Simultaneous activation and blockade of autophagy to fight hepatocellular carcinoma

References

• Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians. 2021;71(3):209–29.
   PubMed Web of Science ®Google Scholar
• Yang JD, Hainaut P, Gores GJ, et al A global view of hepatocellular carcinoma: trends, risk, prevention and management. NRGH. 2019 Oct;16(10):589–604.
   Google Scholar
• Wertheim JA, Petrowsky H, Saab S, Kupiec-Weglinski JW, Busuttil RW. Major Challenges Limiting Liver Transplantation in the United States. Am J Transplant. 2011 Sep;11(9):1773–84.
   PubMed Web of Science ®Google Scholar
• Llovet JM, Montal R, Sia D, Finn RS. Molecular therapies and precision medicine for hepatocellular carcinoma. Nature Reviews Clinical Oncology. 2018 Oct;15(10):599–616.
   PubMed Web of Science ®Google Scholar
• Calderaro J, Ziol M, Paradis V, et al. Molecular and histological correlations in liver cancer. J Hepatol. 2019 Sep;71(3):616–30.
   PubMed Web of Science ®Google Scholar
• Uchiyama Y, Shibata M, Koike M, et al. Autophagy–physiology and pathophysiology. Histochem Cell Biol. 2008 Apr;129(4):407–20.
   PubMed Web of Science ®Google Scholar
• Hamaï A, Codogno P. New Targets for Acetylation in Autophagy. Sci Signal. 2012 Jul 3;5(231):pe29–pe29.
   PubMed Web of Science ®Google Scholar
• Lee YJ, Jang BK. The Role of Autophagy in Hepatocellular Carcinoma. Int J Mol Sci. 2015 Nov 6;16(11):26629–43.
   PubMed Web of Science ®Google Scholar
• Yazdani HO, Huang H, Tsung A. Autophagy: Dual Response in the Development of Hepatocellular Carcinoma. Cells. 2019 Jan 28;8(2):91.
   PubMed Web of Science ®Google Scholar
• Liu L, Liao JZ, He XX, et al. The role of autophagy in hepatocellular carcinoma: friend or foe. Oncotarget. 2017 Apr 18;8(34):57707–22.
   PubMedGoogle Scholar
• Aunan JR, Cho WC, Søreide K. The Biology of Aging and Cancer: A Brief Overview of Shared and Divergent Molecular Hallmarks. Aging Dis. 2017 Oct;8(5):628–42.
   PubMed Web of Science ®Google Scholar
• Singh SS, Vats S, Chia AYQ, et al. Dual role of autophagy in hallmarks of cancer. Oncogene. 2018 Mar;37(9):1142–58.
   PubMed Web of Science ®Google Scholar
• Yun CW, Lee SH. The Roles of Autophagy in Cancer. Int J Mol Sci. 2018 Nov 5;19(11):3466.
   PubMed Web of Science ®Google Scholar
• Nazio F, Bordi M, Cianfanelli V, et al. F. Autophagy and cancer stem cells: molecular mechanisms and therapeutic applications. Cell Death Differ. 2019 Mar;26(4):690–702.
   PubMed Web of Science ®Google Scholar
• Ueno T, Komatsu M. Autophagy in the liver: functions in health and disease. Nat Rev Gastroenterol Hepatol. 2017 Mar;14(3):170–84.
   PubMed Web of Science ®Google Scholar
• Inami Y, Waguri S, Sakamoto A, et al. Persistent activation of Nrf2 through p62 in hepatocellular carcinoma cells. J Cell Biol. 2011 Apr 18;193(2):275–84.
   PubMed Web of Science ®Google Scholar
• Denk H, Stumptner C, Fuchsbichler A, et al. Are the Mallory bodies and intracellular hyaline bodies in neoplastic and non-neoplastic hepatocytes related? J Pathol. 2006 Apr;208(5):653–61.
   PubMed Web of Science ®Google Scholar
• Umemura A, He F, Taniguchi K, et al. p62, Upregulated during Preneoplasia, Induces Hepatocellular Carcinogenesis by Maintaining Survival of Stressed HCC-Initiating Cells. Cancer Cell. 2016 13;29(6):935–48.
   PubMed Web of Science ®Google Scholar
• Lin CW, Chen YS, Lin CC, et al. Autophagy-related gene LC3 expression in tumor and liver microenvironments significantly predicts recurrence of hepatocellular carcinoma after surgical resection. CTG. 2018 Jun;9(6):e166.
   Google Scholar
• Chao X, Wang S, Fulte S, et al. Hepatocytic p62 suppresses ductular reaction and tumorigenesis in mouse livers with mTORC1 activation and defective autophagy. J Hepatol. 2022 Mar;76(3):639–51.
   PubMed Web of Science ®Google Scholar
• Chang Y, Yan W, He X, et al. miR-375 Inhibits Autophagy and Reduces Viability of Hepatocellular Carcinoma Cells Under Hypoxic Conditions. Gastroenterology. 2012 Jul 1;143(1):177–187.e8.
   PubMed Web of Science ®Google Scholar
• Sun K, Guo X l, Zhao Q D et al. Paradoxical role of autophagy in the dysplastic and tumor-forming stages of hepatocarcinoma development in rats. Cell Death Dis. 2013 Feb;4(2):e501.
   Google Scholar
• Hu T, Li P, Luo Z, et al. Chloroquine inhibits hepatocellular carcinoma cell growth in vitro and in vivo. Oncol Rep. 2016 Jan;35(1):43–9.
   PubMed Web of Science ®Google Scholar
• Ding ZB, Hui B, Shi YH, Zhou J, Peng YF, Gu CY, et al. Autophagy Activation in Hepatocellular Carcinoma Contributes to the Tolerance of Oxaliplatin via Reactive Oxygen Species Modulation. Clin Cancer Res. 2011 Oct 1;17(19):6229–38.
   PubMed Web of Science ®Google Scholar
• Chen LH, Loong CC, Su TL, et al. Autophagy inhibition enhances apoptosis triggered by BO-1051, an N-mustard derivative, and involves the ATM signaling pathway. Biochem Pharmacol. 2011 Mar 1;81(5):594–605.
   PubMed Web of Science ®Google Scholar
• Hui B, Shi YH, Ding ZB, et al. Proteasome inhibitor interacts synergistically with autophagy inhibitor to suppress proliferation and induce apoptosis in hepatocellular carcinoma. Cancer. 2012;118(22):5560–71.
   PubMed Web of Science ®Google Scholar
• Du H, Yang W, Chen L, et al. Role of autophagy in resistance to oxaliplatin in hepatocellular carcinoma cells. Oncol Rep. 2012 Jan;27(1):143–50.
   PubMed Web of Science ®Google Scholar
• Shimizu S, Takehara T, Hikita H, et al. Inhibition of autophagy potentiates the antitumor effect of the multikinase inhibitor sorafenib in hepatocellular carcinoma. IJC. 2012;131(3):548–57.
   Google Scholar
• Guo X L, Li D, Hu F, et al. Targeting autophagy potentiates chemotherapy-induced apoptosis and proliferation inhibition in hepatocarcinoma cells. CL. 2012 Jul 28;320(2):171–9.
   Google Scholar
• Guo X L, Li D, Sun K, et al. Inhibition of autophagy enhances anticancer effects of bevacizumab in hepatocarcinoma. J Mol Med (Berl). 2013 Apr;91(4):473–83.
   PubMed Web of Science ®Google Scholar
• Gao L, Song J R, Zhang J W, et al. Chloroquine Promotes the Anticancer Effect of TACE in a Rabbit VX2 Liver Tumor Model. Int J Biol Sci. 2013 Mar 28;9(4):322–30.
   PubMed Web of Science ®Google Scholar
• Chang Z, Shi G, Jin J, et al. Dual PI3K/mTOR inhibitor NVP-BEZ235-induced apoptosis of hepatocellular carcinoma cell lines is enhanced by inhibitors of autophagy. Int J Mol Med. 2013 Jun;31(6):1449–56.
   PubMed Web of Science ®Google Scholar
• Yuan H, Li AJ, Ma SL, et al. Inhibition of autophagy significantly enhances combination therapy with sorafenib and HDAC inhibitors for human hepatoma cells. World J Gastroenterol. 2014 May 7;20(17):4953–62.
   PubMed Web of Science ®Google Scholar
• Tong Y, Huang H, Pan H. Inhibition of MEK/ERK activation attenuates autophagy and potentiates pemetrexed-induced activity against HepG2 hepatocellular carcinoma cells. Biochem Biophys Res Commun. 2015 Jan 2;456(1):86–91.
   PubMed Web of Science ®Google Scholar
• Zhang N, Xie H, Lu W, et.al Chloroquine sensitizes hepatocellular carcinoma cells to chemotherapy via blocking autophagy and promoting mitochondrial dysfunction. Int J Clin Exp Pathol. 2017 Sep 1;10(9):10056–65.
   PubMed Web of Science ®Google Scholar
• Pérez-Hernández M, Arias A, Martínez-García D, et.al Targeting Autophagy for Cancer Treatment and Tumor Chemosensitization. Cancers (Basel). 2019 Oct 19;11(10):1599.
   PubMed Web of Science ®Google Scholar
• Gao M, Yeh PY, Lu YS, et al. OSU-03012, a novel celecoxib derivative, induces reactive oxygen species-related autophagy in hepatocellular carcinoma. Cancer Res. 2008 Nov 15;68(22):9348–57.
   PubMed Web of Science ®Google Scholar
• Liu YL, Yang PM, Shun CT, et al. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy. 2010 Nov;6(8):1057–65.
   PubMed Web of Science ®Google Scholar
• Wang N, Pan W, Zhu M, et al. Fangchinoline induces autophagic cell death via p53/sestrin2/AMPK signalling in human hepatocellular carcinoma cells. Br J Pharmacol. 2011 Sep;164(2b):731–42.
   Web of Science ®Google Scholar
• Li P, Du Q, Cao Z, et al. Interferon-gamma induces autophagy with growth inhibition and cell death in human hepatocellular carcinoma (HCC) cells through interferon-regulatory factor-1 (IRF-1). Cancer Lett. 2012 Jan 28;314(2):213–22.
   PubMed Web of Science ®Google Scholar
• Yu HC, Lin CS, Tai WT, et al. Nilotinib Induces Autophagy in Hepatocellular Carcinoma through AMPK Activation. J Biol Chem. 2013 Jun 21;288(25):18249–59.
   PubMed Web of Science ®Google Scholar
• Hu M, Huang H, Zhao R, et al. AZD8055 induces cell death associated with autophagy and activation of AMPK in hepatocellular carcinoma. Oncol Rep. 2014 Feb;31(2):649–56.
   PubMed Web of Science ®Google Scholar
• Chen YJ, Chi CW, Su WC, et al. Lapatinib induces autophagic cell death and inhibits growth of human hepatocellular carcinoma. Oncotarget. 2014 Jul 15;5(13):4845–54.
   PubMedGoogle Scholar
• Shi Y, Song Q, Hu D, et al. Oleanolic acid induced autophagic cell death in hepatocellular carcinoma cells via PI3K/Akt/mTOR and ROS-dependent pathway. Korean J Physiol Pharmacol. 2016 May;20(3):237–43.
   PubMed Web of Science ®Google Scholar
• Han B, Yu YQ, Yang QL, et al. Kaempferol induces autophagic cell death of hepatocellular carcinoma cells via activating AMPK signaling. Oncotarget. 2017 Sep 16;8(49):86227–39.
   PubMedGoogle Scholar
• Leu YS, Chen YJ, Chen CC, et al. Induction of Autophagic Death of Human Hepatocellular Carcinoma Cells by Armillaridin from Armillaria mellea. Am J Chin Med. 2019;47(6):1365–80.
   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 Jan 15;697:108688.
   PubMed Web of Science ®Google Scholar
• Chen CL, Tseng YW, Wu JC, et al. Suppression of hepatocellular carcinoma by baculovirus-mediated expression of long non-coding RNA PTENP1 and MicroRNA regulation. Biomaterials. 2015 Mar 1;44:71–81.
   PubMed Web of Science ®Google Scholar
• Go DH, Lee YG, Lee DH, et al. 3-Decylcatechol induces autophagy-mediated cell death through the IRE1α/JNK/p62 in hepatocellular carcinoma cells. Oncotarget. 2017 May 9;8(35):58790–800.
   PubMedGoogle Scholar
• Yao C, Liu BB, Qian XD, et al. Crocin induces autophagic apoptosis in hepatocellular carcinoma by inhibiting Akt/mTOR activity. Onco Targets Ther. 2018;11:2017–28.
   PubMed Web of Science ®Google Scholar
• Hu P, Cheng B, He Y, et al. Autophagy suppresses proliferation of HepG2 cells via inhibiting glypican-3/wnt/β-catenin signaling. Onco Targets Ther. 2018 Jan 4;11:193–200.
   PubMed Web of Science ®Google Scholar
• Pan H, Wang Y, Na K, et al. Autophagic flux disruption contributes to Ganoderma lucidum polysaccharide-induced apoptosis in human colorectal cancer cells via MAPK/ERK activation. Cell Death Dis. 2019 Jun 11;10(6):456.
   PubMedGoogle Scholar
• Degtyarev M, De Mazière A, Orr C, et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol. 2008 Oct 6;183(1):101–16.
   PubMed Web of Science ®Google Scholar
• Boya P, González-Polo RA, Casares N, et al. Inhibition of Macroautophagy Triggers Apoptosis. Mol Cell Biol. 2005 Feb;25(3):1025–40.
   PubMed Web of Science ®Google Scholar
• Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004 Apr;11(4):448–57.
   PubMed Web of Science ®Google Scholar
• Gonzalez P, Mader I, Tchoghandjian A, et al. Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ. 2012 Aug;19(8):1337–46.
   PubMed Web of Science ®Google Scholar
• Humbert M, Morán M, de la Cruz-Ojeda P, et al. Assessing Autophagy in Archived Tissue or How to Capture Autophagic Flux from a Tissue Snapshot. Biology (Basel). 2020 Mar 21;9(3):59.
   PubMedGoogle Scholar
• Pant K, Saraya A, Venugopal SK. Oxidative stress plays a key role in butyrate-mediated autophagy via Akt/mTOR pathway in hepatoma cells. CBI. 2017 Aug 1;273:99–106.
   Google Scholar
• Ren Z, Li A, Jiang J, et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut. 2019 Jun;68(6):1014–23.
   PubMed Web of Science ®Google Scholar
• Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010 Jun;221(2):117–24.
   PubMed Web of Science ®Google Scholar
• Mauthe M, Orhon I, Rocchi C, et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy. 2018 Jul 20;14(8):1435–55.
   PubMed Web of Science ®Google Scholar
• Kucharewicz K, Dudkowska M, Zawadzka A, et al. Simultaneous induction and blockade of autophagy by a single agent. CCD. 2018 Mar 2;9(3):1–15.
   Google Scholar
• Mei L, Chen Y, Wang Z, et al. Synergistic anti-tumour effects of tetrandrine and chloroquine combination therapy in human cancer: a potential antagonistic role for p21. Br J Pharmacol. 2015 May;172(9):2232–45.
   PubMed Web of Science ®Google Scholar
• Button RW, Roberts SL, Willis TL, et al. Accumulation of autophagosomes confers cytotoxicity. J Biol Chem. 2017 Aug 18;292(33):13599–614.
   PubMed Web of Science ®Google Scholar
• Wang F, Gómez‐Sintes R, Boya P. Lysosomal membrane permeabilization and cell death. Traffic. 2018;19(12):918–31.
   PubMed Web of Science ®Google Scholar
• Allaire M, Rautou PE, Codogno P, et al. Autophagy in liver diseases: Time for translation? JOH. 2019 May 1;70(5):985–98.
   Google Scholar
• Takamura A, Komatsu M, Hara T, et al. Autophagy-deficient mice develop multiple liver tumors. Genes Dev. 2011 Apr 15;25(8):795–800.
   PubMed Web of Science ®Google Scholar
• Ni HM, Woolbright BL, Williams J, et al. Nrf2 Promotes the Development of Fibrosis and Tumorigenesis in Mice with Defective Hepatic Autophagy. J Hepatol. 2014 Sep;61(3):617–25.
   PubMed Web of Science ®Google Scholar
• Chao X, Ni HM, Ding WX. An unexpected tumor suppressor role of SQSTM1/p62 in liver tumorigenesis. Autophagy. 18(2):459–61.
   PubMed Web of Science ®Google Scholar
• Yang Y, Wang Q, Song D, et al. Lysosomal dysfunction and autophagy blockade contribute to autophagy-related cancer suppressing peptide-induced cytotoxic death of cervical cancer cells through the AMPK/mTOR pathway. JECCR. 2020 Sep 22;39(1):197.
   Google Scholar
• Jang YJ, Kim JH, Byun S. Modulation of Autophagy for Controlling Immunity. Cells. 2019 Feb 9;8(2):138.
   PubMed Web of Science ®Google Scholar
• Li X, Wang ZG, Zhu H, et al. Inducing Autophagy and Blocking Autophagic Flux via a Virus-Mimicking Nanodrug for Cancer Therapy. Nano Lett. 2022 Nov 23;22(22):9163–73.
   PubMedGoogle Scholar
• Appelqvist H, Wäster P, Kågedal K, et al. The lysosome: from waste bag to potential therapeutic target. J Mol Cell Biol. 2013 Aug 1;5(4):214–26.
   PubMed Web of Science ®Google Scholar
• Ono K, Kim SO, Han J. Susceptibility of Lysosomes to Rupture Is a Determinant for Plasma Membrane Disruption in Tumor Necrosis Factor Alpha-Induced Cell Death. Mol Cell Biol. 2003 Jan;23(2):665–76.
   PubMed Web of Science ®Google Scholar
• Domagala A, Fidyt K, Bobrowicz M, et al. Typical and Atypical Inducers of Lysosomal Cell Death: A Promising Anticancer Strategy. IJMS. 2018 Aug;19(8):2256.
   Google Scholar
• Fehrenbacher N, Gyrd-Hansen M, Poulsen B, et al. Sensitization to the Lysosomal Cell Death Pathway upon Immortalization and Transformation. Cancer Res. 2004 Aug 1;64(15):5301–10.
   PubMed Web of Science ®Google Scholar
• Circu M, Cardelli J, Barr M, et al. Modulating lysosomal function through lysosome membrane permeabilization or autophagy suppression restores sensitivity to cisplatin in refractory non-small-cell lung cancer cells. Plos One. 2017 Sep 25;12(9):e0184922.
   PubMed Web of Science ®Google Scholar
• Mora R, Abschuetz A, Kees T, et al. TNF-alpha- and TRAIL-resistant glioma cells undergo autophagy-dependent cell death induced by activated microglia. Glia. 2009 Apr 1;57(5):561–81.
   PubMed Web of Science ®Google Scholar
• Solomon VR, Lee H. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur J Pharmacol. 2009 Dec 25;625(1–3):220–33.
   PubMed Web of Science ®Google Scholar
• Chen HE, Lin JF, Tsai TF, et al. Chloroquine induces lysosomal membrane permeability mediated apoptotic cell death in bladder cancer cells. US. 2016 Jun 1;27(2, Supplement 1):S5.
   Google Scholar
• Jan G, Belzacq AS, Haouzi D, et al. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. CDD. 2002 Feb;9(2):179–88.
   Google Scholar
• Chassaing B, Etienne-Mesmin L, Gewirtz AT. Microbiota-Liver Axis in Hepatic Disease. Hepatology. 2014 Jan;59(1):328–39.
   PubMed Web of Science ®Google Scholar
• Iwai-Kanai E, Yuan H, Huang C, et al. A Method to Measure Cardiac Autophagic Flux in vivo. Autophagy. 2008 Apr;4(3):322–9.
   PubMed Web of Science ®Google Scholar