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Current Cancer Drug Targets

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ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

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Review Article

The Role of Oxidative Stress in the Development and Therapeutic Intervention of Hepatocellular Carcinoma

Author(s): Ying Liu, Chunhai Hao, Lei Li, Haiguang Zhang, Weina Zha, Longbin Ma, Li Chen* and Jianhe Gan*

Volume 23, Issue 10, 2023

Published on: 24 May, 2023

Page: [792 - 804] Pages: 13

DOI: 10.2174/1568009623666230418121130

Price: $65

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Abstract

Oxidative stress (OS) is a condition in which the body has an unbalanced oxidative and antioxidant effect. Oxidative stress has emerged as a critical component in the onset and progression of numerous diseases, including liver cancer and chronic liver disease caused by the hepatitis C virus and hepatitis B virus. Reactive oxygen species (ROS) are the most prevalent reactive chemical species involved in the oxidative stress response during the progression of the disease. Oxidative stress has a unique role in the development of hepatocellular carcinoma (HCC), and excessive ROS production is a common occurrence in liver illnesses of various etiologies. In response to various deleterious stimuli, the liver shows manifestations of lipid accumulation, oxidative damage, inflammatory infiltration, and immune response, which interact with each other in a mutually reinforcing manner, collectively exacerbating liver damage and malignant transformation. The intracellular buildup of ROS is a two-edged sword for tumor advancement. ROS are tumorigenic, and low amounts of ROS can trigger different signaling pathways that promote proliferation, survival, and migration, among other aspects. However, excessive oxidative stress can induce tumor cell death. Understanding the mechanisms of oxidative stress in hepatocellular carcinogenesis is beneficial for the prevention and surveillance of hepatocellular carcinoma in humans. An improved knowledge of the impacts and potential implications of oxidative stress regulation in therapeutic strategies will likely allow us to find new therapeutic targets for cancer. Oxidative stress also plays a significant role in the treatment of hepatocellular carcinoma and the mechanisms of drug resistance involved. This paper reviews recent studies on oxidative stress in HCC that are more reliable and important, and provides a more comprehensive view of the development of the treatment of HCC based on the relevant summaries of the effect of oxidative stress on the treatment.

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[1]
Cheng, Y.T.; Yang, C.C.; Shyur, L.F. Phytomedicine—Modulating oxidative stress and the tumor microenvironment for cancer therapy. Pharmacol. Res., 2016, 114, 128-143.
[http://dx.doi.org/10.1016/j.phrs.2016.10.022] [PMID: 27794498]
[2]
Sosa, V.; Moliné, T.; Somoza, R.; Paciucci, R.; Kondoh, H. LLeonart, M.E. Oxidative stress and cancer: An overview. Ageing Res. Rev., 2013, 12(1), 376-390.
[http://dx.doi.org/10.1016/j.arr.2012.10.004] [PMID: 23123177]
[3]
Castro, L.; Freeman, B.A. Reactive oxygen species in human health and disease. Nutrition., 2001, 17(2), 161-165, 163-165.
[http://dx.doi.org/10.1016/S0899-9007(00)00570-0] [PMID: 11240347]
[4]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[5]
McGlynn, K.A.; Petrick, J.L.; El-Serag, H.B. Epidemiology of hepatocellular carcinoma. Hepatology, 2021, 73(S1), 4-13.
[http://dx.doi.org/10.1002/hep.31288] [PMID: 32319693]
[6]
Llovet, J.M.; Kelley, R.K.; Villanueva, A.; Singal, A.G.; Pikarsky, E.; Roayaie, S.; Lencioni, R.; Koike, K.; Zucman-Rossi, J.; Finn, R.S. Hepatocellular carcinoma. Nat. Rev. Dis. Primers, 2021, 7(1), 6.
[http://dx.doi.org/10.1038/s41572-020-00240-3] [PMID: 33479224]
[7]
Ioannou, G.N. Epidemiology and risk-stratification of NAFLD-associated HCC. J. Hepatol., 2021, 75(6), 1476-1484.
[http://dx.doi.org/10.1016/j.jhep.2021.08.012] [PMID: 34453963]
[8]
Rebouissou, S.; Nault, J.C. Advances in molecular classification and precision oncology in hepatocellular carcinoma. J. Hepatol., 2020, 72(2), 215-229.
[http://dx.doi.org/10.1016/j.jhep.2019.08.017] [PMID: 31954487]
[9]
Massarweh, N.N.; El-Serag, H.B. Epidemiology of hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Cancer Contr., 2017, 24(3)
[http://dx.doi.org/10.1177/1073274817729245] [PMID: 28975830]
[10]
Marra, M.; Sordelli, I.M.; Lombardi, A.; Lamberti, M.; Tarantino, L.; Giudice, A.; Stiuso, P.; Abbruzzese, A.; Sperlongano, R.; Accardo, M.; Agresti, M.; Caraglia, M.; Sperlongano, P. Molecular targets and oxidative stress biomarkers in hepatocellular carcinoma: an overview. J. Transl. Med., 2011, 9(1), 171.
[http://dx.doi.org/10.1186/1479-5876-9-171] [PMID: 21985599]
[11]
Fu, N.; Yao, H.; Nan, Y.; Qiao, L. Role of oxidative stress in hepatitis C virus induced hepatocellular carcinoma. Curr. Cancer Drug Targets, 2017, 17(6), 498-504.
[http://dx.doi.org/10.2174/1568009616666160926124043] [PMID: 27677955]
[12]
Kim, J.; Kim, J.; Bae, J.S. ROS homeostasis and metabolism: A critical liaison for cancer therapy. Exp. Mol. Med., 2016, 48(11), e269.
[http://dx.doi.org/10.1038/emm.2016.119] [PMID: 27811934]
[13]
Bao, X.Z.; Dai, F.; Li, X.R.; Zhou, B. Targeting redox vulnerability of cancer cells by prooxidative intervention of a glutathione-activated Cu(II) pro-ionophore: Hitting three birds with one stone. Free Radic. Biol. Med., 2018, 124, 342-352.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.06.021] [PMID: 29935260]
[14]
Li, S.; Hong, M.; Tan, H.Y.; Wang, N.; Feng, Y. Insights into the role and interdependence of oxidative stress and inflammation in liver diseases. Oxid. Med. Cell. Longev., 2016, 2016, 1-21.
[http://dx.doi.org/10.1155/2016/4234061] [PMID: 28070230]
[15]
D’souza, S.; Lau, K.C.K.; Coffin, C.S.; Patel, T.R. Molecular mechanisms of viral hepatitis induced hepatocellular carcinoma. World J. Gastroenterol., 2020, 26(38), 5759-5783.
[http://dx.doi.org/10.3748/wjg.v26.i38.5759] [PMID: 33132633]
[16]
Lee, H.; Inn, K-S.; Kim, H.; Lee, S-A.; Kim, B.J.; Kim, H-I.; Won, Y-S. Upregulation of endoplasmic reticulum stress and reactive oxygen species by naturally occurring mutations in hepatitis B virus core antigen. J. Gen. Virol., 2015, 96(7), 1850-1854.
[http://dx.doi.org/10.1099/vir.0.000134] [PMID: 25828947]
[17]
Hsieh, Y.H.; Su, I.J.; Wang, H.C.; Chang, W.W.; Lei, H.Y.; Lai, M.D.; Chang, W.T.; Huang, W. Pre-S mutant surface antigens in chronic hepatitis B virus infection induce oxidative stress and DNA damage. Carcinogenesis, 2004, 25(10), 2023-2032.
[http://dx.doi.org/10.1093/carcin/bgh207] [PMID: 15180947]
[18]
Yu, X.; Lan, P.; Hou, X.; Han, Q.; Lu, N.; Li, T.; Jiao, C.; Zhang, J.; Zhang, C.; Tian, Z. HBV inhibits LPS-induced NLRP3 inflammasome activation and IL-1β production via suppressing the NF-κB pathway and ROS production. J. Hepatol., 2017, 66(4), 693-702.
[http://dx.doi.org/10.1016/j.jhep.2016.12.018] [PMID: 28027970]
[19]
Boulahtouf, Z.; Virzì, A.; Baumert, T.F.; Verrier, E.R.; Lupberger, J. Signaling induced by chronic viral hepatitis: Dependence and consequences. Int. J. Mol. Sci., 2022, 23(5), 2787.
[http://dx.doi.org/10.3390/ijms23052787] [PMID: 35269929]
[20]
Ivanov, A.; Smirnova, O.; Petrushanko, I.; Ivanova, O.; Karpenko, I.; Alekseeva, E.; Sominskaya, I.; Makarov, A.; Bartosch, B.; Kochetkov, S.; Isaguliants, M. HCV core protein uses multiple mechanisms to induce oxidative stress in human hepatoma Huh7 cells. Viruses, 2015, 7(6), 2745-2770.
[http://dx.doi.org/10.3390/v7062745] [PMID: 26035647]
[21]
Dionisio, N.; Garcia-Mediavilla, M.V.; Sanchez-Campos, S.; Majano, P.L.; Benedicto, I.; Rosado, J.A.; Salido, G.M.; Gonzalez-Gallego, J. Hepatitis C virus NS5A and core proteins induce oxidative stress-mediated calcium signalling alterations in hepatocytes. J. Hepatol., 2009, 50(5), 872-882.
[http://dx.doi.org/10.1016/j.jhep.2008.12.026] [PMID: 19303156]
[22]
Gong, G.; Waris, G.; Tanveer, R.; Siddiqui, A. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-κB. Proc. Natl. Acad. Sci., 2001, 98(17), 9599-9604.
[http://dx.doi.org/10.1073/pnas.171311298] [PMID: 11481452]
[23]
Williams, V.; Brichler, S.; Khan, E.; Chami, M.; Dény, P.; Kremsdorf, D.; Gordien, E. Large hepatitis delta antigen activates STAT-3 and NF-κB via oxidative stress. J. Viral Hepat., 2012, 19(10), 744-753.
[http://dx.doi.org/10.1111/j.1365-2893.2012.01597.x] [PMID: 22967106]
[24]
Chen, M.; Du, D.; Zheng, W.; Liao, M.; Zhang, L.; Liang, G.; Gong, M. Small hepatitis delta antigen selectively binds to target mRNA in hepatic cells: A potential mechanism by which hepatitis D virus downregulates glutathione S -transferase P1 and induces liver injury and hepatocarcinogenesis. Biochem. Cell Biol., 2019, 97(2), 130-139.
[http://dx.doi.org/10.1139/bcb-2017-0321] [PMID: 30153423]
[25]
Hendrikx, T.; Binder, C.J. Oxidation-specific epitopes in non-alcoholic fatty liver disease. Front. Endocrinol., 2020, 11, 607011.
[http://dx.doi.org/10.3389/fendo.2020.607011] [PMID: 33362721]
[26]
Takakura, K.; Oikawa, T.; Nakano, M.; Saeki, C.; Torisu, Y.; Kajihara, M.; Saruta, M. Recent insights into the multiple pathways driving non-alcoholic steatohepatitis-derived hepatocellular carcinoma. Front. Oncol., 2019, 9, 762.
[http://dx.doi.org/10.3389/fonc.2019.00762] [PMID: 31456946]
[27]
Sutti, S.; Albano, E. Adaptive immunity: An emerging player in the progression of NAFLD. Nat. Rev. Gastroenterol. Hepatol., 2020, 17(2), 81-92.
[http://dx.doi.org/10.1038/s41575-019-0210-2] [PMID: 31605031]
[28]
Gabbia, D.; Cannella, L.; De Martin, S. The role of oxidative stress in NAFLD–NASH–HCC transition—focus on NADPH oxidases. Biomedicines, 2021, 9(6), 687.
[http://dx.doi.org/10.3390/biomedicines9060687] [PMID: 34204571]
[29]
Ma, C.; Kesarwala, A.H.; Eggert, T.; Medina-Echeverz, J.; Kleiner, D.E.; Jin, P.; Stroncek, D.F.; Terabe, M.; Kapoor, V.; ElGindi, M.; Han, M.; Thornton, A.M.; Zhang, H.; Egger, M.; Luo, J.; Felsher, D.W.; McVicar, D.W.; Weber, A.; Heikenwalder, M.; Greten, T.F. NAFLD causes selective CD4+ T lymphocyte loss and promotes hepatocarcinogenesis. Nature, 2016, 531(7593), 253-257.
[http://dx.doi.org/10.1038/nature16969] [PMID: 26934227]
[30]
Valgimigli, L.; Valgimigli, M.; Gaiani, S.; Pedulli, G.F.; Bolondi, L. Measurement of oxidative stress in human liver by EPR spin-probe technique. Free Radic. Res., 2000, 33(2), 167-178.
[http://dx.doi.org/10.1080/10715760000300721] [PMID: 10885624]
[31]
Ljubuncic, P.; Tanne, Z.; Bomzon, A. Evidence of a systemic phenomenon for oxidative stress in cholestatic liver disease. Gut, 2000, 47(5), 710-716.
[http://dx.doi.org/10.1136/gut.47.5.710] [PMID: 11034590]
[32]
Moreno-Otero, R. May oxidative stress contribute to autoimmune hepatitis pathogenesis, and can antioxidants be of value as adjuvant therapy for refractory patients? Dig. Dis. Sci., 2013, 58(5), 1440-1442.
[http://dx.doi.org/10.1007/s10620-013-2622-0] [PMID: 23504353]
[33]
Kaffe, E.T.; Rigopoulou, E.I.; Koukoulis, G.K.; Dalekos, G.N.; Moulas, A.N. Oxidative stress and antioxidant status in patients with autoimmune liver diseases. Redox Rep., 2015, 20(1), 33-41.
[http://dx.doi.org/10.1179/1351000214Y.0000000101] [PMID: 25117650]
[34]
Patel, A.; Perl, A. Redox control of integrin-mediated hepatic inflammation in systemic autoimmunity. Antioxid. Redox Signal., 2022, 36(7-9), 367-388.
[http://dx.doi.org/10.1089/ars.2021.0068] [PMID: 34036799]
[35]
Tao, S.; Zhang, H.; Zhao, Q.; Bu, H.; Wang, H.; Guo, H. Correlation of vitamin D with inflammatory factors, oxidative stress and T cell subsets in patients with autoimmune hepatitis. Exp. Ther. Med., 2020, 19(5), 3419-3424.
[http://dx.doi.org/10.3892/etm.2020.8601] [PMID: 32266042]
[36]
Comar, J.F.; de Sá-Nakanishi, B.A.; de Oliveira, A.L.; Marques, N.W.M.; Bersani, A.C.A.; Ishii, I.E.L.; Peralta, R.M.; Bracht, A. Oxidative state of the liver of rats with adjuvant-induced arthritis. Free Radic. Biol. Med., 2013, 58, 144-153.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.12.003] [PMID: 23246655]
[37]
Gerschman, R.; Gilbert, D.L.; Nye, S.W.; Dwyer, P.; Fenn, W.O. Oxygen poisoning and x-irradiation: A mechanism in common. Science, 1954, 119(3097), 623-626.
[http://dx.doi.org/10.1126/science.119.3097.623] [PMID: 13156638]
[38]
Loft, S.; Poulsen, H.E. Cancer risk and oxidative DNA damage in man. J. Mol. Med., 1996, 74(6), 297-312.
[http://dx.doi.org/10.1007/BF00207507] [PMID: 8862511]
[39]
El-Zayadi, A.R. Heavy smoking and liver. World J. Gastroenterol., 2006, 12(38), 6098-6101.
[http://dx.doi.org/10.3748/wjg.v12.i38.6098] [PMID: 17036378]
[40]
Kalthoff, S.; Landerer, S.; Reich, J.; Strassburg, C.P. Protective effects of coffee against oxidative stress induced by the tobacco carcinogen benzo[α]pyrene. Free Radic. Biol. Med., 2017, 108, 66-76.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.03.006] [PMID: 28300668]
[41]
Bondy, S.C. Ethanol toxicity and oxidative stress. Toxicol. Lett., 1992, 63(3), 231-241.
[http://dx.doi.org/10.1016/0378-4274(92)90086-Y] [PMID: 1488774]
[42]
Ceni, E.; Mello, T.; Galli, A. Pathogenesis of alcoholic liver disease: Role of oxidative metabolism. World J. Gastroenterol., 2014, 20(47), 17756-17772.
[http://dx.doi.org/10.3748/wjg.v20.i47.17756] [PMID: 25548474]
[43]
Wang, Z.; Li, B.; Jiang, H.; Ma, Y.; Bao, Y.; Zhu, X.; Xia, H.; Jin, Y. IL-8 exacerbates alcohol-induced fatty liver disease via the Akt/HIF-1α pathway in human IL-8-expressing mice. Cytokine, 2021, 138, 155402.
[http://dx.doi.org/10.1016/j.cyto.2020.155402] [PMID: 33352397]
[44]
Leung, T.M.; Nieto, N. CYP2E1 and oxidant stress in alcoholic and non-alcoholic fatty liver disease. J. Hepatol., 2013, 58(2), 395-398.
[http://dx.doi.org/10.1016/j.jhep.2012.08.018] [PMID: 22940046]
[45]
Amstad, P.; Levy, A.; Emerit, I.; Cerutti, P. Evidence for membrane-mediated chromosomal damage by aflatoxin B1 in human lymphocytes. Carcinogenesis, 1984, 5(6), 719-723.
[http://dx.doi.org/10.1093/carcin/5.6.719] [PMID: 6426812]
[46]
Shen, H.; Ong, C.N.; Shi, C.Y. Involvement of reactive oxygen species in aflatoxin B1-induced cell injury in cultured rat hepatocytes. Toxicology, 1995, 99(1-2), 115-123.
[http://dx.doi.org/10.1016/0300-483X(94)03008-P] [PMID: 7761996]
[47]
Shen, H.M.; Shi, C.Y.; Shen, Y.; Ong, C.N. Detection of elevated reactive oxygen species level in cultured rat hepatocytes treated with aflatoxin B1. Free Radic. Biol. Med., 1996, 21(2), 139-146.
[http://dx.doi.org/10.1016/0891-5849(96)00019-6] [PMID: 8818628]
[48]
Wu, H.C.; Wang, Q.; Wang, L.W.; Yang, H.I.; Ahsan, H.; Tsai, W.Y.; Wang, L.Y.; Chen, S.Y.; Chen, C.J.; Santella, R.M. Urinary 8-oxodeoxyguanosine, aflatoxin B1 exposure and hepatitis B virus infection and hepatocellular carcinoma in Taiwan. Carcinogenesis, 2006, 28(5), 995-999.
[http://dx.doi.org/10.1093/carcin/bgl234] [PMID: 17127712]
[49]
Liu, Z.M.; Li, L.Q.; Peng, M.H.; Liu, T.W.; Qin, Z.; Guo, Y.; Xiao, K.Y.; Ye, X.P.; Mo, X.S.; Qin, X.; Li, S.; Yan, L.N.; Shen, H.M.; Wang, L.; Wang, Q.; Wang, K.; Liang, R.; Wei, Z.; Ong, C.N.; Santella, R.M.; Peng, T. Hepatitis B virus infection contributes to oxidative stress in a population exposed to aflatoxin B1 and high-risk for hepatocellular carcinoma. Cancer Lett., 2008, 263(2), 212-222.
[http://dx.doi.org/10.1016/j.canlet.2008.01.006] [PMID: 18280645]
[50]
Singh, K.B.; Maurya, B.K.; Trigun, S.K. Activation of oxidative stress and inflammatory factors could account for histopathological progression of aflatoxin-B1 induced hepatocarcinogenesis in rat. Mol. Cell. Biochem., 2015, 401(1-2), 185-196.
[http://dx.doi.org/10.1007/s11010-014-2306-x] [PMID: 25543524]
[51]
Rotimi, O.A.; Rotimi, S.O.; Goodrich, J.M.; Adelani, I.B.; Agbonihale, E.; Talabi, G. Time-course effects of acute aflatoxin B1 exposure on hepatic mitochondrial lipids and oxidative stress in rats. Front. Pharmacol., 2019, 10, 467.
[http://dx.doi.org/10.3389/fphar.2019.00467] [PMID: 31133854]
[52]
Li, C.I.; Chen, H.J.; Lai, H.C.; Liu, C.S.; Lin, W.Y.; Li, T.C.; Lin, C.C. Hyperglycemia and chronic liver diseases on risk of hepatocellular carcinoma in Chinese patients with type 2 diabetes--National cohort of Taiwan Diabetes Study. Int. J. Cancer, 2015, 136(11), 2668-2679.
[http://dx.doi.org/10.1002/ijc.29321] [PMID: 25387451]
[53]
Estes, C.; Anstee, Q.M.; Arias-Loste, M.T.; Bantel, H.; Bellentani, S.; Caballeria, J.; Colombo, M.; Craxi, A.; Crespo, J.; Day, C.P.; Eguchi, Y.; Geier, A.; Kondili, L.A.; Kroy, D.C.; Lazarus, J.V.; Loomba, R.; Manns, M.P.; Marchesini, G.; Nakajima, A.; Negro, F.; Petta, S.; Ratziu, V.; Romero-Gomez, M.; Sanyal, A.; Schattenberg, J.M.; Tacke, F.; Tanaka, J.; Trautwein, C.; Wei, L.; Zeuzem, S.; Razavi, H. Modeling NAFLD disease burden in China, France, Germany, Italy, Japan, Spain, United Kingdom, and United States for the period 2016–2030. J. Hepatol., 2018, 69(4), 896-904.
[http://dx.doi.org/10.1016/j.jhep.2018.05.036] [PMID: 29886156]
[54]
Manka, P.P.; Kaya, E.; Canbay, A.; Syn, W.K. A review of the epidemiology, pathophysiology, and efficacy of anti-diabetic drugs used in the treatment of nonalcoholic fatty liver disease. Dig. Dis. Sci., 2021, 66(11), 3676-3688.
[http://dx.doi.org/10.1007/s10620-021-07206-9] [PMID: 34410573]
[55]
Kumar, V.; Xin, X.; Ma, J.; Tan, C.; Osna, N.; Mahato, R.I. Therapeutic targets, novel drugs, and delivery systems for diabetes associated NAFLD and liver fibrosis. Adv. Drug Deliv. Rev., 2021, 176, 113888.
[http://dx.doi.org/10.1016/j.addr.2021.113888] [PMID: 34314787]
[56]
Sakurai, Y.; Kubota, N.; Yamauchi, T.; Kadowaki, T. Role of insulin resistance in MAFLD. Int. J. Mol. Sci., 2021, 22(8), 4156.
[http://dx.doi.org/10.3390/ijms22084156] [PMID: 33923817]
[57]
Masarone, M.; Rosato, V.; Aglitti, A.; Bucci, T.; Caruso, R.; Salvatore, T.; Sasso, F.C.; Tripodi, M.F.; Persico, M. Liver biopsy in type 2 diabetes mellitus: Steatohepatitis represents the sole feature of liver damage. PLoS One, 2017, 12(6), e0178473.
[http://dx.doi.org/10.1371/journal.pone.0178473] [PMID: 28570615]
[58]
Jabir, N.R.; Ahmad, S.; Tabrez, S. An insight on the association of glycation with hepatocellular carcinoma. Semin. Cancer Biol., 2018, 49, 56-63.
[http://dx.doi.org/10.1016/j.semcancer.2017.06.005] [PMID: 28634055]
[59]
Malaguti, C.; La Guardia, P.G.; Leite, A.C.R.; Oliveira, D.N.; de Lima Zollner, R.L.; Catharino, R.R.; Vercesi, A.E.; Oliveira, H.C.F. Oxidative stress and susceptibility to mitochondrial permeability transition precedes the onset of diabetes in autoimmune non-obese diabetic mice. Free Radic. Res., 2014, 48(12), 1494-1504.
[http://dx.doi.org/10.3109/10715762.2014.966706] [PMID: 25236567]
[60]
Ozutsumi, T.; Namisaki, T.; Shimozato, N.; Kaji, K.; Tsuji, Y.; Kaya, D.; Fujinaga, Y.; Furukawa, M.; Nakanishi, K.; Sato, S.; Sawada, Y.; Saikawa, S.; Kitagawa, K.; Takaya, H.; Kawaratani, H.; Kitade, M.; Moriya, K.; Noguchi, R.; Akahane, T.; Mitoro, A.; Yoshiji, H. Combined treatment with Sodium-Glucose Cotransporter-2 Inhibitor (Canagliflozin) and dipeptidyl peptidase-4 inhibitor (Teneligliptin) alleviates NASH progression in a non-diabetic rat model of steatohepatitis. Int. J. Mol. Sci., 2020, 21(6), 2164.
[http://dx.doi.org/10.3390/ijms21062164] [PMID: 32245205]
[61]
Zhang, Y.; Wang, H.; Xiao, H. Metformin actions on the liver: Protection mechanisms emerging in hepatocytes and immune cells against NASH-Related HCC. Int. J. Mol. Sci., 2021, 22(9), 5016.
[http://dx.doi.org/10.3390/ijms22095016] [PMID: 34065108]
[62]
Bäckhed, F.; Ding, H.; Wang, T.; Hooper, L.V.; Koh, G.Y.; Nagy, A.; Semenkovich, C.F.; Gordon, J.I. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl. Acad. Sci., 2004, 101(44), 15718-15723.
[http://dx.doi.org/10.1073/pnas.0407076101] [PMID: 15505215]
[63]
Neish, A.S.; Jones, R.M. Redox signaling mediates symbiosis between the gut microbiota and the intestine. Gut Microbes, 2014, 5(2), 250-253.
[http://dx.doi.org/10.4161/gmic.27917] [PMID: 24637602]
[64]
Jones, R.M.; Neish, A.S. Redox signaling mediated by the gut microbiota. Free Radic. Biol. Med., 2017, 105, 41-47.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.10.495] [PMID: 27989756]
[65]
Lee, W.J. Bacterial-modulated signaling pathways in gut homeostasis. Sci. Signal., 2008, 1(21), pe24.
[http://dx.doi.org/10.1126/stke.121pe24] [PMID: 18506033]
[66]
Weng, M.T.; Chiu, Y.T.; Wei, P.Y.; Chiang, C.W.; Fang, H.L.; Wei, S.C. Microbiota and gastrointestinal cancer. J. Formos. Med. Assoc., 2019, 118(S1), S32-S41.
[http://dx.doi.org/10.1016/j.jfma.2019.01.002] [PMID: 30655033]
[67]
Yu, L.X.; Schwabe, R.F. The gut microbiome and liver cancer: Mechanisms and clinical translation. Nat. Rev. Gastroenterol. Hepatol., 2017, 14(9), 527-539.
[http://dx.doi.org/10.1038/nrgastro.2017.72] [PMID: 28676707]
[68]
Castaldo, S.A.; Freitas, J.R.; Conchinha, N.V.; Madureira, P.A. The tumorigenic roles of the cellular REDOX regulatory systems. Oxid. Med. Cell. Longev., 2016, 2016, 1-17.
[http://dx.doi.org/10.1155/2016/8413032] [PMID: 26682014]
[69]
Zhu, J.; Xiong, Y.; Zhang, Y.; Wen, J.; Cai, N.; Cheng, K.; Liang, H.; Zhang, W. The molecular mechanisms of regulating oxidative stress-induced ferroptosis and therapeutic strategy in tumors. Oxid. Med. Cell. Longev., 2020, 2020, 1-14.
[http://dx.doi.org/10.1155/2020/8810785] [PMID: 33425217]
[70]
Dong, G.; Ye, X.; Wang, S.; Li, W.; Cai, R.; Du, L.; Shi, X.; Li, M. Au-24 as a potential thioredoxin reductase inhibitor in hepatocellular carcinoma cells. Pharmacol. Res., 2022, 177, 106113.
[http://dx.doi.org/10.1016/j.phrs.2022.106113] [PMID: 35124208]
[71]
Lee, D.; Xu, I.M.J.; Chiu, D.K.C.; Leibold, J.; Tse, A.P.W.; Bao, M.H.R.; Yuen, V.W.H.; Chan, C.Y.K.; Lai, R.K.H.; Chin, D.W.C.; Chan, D.F.F.; Cheung, T.T.; Chok, S.H.; Wong, C.M.; Lowe, S.W.; Ng, I.O.L.; Wong, C.C.L. Induction of oxidative stress through inhibition of thioredoxin reductase 1 Is an effective therapeutic approach for hepatocellular carcinoma. Hepatology, 2019, 69(4), 1768-1786.
[http://dx.doi.org/10.1002/hep.30467] [PMID: 30561826]
[72]
Chiou, J.F.; Tai, C.J.; Wang, Y.H.; Liu, T.Z.; Jen, Y.M.; Shiau, C.Y. Sorafenib induces preferential apoptotic killing of a drug- and radio-resistant hep G2 cells through a mitochondria-dependent oxidative stress mechanism. Cancer Biol. Ther., 2009, 8(20), 1904-1913.
[http://dx.doi.org/10.4161/cbt.8.20.9436] [PMID: 19770576]
[73]
Okuda, K.; Umemura, A.; Kataoka, S.; Yano, K.; Takahashi, A.; Okishio, S.; Taketani, H.; Seko, Y.; Nishikawa, T.; Yamaguchi, K.; Moriguchi, M.; Nakagawa, H.; Liu, Y.; Mitsumoto, Y.; Kanbara, Y.; Shima, T.; Okanoue, T.; Itoh, Y. Enhanced antitumor effect in liver cancer by amino acid depletion-induced oxidative stress. Front. Oncol., 2021, 11, 758549.
[http://dx.doi.org/10.3389/fonc.2021.758549] [PMID: 34796113]
[74]
Paech, F.; Mingard, C.; Grünig, D.; Abegg, V.F.; Bouitbir, J.; Krähenbühl, S. Mechanisms of mitochondrial toxicity of the kinase inhibitors ponatinib, regorafenib and sorafenib in human hepatic HepG2 cells. Toxicology, 2018, 395, 34-44.
[http://dx.doi.org/10.1016/j.tox.2018.01.005] [PMID: 29341879]
[75]
Coriat, R.; Nicco, C.; Chéreau, C.; Mir, O.; Alexandre, J.; Ropert, S.; Weill, B.; Chaussade, S.; Goldwasser, F.; Batteux, F. Sorafenib-induced hepatocellular carcinoma cell death depends on reactive oxygen species production in vitro and in vivo. Mol. Cancer Ther., 2012, 11(10), 2284-2293.
[http://dx.doi.org/10.1158/1535-7163.MCT-12-0093] [PMID: 22902857]
[76]
Li, Z.; Dai, H.; Huang, X.; Feng, J.; Deng, J.; Wang, Z.; Yang, X.; Liu, Y.; Wu, Y.; Chen, P.; Shi, H.; Wang, J.; Zhou, J.; Lu, G. Artesunate synergizes with sorafenib to induce ferroptosis in hepatocellular carcinoma. Acta Pharmacol. Sin., 2021, 42(2), 301-310.
[http://dx.doi.org/10.1038/s41401-020-0478-3] [PMID: 32699265]
[77]
Prieto-Domínguez, N.; Ordóñez, R.; Fernández, A.; Méndez-Blanco, C.; Baulies, A.; Garcia-Ruiz, C.; Fernández-Checa, J.C.; Mauriz, J.L.; González-Gallego, J. Melatonin-induced increase in sensitivity of human hepatocellular carcinoma cells to sorafenib is associated with reactive oxygen species production and mitophagy. J. Pineal Res., 2016, 61(3), 396-407.
[http://dx.doi.org/10.1111/jpi.12358] [PMID: 27484637]
[78]
Ding, Z.B.; Hui, B.; Shi, Y.H.; Zhou, J.; Peng, Y.F.; Gu, C.Y.; Yang, H.; Shi, G.M.; Ke, A.W.; Wang, X.Y.; Song, K.; Dai, Z.; Shen, Y.H.; Fan, J. Autophagy activation in hepatocellular carcinoma contributes to the tolerance of oxaliplatin via reactive oxygen species modulation. Clin. Cancer Res., 2011, 17(19), 6229-6238.
[http://dx.doi.org/10.1158/1078-0432.CCR-11-0816] [PMID: 21825039]
[79]
Guo, X.; Li, D.; Sun, K.; Wang, J.; Liu, Y.; Song, J.; Zhao, Q.; Zhang, S.; Deng, W.; Zhao, X.; Wu, M.; Wei, L. Inhibition of autophagy enhances anticancer effects of bevacizumab in hepatocarcinoma. J. Mol. Med., 2013, 91(4), 473-483.
[http://dx.doi.org/10.1007/s00109-012-0966-0] [PMID: 23052483]
[80]
Li, Y.; Zhang, J.; Zhang, K.; Chen, Y.; Wang, W.; Chen, H.; Zou, Z.; Li, Y.; Dai, M. Scutellaria barbata inhibits hepatocellular carcinoma tumorigenicity by inducing ferroptosis of hepatocellular carcinoma cells. Front. Oncol., 2022, 12, 693395.
[http://dx.doi.org/10.3389/fonc.2022.693395] [PMID: 35321425]
[81]
Liu, C.; Gong, K.; Mao, X.; Li, W. Tetrandrine induces apoptosis by activating reactive oxygen species and repressing Akt activity in human hepatocellular carcinoma. Int. J. Cancer, 2011, 129(6), 1519-1531.
[http://dx.doi.org/10.1002/ijc.25817] [PMID: 21128229]
[82]
Cucarull, B.; Tutusaus, A.; Hernáez-Alsina, T.; García de Frutos, P.; Reig, M.; Colell, A.; Marí, M.; Morales, A. Antioxidants threaten multikinase inhibitor efficacy against liver cancer by blocking mitochondrial reactive oxygen species. Antioxidants, 2021, 10(9), 1336.
[http://dx.doi.org/10.3390/antiox10091336] [PMID: 34572967]
[83]
Lim, S.C.; Choi, J.E.; Kang, H.S.; Si, H. Ursodeoxycholic acid switches oxaliplatin-induced necrosis to apoptosis by inhibiting reactive oxygen species production and activating p53-caspase 8 pathway in HepG2 hepatocellular carcinoma. Int. J. Cancer, 2009, 126(7) NA
[http://dx.doi.org/10.1002/ijc.24853] [PMID: 19728331]
[84]
Xu, J.; Ji, L.; Ruan, Y.; Wan, Z.; Lin, Z.; Xia, S.; Tao, L.; Zheng, J.; Cai, L.; Wang, Y.; Liang, X.; Cai, X. UBQLN1 mediates sorafenib resistance through regulating mitochondrial biogenesis and ROS homeostasis by targeting PGC1β in hepatocellular carcinoma. Signal Transduct. Target. Ther., 2021, 6(1), 190.
[http://dx.doi.org/10.1038/s41392-021-00594-4] [PMID: 34001851]
[85]
Lee, H.A.; Chu, K.B.; Moon, E.K.; Kim, S.S.; Quan, F.S. Sensitization to oxidative stress and G2/M cell cycle arrest by histone deacetylase inhibition in hepatocellular carcinoma cells. Free Radic. Biol. Med., 2020, 147, 129-138.
[http://dx.doi.org/10.1016/j.freeradbiomed.2019.12.021] [PMID: 31870798]
[86]
Shen, J.; Chen, M.; Lee, D.; Law, C.T.; Wei, L.; Tsang, F.H.C.; Chin, D.W.C.; Cheng, C.L.H.; Lee, J.M.F.; Ng, I.O.L.; Wong, C.C.L.; Wong, C.M. Histone chaperone FACT complex mediates oxidative stress response to promote liver cancer progression. Gut, 2020, 69(2), 329-342.
[http://dx.doi.org/10.1136/gutjnl-2019-318668] [PMID: 31439637]
[87]
Xu, I.M.J.; Lai, R.K.H.; Lin, S.H.; Tse, A.P.W.; Chiu, D.K.C.; Koh, H.Y.; Law, C.T.; Wong, C.M.; Cai, Z.; Wong, C.C.L.; Ng, I.O.L. Transketolase counteracts oxidative stress to drive cancer development. Proc. Natl. Acad. Sci., 2016, 113(6), E725-E734.
[http://dx.doi.org/10.1073/pnas.1508779113] [PMID: 26811478]
[88]
Wei, L.; Lee, D.; Law, C.T.; Zhang, M.S.; Shen, J.; Chin, D.W.C.; Zhang, A.; Tsang, F.H.C.; Wong, C.L.S.; Ng, I.O.L.; Wong, C.C.L.; Wong, C.M. Genome-wide CRISPR/Cas9 library screening identified PHGDH as a critical driver for Sorafenib resistance in HCC. Nat. Commun., 2019, 10(1), 4681.
[http://dx.doi.org/10.1038/s41467-019-12606-7] [PMID: 31615983]
[89]
Huang, X.F.; Sheu, G.T.; Chang, K.F.; Huang, Y.C.; Hung, P.H.; Tsai, N.M. Pogostemon cablin triggered ROS-Induced DNA damage to arrest cell cycle progression and induce apoptosis on human hepatocellular carcinoma in vitro and in vivo. Molecules, 2020, 25(23), 5639.
[http://dx.doi.org/10.3390/molecules25235639] [PMID: 33266043]
[90]
Moloney, J.N.; Cotter, T.G. ROS signalling in the biology of cancer. Semin. Cell Dev. Biol., 2018, 80, 50-64.
[http://dx.doi.org/10.1016/j.semcdb.2017.05.023] [PMID: 28587975]
[91]
Brenner, C.; Galluzzi, L.; Kepp, O.; Kroemer, G. Decoding cell death signals in liver inflammation. J. Hepatol., 2013, 59(3), 583-594.
[http://dx.doi.org/10.1016/j.jhep.2013.03.033] [PMID: 23567086]
[92]
Lu, C.S.; Lin, C.W.; Chang, Y.H.; Chen, H.Y.; Chung, W.C.; Lai, W.Y.; Ho, C.C.; Wang, T.H.; Chen, C.Y.; Yeh, C.L.; Wu, S.; Wang, S.P.; Yang, P.C. Antimetabolite pemetrexed primes a favorable tumor microenvironment for immune checkpoint blockade therapy. J. Immunother. Cancer, 2020, 8(2), e001392.
[http://dx.doi.org/10.1136/jitc-2020-001392] [PMID: 33243934]
[93]
Teppo, H.R.; Soini, Y.; Karihtala, P. Reactive oxygen species-mediated mechanisms of action of targeted cancer therapy. Oxid. Med. Cell. Longev., 2017, 2017, 1-11.
[http://dx.doi.org/10.1155/2017/1485283] [PMID: 28698765]

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