd.2017.4128475179
   PubMed Web of Science ®Google Scholar
• ErazoT, LorenteM, Lopez-PlanaA, et al. The new antitumor drug ABTL0812 inhibits the Akt/mTORC1 axis by upregulating tribbles-3 pseudokinase. Clin Cancer Res. 2016;22(10):2508–2519. doi:10.1158/1078-0432.CCR-15-180826671995
   PubMed Web of Science ®Google Scholar
• ImanshahidiM, HosseinzadehH. Pharmacological and therapeutic effects of Berberis vulgaris and its active constituent, berberine. Phytother Res. 2008;22(8):999–1012. doi:10.1002/ptr.239918618524
   PubMed Web of Science ®Google Scholar
• AhmadS, HussainA, HussainA, et al. Quantification of berberine in berberis vulgaris l. root extract and its curative and prophylactic role in cisplatin-induced in vivo toxicity and in vitro cytotoxicity. Antioxidants. 2019;8(6):185. doi:10.3390/antiox8060185
   Web of Science ®Google Scholar
• NassourJ, RadfordR, CorreiaA, et al. Autophagic cell death restricts chromosomal instability during replicative crisis. Nature. 2019;565(7741):659–663. doi:10.1038/s41586-019-0885-030675059
   PubMed Web of Science ®Google Scholar
• SehgalAR, KonigH, JohnsonDE, et al. You eat what you are: autophagy inhibition as a therapeutic strategy in leukemia. Leukemia. 2015;29(3):517–525. doi:10.1038/leu.2014.34925541151
   PubMed Web of Science ®Google Scholar
• Seton-RogersS. Eliminating protective autophagy in KRAS-mutant cancers. Nat Rev Cancer. 2019;19(5):247. doi:10.1038/s41568-019-0137-530936466
   PubMed Web of Science ®Google Scholar
• VodnalaSK, EilR, KishtonRJ, et al. T cell stemness and dysfunction in tumors are triggered by a common mechanism. Science. 2019;363(6434):eaau0135. doi:10.1126/science.aau013530923193
   PubMed Web of Science ®Google Scholar
• JiY, LiL, MaYX, et al. Quercetin inhibits growth of hepatocellular carcinoma by apoptosis induction in part via autophagy stimulation in mice. J Nutr Biochem. 2019;69:108–119. doi:10.1016/j.jnutbio.2019.03.01831078904
   PubMed Web of Science ®Google Scholar
• DuS, LiC, LuY, et al. Dioscin alleviates crystalline silica-induced pulmonary inflammation and fibrosis through promoting alveolar macrophage autophagy. Theranostics. 2019;9(7):1878–1892. doi:10.7150/thno.2968231037145
   PubMed Web of Science ®Google Scholar
• DyczynskiM, VesterlundM, BjorklundAC, et al. Metabolic reprogramming of acute lymphoblastic leukemia cells in response to glucocorticoid treatment. Cell Death Dis. 2018;9(9):846. doi:10.1038/s41419-018-0625-730154400
   PubMed Web of Science ®Google Scholar
• EvangelistiC, ChiariniF, McCubreyJA, MartelliAM. Therapeutic targeting of mTOR in T-cell acute lymphoblastic leukemia: an update. Int J Mol Sci. 2018;19:1878.
   PubMed Web of Science ®Google Scholar
• DikicI, ElazarZ. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 2018;19(6):349–364. doi:10.1038/s41580-018-0003-429618831
   PubMed Web of Science ®Google Scholar
• ZhengW, XieW, YinD, LuoR, LiuM, GuoF. ATG5 and ATG7 induced autophagy interplays with UPR via PERK signaling. Cell Commun Signal. 2019;17:42.31060556
   PubMed Web of Science ®Google Scholar
• PowellJD, PollizziKN, HeikampEB, HortonMR. Regulation of immune responses by mTOR. Annu Rev Immunol. 2012;30(1):39–68. doi:10.1146/annurev-immunol-020711-07502422136167
   PubMed Web of Science ®Google Scholar
• JewellJL, FuV, HongAW, et al. GPCR signaling inhibits mTORC1 via PKA phosphorylation of Raptor. Elife. 2019;8. doi:10.7554/eLife.43038
   PubMed Web of Science ®Google Scholar
• Silva-PavezE, VillarP, TrigoC, et al. CK2 inhibition with silmitasertib promotes methuosis-like cell death associated to catastrophic massive vacuolization of colorectal cancer cells. Cell Death Dis. 2019;10(2):73. doi:10.1038/s41419-019-1306-x30683840
   PubMed Web of Science ®Google Scholar
• Martinez-CarreresL, PuyalJ, Leal-EstebanLC, et al. CDK4 regulates lysosomal function and mTORC1 activation to promote cancer cell survival. Cancer Res. 2019;79(20):5245–5259. doi:10.1158/0008-5472.CAN-19-070831395606
   PubMed Web of Science ®Google Scholar