Research advances in immunotherapy combined with DNA damage response inhibitors for liver cancer therapy

Chen Yang , Tao Tao , Yijie Wu , Weijie Wang , Song-Bai Liu

Journal of Cancer Metastasis and Treatment ›› 2024, Vol. 10 : 14

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Journal of Cancer Metastasis and Treatment ›› 2024, Vol. 10:14 DOI: 10.20517/2394-4722.2023.175
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Research advances in immunotherapy combined with DNA damage response inhibitors for liver cancer therapy

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Abstract

Cancer immunotherapy utilizes checkpoint inhibitors to amplify the antitumor immune response. The DNA damage repair system plays a crucial role in preserving genome stability, offering therapeutic avenues for tumor treatment by impeding the DNA damage repair pathway. In cancer immunotherapy, checkpoint inhibitors are used to enhance the antitumor immune response. The DNA damage response (DDR) and immune response are inseparably intertwined and have the potential for synergy. Various recent studies have demonstrated that DDR inhibitors (DDRis) can substantially enhance the clinical efficacy of immunotherapy for hepatocellular carcinoma (HCC) by enhancing the immune response of cancer cells. This article primarily describes the immunotherapy of HCC and compiles the research findings and advancements in clinical applications of combined immunotherapy with DDRis. This study provides insight into the application of the DDR pathway in immunotherapy and provides invaluable insights for the clinical advancement of precise and efficacious treatment strategies.

Keywords

Immunotherapy / DNA damage repair / hepatocellular carcinoma

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Chen Yang, Tao Tao, Yijie Wu, Weijie Wang, Song-Bai Liu. Research advances in immunotherapy combined with DNA damage response inhibitors for liver cancer therapy. Journal of Cancer Metastasis and Treatment, 2024, 10: 14 DOI:10.20517/2394-4722.2023.175

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References

[1]

Siegel RL,Jemal A.Cancer statistics, 2019.CA Cancer J Clin2019;69:7-34

[2]

Anwanwan D,Singh S,Singh R.Challenges in liver cancer and possible treatment approaches.Biochim Biophys Acta Rev Cancer2020;1873:188314 PMCID:PMC6981221

[3]

Racanelli V.The liver as an immunological organ.Hepatology2006;43:S54-62

[4]

Nishida N.Oncogenic signal and tumor microenvironment in hepatocellular carcinoma.Oncology2017;93 Suppl 1:160-4

[5]

Donne R.The liver cancer immune microenvironment: therapeutic implications for hepatocellular carcinoma.Hepatology2023;77:1773-96 PMCID:PMC9941399

[6]

Li H,Qu X.Establishment and validation of a novel lysosome-related gene signature for predicting prognosis and immune landscape in hepatocellular carcinoma.J Cancer Res Clin Oncol2023;149:17543-57

[7]

Li X,Pfister D,Zender L.The immunological and metabolic landscape in primary and metastatic liver cancer.Nat Rev Cancer2021;21:541-57

[8]

Degasperi E.Distinctive features of hepatocellular carcinoma in non-alcoholic fatty liver disease.Lancet Gastroenterol Hepatol2016;1:156-64

[9]

Marengo A,Bugianesi E.Liver cancer: connections with obesity, fatty liver, and cirrhosis.Annu Rev Med2016;67:103-17

[10]

Sim HW.Hepatocellular carcinoma in the era of immunotherapy.Curr Probl Cancer2018;42:40-8

[11]

Pennock GK.The evolving role of immune checkpoint inhibitors in cancer treatment.Oncologist2015;20:812-22 PMCID:PMC4492230

[12]

Reig M,Rimola J.BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update.J Hepatol2022;76:681-93 PMCID:PMC8866082

[13]

Galluzzi L,Buqué A,Kroemer G.Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors.Nat Rev Clin Oncol2020;17:725-41

[14]

Xing R,Cui Q.Strategies to improve the antitumor effect of immunotherapy for hepatocellular carcinoma.Front Immunol2021;12:783236 PMCID:PMC8660685

[15]

Shi C,Lin A.The role of DNA damage repair (DDR) system in response to immune checkpoint inhibitor (ICI) therapy.J Exp Clin Cancer Res2022;41:268 PMCID:PMC9450390

[16]

Rizzo A.PD-L1, TMB, and other potential predictors of response to immunotherapy for hepatocellular carcinoma: how can they assist drug clinical trials?.Expert Opin Investig Drugs2022;31:415-23

[17]

O’Connor MJ.Targeting the DNA damage response in cancer.Mol Cell2015;60:547-60

[18]

Carusillo A.DNA damage: from threat to treatment.Cells2020;9:1665 PMCID:PMC7408370

[19]

Cleary JM,Shapiro GI.Biomarker-guided development of DNA repair inhibitors.Mol Cell2020;78:1070-85 PMCID:PMC7316088

[20]

Jiang M,Wang L.Alterations of DNA damage response pathway: biomarker and therapeutic strategy for cancer immunotherapy.Acta Pharm Sin B2021;11:2983-94 PMCID:PMC8546664

[21]

DuBray BJ., Chapman WC, Anderson CD. Hepatocellular carcinoma: a review of the surgical approaches to management.Mo Med2011;108:195-8.

[22]

Worlikar T,Vlaisavljevich E.Effects of histotripsy on local tumor progression in an in vivo orthotopic rodent liver tumor model.BME Front2020;2020:9830304

[23]

O'Leary C,Soulen MC.Curative-intent therapies in localized hepatocellular carcinoma.Curr Treat Options Oncol2020;21:31

[24]

Hartke J,Ghabril M.The diagnosis and treatment of hepatocellular carcinoma.Semin Diagn Pathol2017;34:153-9

[25]

Sunaga N,Kasahara N.Targeting oncogenic KRAS in non-small-cell lung cancer.Cancers2021;13:5956 PMCID:PMC8656763

[26]

Greten TF,Li G.Targeted and Immune-Based Therapies for Hepatocellular Carcinoma.Gastroenterology2019;156:510-24 PMCID:PMC6340758

[27]

Chang Y,Young Jang J.Recent updates of transarterial chemoembolilzation in hepatocellular carcinoma.Int J Mol Sci2020;21:8165 PMCID:PMC7662786

[28]

Chiang CL,Chan KSK.Sequential transarterial chemoembolisation and stereotactic body radiotherapy followed by immunotherapy as conversion therapy for patients with locally advanced, unresectable hepatocellular carcinoma (START-FIT): a single-arm, phase 2 trial.Lancet Gastroenterol Hepatol2023;8:169-78

[29]

Li SH,Cheng Y.Postoperative adjuvant hepatic arterial infusion chemotherapy with FOLFOX in hepatocellular carcinoma with microvascular invasion: a multicenter, phase III, randomized study.J Clin Oncol2023;41:1898-908 PMCID:PMC10082249

[30]

Yuan Y,Yang Z.TACE-HAIC combined with targeted therapy and immunotherapy versus TACE alone for hepatocellular carcinoma with portal vein tumour thrombus: a propensity score matching study.Int J Surg2023;109:1222-30 PMCID:PMC10389515

[31]

Zhu ZX,Liao MH.Treatment strategy for hepatocellular carcinoma in China: radiofrequency ablation versus liver resection.Jpn J Clin Oncol2016;46:1075-80

[32]

Wang J,Sun M.Deep segmentation feature-based radiomics improves recurrence prediction of hepatocellular carcinoma.BME Front2022;2022:9793716 PMCID:PMC10521680

[33]

Feng M.Radiation therapy for hepatocellular carcinoma.Semin Radiat Oncol2011;21:271-7

[34]

Sanuki N,Oku Y.Stereotactic body radiotherapy for small hepatocellular carcinoma: a retrospective outcome analysis in 185 patients.Acta Oncol2014;53:399-404

[35]

Wu F,Dong D.Phase 2 evaluation of neoadjuvant intensity-modulated radiotherapy in centrally located hepatocellular carcinoma: a nonrandomized controlled trial.JAMA Surg2022;157:1089-96 PMCID:PMC9535533

[36]

Huang A,Chung WY,Zhou J.Targeted therapy for hepatocellular carcinoma.Signal Transduct Target Ther2020;5:146 PMCID:PMC7419547

[37]

Feng MY,Chan SL.Drug treatment for advanced hepatocellular carcinoma: first-line and beyond.Curr Oncol2022;29:5489-507 PMCID:PMC9406660

[38]

Obi S,Toune R.Combination therapy of intraarterial 5-fluorouracil and systemic interferon-alpha for advanced hepatocellular carcinoma with portal venous invasion.Cancer2006;106:1990-7

[39]

Oura K,Tani J.Tumor immune microenvironment and immunosuppressive therapy in hepatocellular carcinoma: a review.Int J Mol Sci2021;22:5801 PMCID:PMC8198390

[40]

Sharma A,Dutertre CA.Onco-fetal reprogramming of endothelial cells drives immunosuppressive macrophages in hepatocellular carcinoma.Cell2020;183:377-94.e21

[41]

Lee HW,Park JY.Current status and future direction of immunotherapy in hepatocellular carcinoma: what do the data suggest?.Immune Netw2020;20:e11 PMCID:PMC7049588

[42]

Chen C,Ding Y.Tumor microenvironment-mediated immune evasion in hepatocellular carcinoma.Front Immunol2023;14:1133308 PMCID:PMC9950271

[43]

Sangro B,Hervás-Stubbs S.Advances in immunotherapy for hepatocellular carcinoma.Nat Rev Gastroenterol Hepatol2021;18:525-43 PMCID:PMC8042636

[44]

De Martin E,Papouin B.Characterization of liver injury induced by cancer immunotherapy using immune checkpoint inhibitors.J Hepatol2018;68:1181-90

[45]

Chamoto K,Honjo T.Role of PD-1 in immunity and diseases. In: Yoshimura A, editor. Emerging concepts targeting immune checkpoints in cancer and autoimmunity. Cham: Springer International Publishing; 2017. pp. 75-97.

[46]

Sato H,Shibata A.Regulation of programmed death-ligand 1 expression in response to DNA damage in cancer cells: Implications for precision medicine.Cancer Sci2019;110:3415-23 PMCID:PMC6824998

[47]

Li Q,Yang Y.PD-1/PD-L1 checkpoint inhibitors in advanced hepatocellular carcinoma immunotherapy.Front Immunol2022;13:1070961 PMCID:PMC9806143

[48]

Khan M,Wang H.NK cell-based immune checkpoint inhibition.Front Immunol2020;11:167 PMCID:PMC7031489

[49]

Liu Y,Xu Y.Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers.Oncogene2017;36:6143-53 PMCID:PMC5671935

[50]

Shiravand Y,Kashani SMA.Immune checkpoint inhibitors in cancer therapy.Curr Oncol2022;29:3044-60 PMCID:PMC9139602

[51]

Kudo M,Edeline J.KEYNOTE-224 InvestigatorsUpdated efficacy and safety of KEYNOTE-224: a phase II study of pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib.Eur J Cancer2022;167:1-12

[52]

Castria TB, Khalil DN, Harding JJ, O'Reilly EM, Abou-Alfa GK. Tremelimumab and durvalumab in the treatment of unresectable, advanced hepatocellular carcinoma.Future Oncol2022;18:3769-82

[53]

Xiang YJ,Yu HM.Transarterial chemoembolization plus a PD-1 inhibitor with or without lenvatinib for intermediate-stage hepatocellular carcinoma.Hepatol Res2022;52:721-9

[54]

Finn RS.Evolution of Systemic Therapy for Hepatocellular Carcinoma.Hepatology2021;73 Suppl 1:150-7

[55]

Mody K.Systemic Therapy for Advanced Hepatocellular Carcinoma in an Evolving Landscape.Curr Treat Options Oncol2019;20:3

[56]

Qin S,Gu S.CARES-310 Study GroupCamrelizumab plus rivoceranib versus sorafenib as first-line therapy for unresectable hepatocellular carcinoma (CARES-310): a randomised, open-label, international phase 3 study.Lancet2023;402:1133-46

[57]

Kaufmann DE,Pereyra F.Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction.Nat Immunol2007;8:1246-54

[58]

Song X,Khan AA.Exposure-response analyses of tremelimumab monotherapy or in combination with durvalumab in patients with unresectable hepatocellular carcinoma.Clin Cancer Res2023;29:754-63

[59]

Zhao M,Mi L.Prognosis of hepatocellular carcinoma and its association with immune cells using systemic inflammatory response index.Future Oncol2022;18:2269-88

[60]

Yau T,Kim TY.Efficacy and safety of nivolumab plus ipilimumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib: the checkmate 040 randomized clinical trial.JAMA Oncol2020;6:e204564 PMCID:PMC7530824

[61]

Li X,Chen X.Efficacy and safety of lenvatinib combined with PD-1 inhibitors plus TACE for unresectable hepatocellular carcinoma patients in china real-world.Front Oncol2022;12:950266 PMCID:PMC9289205

[62]

Li L,Teng YX.Second-line treatment options for hepatocellular carcinoma: current state and challenges for the future.Expert Opin Investig Drugs2022;31:1151-67

[63]

Finn RS,Ikeda M.IMbrave150 InvestigatorsAtezolizumab plus bevacizumab in unresectable hepatocellular carcinoma.N Engl J Med2020;382:1894-905

[64]

Liu X,Qin S.Atezolizumab and bevacizumab for hepatocellular carcinoma: mechanism, pharmacokinetics and future treatment strategies.Future Oncol2021;17:2243-56

[65]

Xin Y,Liu N.Efficacy and safety of lenvatinib plus PD-1 inhibitor with or without transarterial chemoembolization in unresectable hepatocellular carcinoma.Hepatol Int2023;17:753-64

[66]

Mei J,Wei W.Hepatic arterial infusion chemotherapy combined with PD-1 inhibitors plus lenvatinib versus pd-1 inhibitors plus lenvatinib for advanced hepatocellular carcinoma.Front Oncol2021;11:618206 PMCID:PMC7947809

[67]

He MK,Zhao Y.Lenvatinib, toripalimab, plus hepatic arterial infusion chemotherapy versus lenvatinib alone for advanced hepatocellular carcinoma.Ther Adv Med Oncol2021;13:17588359211002720 PMCID:PMC8010824

[68]

Hong Y,Sun H.Tislelizumab uniquely binds to the CC' loop of PD-1 with slow-dissociated rate and complete PD-L1 blockage.FEBS Open Bio2021;11:782-92 PMCID:PMC7931243

[69]

Xiao Y,Xie J.Pretreatment neutrophil-to-lymphocyte ratio as prognostic biomarkers in patients with unresectable hepatocellular carcinoma treated with hepatic arterial infusion chemotherapy combined with lenvatinib and camrelizumab.J Hepatocell Carcinoma2023;10:2049-58 PMCID:PMC10642375

[70]

Qin S,Kudo M.RATIONALE 301 study: tislelizumab versus sorafenib as first-line treatment for unresectable hepatocellular carcinoma.Future Oncol2019;15:1811-22

[71]

Qin S,Meng Z.Camrelizumab in patients with previously treated advanced hepatocellular carcinoma: a multicentre, open-label, parallel-group, randomised, phase 2 trial.Lancet Oncol2020;21:571-80

[72]

Yau T,Finn RS.Nivolumab versus sorafenib in advanced hepatocellular carcinoma (CheckMate 459): a randomised, multicentre, open-label, phase 3 trial.Lancet Oncol2022;23:77-90

[73]

Merle P,Edeline J.Pembrolizumab as second-line therapy for advanced hepatocellular carcinoma: longer term follow-up from the phase 3 KEYNOTE-240 trial.Liver Cancer2023;12:309-20 PMCID:PMC10601873

[74]

Zhao Y,Wang KT.Lenvatinib for hepatocellular carcinoma: from preclinical mechanisms to anti-cancer therapy.Biochim Biophys Acta Rev Cancer2020;1874:188391

[75]

Chen R,di Carlo A.Donafenib in hepatocellular carcinoma.Drugs Today2023;59:83-90

[76]

Llovet JM,Villanueva A.Hepatocellular carcinoma.Nat Rev Dis Primers2021;7:6

[77]

Kim HD,Lim HY.Regorafenib plus nivolumab in unresectable hepatocellular carcinoma: the phase 2 RENOBATE trial.Nat Med2024;30:699-707 PMCID:PMC10957471

[78]

Ren Z,Bai Y.ORIENT-32 study groupSintilimab plus a bevacizumab biosimilar (IBI305) versus sorafenib in unresectable hepatocellular carcinoma (ORIENT-32): a randomised, open-label, phase 2-3 study.Lancet Oncol2021;22:977-90

[79]

Zhang T,Wang H,Kudo M.Combination therapy for advanced hepatocellular carcinoma: do we see the light at the end of the tunnel?.Hepatobiliary Surg Nutr2021;10:180-92 PMCID:PMC8050575

[80]

Yau T,Santoro A.Nivolumab plus cabozantinib with or without ipilimumab for advanced hepatocellular carcinoma: results from cohort 6 of the CheckMate 040 trial.J Clin Oncol2023;41:1747-57 PMCID:PMC10022845

[81]

Hatanaka T,Naganuma A.Treatment strategy for intermediate-stage hepatocellular carcinoma: transarterial chemoembolization, systemic therapy, and conversion therapy.Cancers2023;15:1798 PMCID:PMC10046825

[82]

Chatterjee N.Mechanisms of DNA damage, repair, and mutagenesis.Environ Mol Mutagen2017;58:235-63 PMCID:PMC5474181

[83]

Vickridge E,Nepveu A.Base excision repair accessory factors in senescence avoidance and resistance to treatments.Cancer Drug Resist2022;5:703-20 PMCID:PMC9511810

[84]

Li Z,Hsieh P.DNA mismatch repair and the DNA damage response.DNA Repair2016;38:94-101 PMCID:PMC4740233

[85]

Li W,Burke TJ,Lariscy L.Epigenetic regulation of nucleotide excision repair.Front Cell Dev Biol2022;10:847051 PMCID:PMC9023881

[86]

Wright WD,Heyer WD.Homologous recombination and the repair of DNA double-strand breaks.J Biol Chem2018;293:10524-35 PMCID:PMC6036207

[87]

Chang HHY,Adachi N.Non-homologous DNA end joining and alternative pathways to double-strand break repair.Nat Rev Mol Cell Biol2017;18:495-506 PMCID:PMC7062608

[88]

Wang Z,Wang G.Comutations in DNA damage response pathways serve as potential biomarkers for immune checkpoint blockade.Cancer Res2018;78:6486-96

[89]

Bai Y,Ma Y,Li M.Identification of DNA repair gene signature and potential molecular subtypes in hepatocellular carcinoma.Front Oncol2023;13:1180722 PMCID:PMC10227583

[90]

Chen Y,Deng X.DNA damage repair status predicts opposite clinical prognosis immunotherapy and non-immunotherapy in hepatocellular carcinoma.Front Immunol2021;12:676922 PMCID:PMC8320764

[91]

Lin P,Wen R,Yang H.DNA damage repair profiles alteration characterize a hepatocellular carcinoma subtype with unique molecular and clinicopathologic features.Front Immunol2021;12:715460 PMCID:PMC8387599

[92]

Li H,Wu N,Cheng Q.PARP inhibitor resistance: the underlying mechanisms and clinical implications.Mol Cancer2020;19:107 PMCID:PMC7305609

[93]

Singh MP,Kim JT,Lee HG.Morin hydrate reverses cisplatin resistance by impairing PARP1/HMGB1-dependent autophagy in hepatocellular carcinoma.Cancers2019;11:986 PMCID:PMC6678360

[94]

Tong Y,Li S.Histone methyltransferase KMT5C drives liver cancer progression and directs therapeutic response to PARP inhibitors.Hepatology2023;

[95]

Wang M,Ao D.Targeting DNA repair pathway in cancer: mechanisms and clinical application.MedComm2021;2:654-91 PMCID:PMC8706759

[96]

Baxter JS,Pettitt SJ.Resistance to DNA repair inhibitors in cancer.Mol Oncol2022;16:3811-27 PMCID:PMC9627783

[97]

Groelly FJ,Dagg RA,Tarsounas M.Targeting DNA damage response pathways in cancer.Nat Rev Cancer2023;23:78-94

[98]

Cheng B,Xing Y,Chen J.Recent advances in DDR (DNA damage response) inhibitors for cancer therapy.Eur J Med Chem2022;230:114109

[99]

Reisländer T,Tarsounas M.DNA damage and cancer immunotherapy: a STING in the tale.Mol Cell2020;80:21-8

[100]

Yang XD,Qi L.PARP inhibitor Olaparib overcomes Sorafenib resistance through reshaping the pluripotent transcriptome in hepatocellular carcinoma.Mol Cancer2021;20:20 PMCID:PMC7824946

[101]

Hunia J,Szredzka A,Nowis D.The potential of PARP inhibitors in targeted cancer therapy and immunotherapy.Front Mol Biosci2022;9:1073797 PMCID:PMC9751342

[102]

Vikas P,Chennamadhavuni A.Therapeutic potential of combining PARP inhibitor and immunotherapy in solid tumors.Front Oncol2020;10:570 PMCID:PMC7228136

[103]

Sun G,Li Z.Inhibition of PARP potentiates immune checkpoint therapy through miR-513/PD-L1 pathway in hepatocellular carcinoma.J Oncol2022;2022:6988923 PMCID:PMC9020948

[104]

Jin MH.ATM in DNA repair in cancer.Pharmacol Ther2019;203:107391

[105]

Sheng H,Xiao Y.ATR inhibitor AZD6738 enhances the antitumor activity of radiotherapy and immune checkpoint inhibitors by potentiating the tumor immune microenvironment in hepatocellular carcinoma.J Immunother Cancer2020;8:e000340 PMCID:PMC7254123

[106]

Guo Y,Benedict B.Targeting CDC7 potentiates ATR-CHK1 signaling inhibition through induction of DNA replication stress in liver cancer.Genome Med2021;13:166 PMCID:PMC8524847

[107]

Benson AB,Abbott DE.Hepatobiliary cancers, version 2.2021, NCCN clinical practice guidelines in oncology.J Natl Compr Canc Netw2021;19:541-65

[108]

Xu J,Gu S.Camrelizumab in combination with apatinib in patients with advanced hepatocellular carcinoma (RESCUE): a nonrandomized, open-label, phase II trial.Clin Cancer Res2021;27:1003-11

[109]

Sen T,Chen L.Targeting DNA damage response promotes antitumor immunity through STING-mediated T-cell activation in small cell lung cancer.Cancer Discov2019;9:646-61 PMCID:PMC6563834

[110]

Qiu Z,Zhang J.ATR/CHK1 inhibitors and cancer therapy.Radiother Oncol2018;126:450-64 PMCID:PMC5856582

[111]

Drew Y,Penson RT.MEDIOLA InvestigatorsOlaparib plus durvalumab, with or without bevacizumab, as treatment in PARP inhibitor-naïve platinum-sensitive relapsed ovarian cancer: a phase ii multi-cohort study.Clin Cancer Res2024;30:50-62 PMCID:PMC10767301

[112]

Konstantinopoulos PA,Vidal GA.Single-arm phases 1 and 2 trial of niraparib in combination with pembrolizumab in patients with recurrent platinum-resistant ovarian carcinoma.JAMA Oncol2019;5:1141-9 PMCID:PMC6567832

[113]

Konyn P,Kim D.Current epidemiology in hepatocellular carcinoma.Expert Rev Gastroenterol Hepatol2021;15:1295-307

[114]

Yang WS,Liu ZN.Diet and liver cancer risk: a narrative review of epidemiological evidence.Br J Nutr2020;124:330-40

[115]

Ogino S,Chan AT.Molecular pathological epidemiology of epigenetics: emerging integrative science to analyze environment, host, and disease.Mod Pathol2013;26:465-84 PMCID:PMC3637979

[116]

Li L.Heterogeneity of liver cancer and personalized therapy.Cancer Lett2016;379:191-7

[117]

Chuang SC,Boffetta P.Liver cancer: descriptive epidemiology and risk factors other than HBV and HCV infection.Cancer Lett2009;286:9-14

[118]

Ueyama M,Korenaga M.The impact of PNPLA3 and JAZF1 on hepatocellular carcinoma in non-viral hepatitis patients with type 2 diabetes mellitus.J Gastroenterol2016;51:370-9

[119]

Cichoż-Lach H.Oxidative stress as a crucial factor in liver diseases.World J Gastroenterol2014;20:8082-91 PMCID:PMC4081679

[120]

Cesaratto L,Calligaris S.The importance of redox state in liver damage.Ann Hepatol2004;3:86-92.

[121]

Wang X,Lin H,Zhang Z.Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling.Open Life Sci2023;18:20220618 PMCID:PMC10276545

[122]

Karabekir SC.Possible protective effects of resveratrol in hepatocellular carcinoma.Iran J Basic Med Sci2020;23:71-8 PMCID:PMC7206832

[123]

Li S,Xu X,Zhang L.Nanocarrier-mediated antioxidant delivery for liver diseases.Theranostics2020;10:1262-80 PMCID:PMC6956819

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