An Overview of Hepatocellular Carcinoma After Insufficient Radiofrequency Ablation

References

• European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236. doi:10.1016/j.jhep.2018.03.019
   PubMed Web of Science ®Google Scholar
• Luo W, Zhang Y, He G, et al. Effects of radiofrequency ablation versus other ablating techniques on hepatocellular carcinomas: a systematic review and meta-analysis. World J Surg Oncol. 2017;15(1):126. doi:10.1186/s12957-017-1196-2
   PubMed Web of Science ®Google Scholar
• Minami Y, Nishida N, Kudo M. Radiofrequency ablation of liver metastasis: potential impact on immune checkpoint inhibitor therapy. Eur Radiol. 2019;29(9):5045–5051. doi:10.1007/s00330-019-06189-6
   PubMed Web of Science ®Google Scholar
• Shady W, Petre EN, Gonen M, et al. Percutaneous radiofrequency ablation of colorectal cancer liver metastases: factors affecting outcomes–A 10-year experience at a single center. Radiology. 2016;278(2):601–611. doi:10.1148/radiol.2015142489
   PubMed Web of Science ®Google Scholar
• Cucchetti A, Piscaglia F, Cescon M, et al. Cost-effectiveness of hepatic resection versus percutaneous radiofrequency ablation for early hepatocellular carcinoma. J Hepatol. 2013;59(2):300–307. doi:10.1016/j.jhep.2013.04.009
   PubMed Web of Science ®Google Scholar
• Cheung TT, Ma KW, She WH. A review on radiofrequency, microwave and high-intensity focused ultrasound ablations for hepatocellular carcinoma with cirrhosis. Hepatobiliary Surg Nutr. 2021;10(2):193–209. doi:10.21037/hbsn.2020.03.11
   PubMed Web of Science ®Google Scholar
• Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A, Roberts LR. A global view of hepatocellular carcinoma: trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol. 2019;16(10):589–604. doi:10.1038/s41575-019-0186-y
   PubMed Web of Science ®Google Scholar
• Lee S, Kang TW, Song KD, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg. 2021;273(3):564–571. doi:10.1097/SLA.0000000000003268
   PubMed Web of Science ®Google Scholar
• Lee S, Kang TW, Cha DI, et al. Radiofrequency ablation vs. surgery for perivascular hepatocellular carcinoma: propensity score analyses of long-term outcomes. J Hepatol. 2018;69(1):70–78. doi:10.1016/j.jhep.2018.02.026
   PubMed Web of Science ®Google Scholar
• Kong J, Yao C, Dong S, et al. ICAM-1 activates platelets and promotes endothelial permeability through VE-cadherin after insufficient radiofrequency ablation. Adv Sci. 2021;8(4):2002228. doi:10.1002/advs.202002228
   Web of Science ®Google Scholar
• Huang J, Yan L, Cheng Z, et al. A randomized trial comparing radiofrequency ablation and surgical resection for HCC conforming to the Milan criteria. Ann Surg. 2010;252(6):903–912. doi:10.1097/SLA.0b013e3181efc656
   PubMed Web of Science ®Google Scholar
• Seki T, Tamai T, Ikeda K, et al. Rapid progression of hepatocellular carcinoma after transcatheter arterial chemoembolization and percutaneous radiofrequency ablation in the primary tumour region. Eur J Gastroenterol Hepatol. 2001;13(3):291–294. doi:10.1097/00042737-200103000-00014
   PubMed Web of Science ®Google Scholar
• Koda M, Maeda Y, Matsunaga Y, Mimura K, Murawaki Y, Horie Y. Hepatocellular carcinoma with sarcomatous change arising after radiofrequency ablation for well-differentiated hepatocellular carcinoma. Hepatol Res. 2003;27(2):163–167. doi:10.1016/S1386-6346(03)00207-9
   PubMed Web of Science ®Google Scholar
• Portolani N, Tiberio GA, Ronconi M, et al. Aggressive recurrence after radiofrequency ablation of liver neoplasms. Hepato-Gastroenterology. 2003;50(54):2179–2184.
   PubMedGoogle Scholar
• Takada Y, Kurata M, Ohkohchi N. Rapid and aggressive recurrence accompanied by portal tumor thrombus after radiofrequency ablation for hepatocellular carcinoma. Int J Clin Oncol. 2003;8(5):332–335. doi:10.1007/s10147-003-0328-6
   PubMedGoogle Scholar
• Ruzzenente A, Manzoni GD, Molfetta M, et al. Rapid progression of hepatocellular carcinoma after Radiofrequency Ablation. World j Gastroenterol. 2004;10(8):1137–1140. doi:10.3748/wjg.v10.i8.1137
   PubMed Web of Science ®Google Scholar
• Lam VW, Ng KK, Chok KS, et al. Incomplete ablation after radiofrequency ablation of hepatocellular carcinoma: analysis of risk factors and prognostic factors. Ann Surg Oncol. 2008;15(3):782–790. doi:10.1245/s10434-007-9733-9
   PubMed Web of Science ®Google Scholar
• Ahmed M, Brace CL, Lee FT Jr., Goldberg SN. Principles of and advances in percutaneous ablation. Radiology. 2011;258(2):351–369. doi:10.1148/radiol.10081634
   PubMed Web of Science ®Google Scholar
• Nijkamp MW, Hoogwater FJ, Steller EJ, et al. CD95 is a key mediator of invasion and accelerated outgrowth of mouse colorectal liver metastases following radiofrequency ablation. J Hepatol. 2010;53(6):1069–1077. doi:10.1016/j.jhep.2010.04.040
   PubMed Web of Science ®Google Scholar
• Dong S, Kong J, Kong F, et al. Insufficient radiofrequency ablation promotes epithelial-mesenchymal transition of hepatocellular carcinoma cells through Akt and ERK signaling pathways. J Transl Med. 2013;11(1):273. doi:10.1186/1479-5876-11-273
   PubMed Web of Science ®Google Scholar
• Yoshida S, Kornek M, Ikenaga N, et al. Sublethal heat treatment promotes epithelial-mesenchymal transition and enhances the malignant potential of hepatocellular carcinoma. Hepatology. 2013;58(5):1667–1680. doi:10.1002/hep.26526
   PubMed Web of Science ®Google Scholar
• Zhang N, Wang L, Chai ZT, et al. Incomplete radiofrequency ablation enhances invasiveness and metastasis of residual cancer of hepatocellular carcinoma cell HCCLM3 via activating β-catenin signaling. PLoS One. 2014;9(12):e115949. doi:10.1371/journal.pone.0115949
   PubMed Web of Science ®Google Scholar
• Dong S, Kong J, Kong F, et al. Sorafenib suppresses the epithelial-mesenchymal transition of hepatocellular carcinoma cells after insufficient radiofrequency ablation. BMC Cancer. 2015;15:939. doi:10.1186/s12885-015-1949-7
   PubMed Web of Science ®Google Scholar
• Tong Y, Yang H, Xu X, et al. Effect of a hypoxic microenvironment after radiofrequency ablation on residual hepatocellular cell migration and invasion. Cancer Sci. 2017;108(4):753–762. doi:10.1111/cas.13191
   PubMed Web of Science ®Google Scholar
• Su T, Liao J, Dai Z, et al. Stress-induced phosphoprotein 1 mediates hepatocellular carcinoma metastasis after insufficient radiofrequency ablation. Oncogene. 2018;37(26):3514–3527. doi:10.1038/s41388-018-0169-4
   PubMed Web of Science ®Google Scholar
• Zeng J, Cai X, Hao X, et al. LncRNA FUNDC2P4 down-regulation promotes epithelial-mesenchymal transition by reducing E-cadherin expression in residual hepatocellular carcinoma after insufficient radiofrequency ablation. Int j Hyperthermia. 2018;34(6):802–811. doi:10.1080/02656736.2017.1422030
   PubMed Web of Science ®Google Scholar
• Zhang R, Lin XH, Ma M, et al. Periostin involved in the activated hepatic stellate cells-induced progression of residual hepatocellular carcinoma after sublethal heat treatment: its role and potential for therapeutic inhibition. J Transl Med. 2018;16(1):302. doi:10.1186/s12967-018-1676-3
   PubMed Web of Science ®Google Scholar
• Zhang R, Ma M, Lin XH, et al. Extracellular matrix collagen I promotes the tumor progression of residual hepatocellular carcinoma after heat treatment. BMC Cancer. 2018;18(1):901. doi:10.1186/s12885-018-4820-9
   PubMed Web of Science ®Google Scholar
• Zhang N, Li H, Qin C, et al. Insufficient radiofrequency ablation promotes the metastasis of residual hepatocellular carcinoma cells via upregulating flotillin proteins. J Cancer Res Clin Oncol. 2019;145(4):895–907. doi:10.1007/s00432-019-02852-z
   PubMed Web of Science ®Google Scholar
• Kong J, Yao C, Ding X, et al. ATPase inhibitory factor 1 promotes hepatocellular carcinoma progression after insufficient radiofrequency ablation, and attenuates cell sensitivity to sorafenib therapy. Front Oncol. 2020;10:1080. doi:10.3389/fonc.2020.01080
   PubMed Web of Science ®Google Scholar
• Li Z, Jiang M, Zhang T, Liu S. GAS6-AS2 promotes hepatocellular carcinoma via miR-3619-5p/ARL2 axis under insufficient radiofrequency ablation condition. Cancer Biother Radiopharm. 2020;36:879–889.
   PubMed Web of Science ®Google Scholar
• Ma D, Gao X, Liu Z, Lu X, Ju H, Zhang N. Exosome-transferred long non-coding RNA ASMTL-AS1 contributes to malignant phenotypes in residual hepatocellular carcinoma after insufficient radiofrequency ablation. Cell Prolif. 2020;53(9):e12795. doi:10.1111/cpr.12795
   PubMed Web of Science ®Google Scholar
• Zhou T, Liu B, Wang Y, et al. Insufficient radiofrequency ablation promotes epithelial-mesenchymal transition mediated by interleukin-6/signal transducer and activator of transcription 3/Snail pathway in the H22 cells. J Cancer Res Ther. 2020;16(5):1112–1118. doi:10.4103/jcrt.JCRT_12_20
   PubMed Web of Science ®Google Scholar
• Chen Y, Bei J, Liu M, et al. Sublethal heat stress-induced O-GlcNAcylation coordinates the Warburg effect to promote hepatocellular carcinoma recurrence and metastasis after thermal ablation. Cancer Lett. 2021;518:23–34. doi:10.1016/j.canlet.2021.06.001
   PubMed Web of Science ®Google Scholar
• Fan Z, Gao Y, Zhang W, et al. METTL3/IGF2BP1/CD47 contributes to the sublethal heat treatment induced mesenchymal transition in HCC. Biochem Biophys Res Commun. 2021;546:169–177. doi:10.1016/j.bbrc.2021.01.085
   PubMed Web of Science ®Google Scholar
• Su T, Huang M, Liao J, et al. Insufficient radiofrequency ablation promotes hepatocellular carcinoma metastasis through N6-Methyladenosine mRNA methylation-dependent mechanism. Hepatology. 2021;74(3):1339–1356. doi:10.1002/hep.31766
   PubMed Web of Science ®Google Scholar
• Wang X, Deng Q, Feng K, et al. Insufficient radiofrequency ablation promotes hepatocellular carcinoma cell progression via autophagy and the CD133 feedback loop. Oncol Rep. 2018;40(1):241–251. doi:10.3892/or.2018.6403
   PubMed Web of Science ®Google Scholar
• Zhao Z, Wu J, Liu X, et al. Insufficient radiofrequency ablation promotes proliferation of residual hepatocellular carcinoma via autophagy. Cancer Lett. 2018;421:73–81. doi:10.1016/j.canlet.2018.02.024
   PubMed Web of Science ®Google Scholar
• Chen F, Bao H, Xie H, Tian G, Jiang T. Heat shock protein expression and autophagy after incomplete thermal ablation and their correlation. Int j Hyperthermia. 2019;36(1):95–103. doi:10.1080/02656736.2018.1536285
   PubMed Web of Science ®Google Scholar
• Jiang J, Chen S, Li K, et al. Targeting autophagy enhances heat stress-induced apoptosis via the ATP-AMPK-mTOR axis for hepatocellular carcinoma. Int J Hyperthermia. 2019;36(1):499–510. doi:10.1080/02656736.2019.1600052
   PubMed Web of Science ®Google Scholar
• Xu WL, Wang SH, Sun WB, et al. Insufficient radiofrequency ablation-induced autophagy contributes to the rapid progression of residual hepatocellular carcinoma through the HIF-1α/BNIP3 signaling pathway. BMB Rep. 2019;52(4):277–282. doi:10.5483/BMBRep.2019.52.4.263
   PubMed Web of Science ®Google Scholar
• Zhang R, Lin XH, Liu HH, et al. Activated hepatic stellate cells promote progression of post-heat residual hepatocellular carcinoma from autophagic survival to proliferation. Int J Hyperthermia. 2019;36(1):253–263. doi:10.1080/02656736.2018.1558459
   PubMed Web of Science ®Google Scholar
• Chen F, Xie H, Bao H, Violetta L, Zheng S. Combination of HSP90 and autophagy inhibitors promotes hepatocellular carcinoma apoptosis following incomplete thermal ablation. Mol Med Rep. 2020;22(1):337–343. doi:10.3892/mmr.2020.11080
   PubMed Web of Science ®Google Scholar
• Li Q, Ni Y, Zhang L, et al. HIF-1α-induced expression of m6A reader YTHDF1 drives hypoxia-induced autophagy and malignancy of hepatocellular carcinoma by promoting ATG2A and ATG14 translation. Signal Transduct Targeted Ther. 2021;6(1):76. doi:10.1038/s41392-020-00453-8
   PubMed Web of Science ®Google Scholar
• Zhang R, Yao RR, Li JH, et al. Activated hepatic stellate cells secrete periostin to induce stem cell-like phenotype of residual hepatocellular carcinoma cells after heat treatment. Sci Rep. 2017;7(1):2164. doi:10.1038/s41598-017-01177-6
   PubMed Web of Science ®Google Scholar
• Tan L, Chen S, Wei G, et al. Sublethal heat treatment of hepatocellular carcinoma promotes intrahepatic metastasis and stemness in a VEGFR1-dependent manner. Cancer Lett. 2019;460:29–40. doi:10.1016/j.canlet.2019.05.041
   PubMed Web of Science ®Google Scholar
• Zaimoku R, Miyashita T, Tajima H, et al. Monitoring of heat shock response and phenotypic changes in hepatocellular carcinoma after heat treatment. Anticancer Res. 2019;39(10):5393–5401. doi:10.21873/anticanres.13733
   PubMed Web of Science ®Google Scholar
• Kong J, Kong J, Pan B, et al. Insufficient radiofrequency ablation promotes angiogenesis of residual hepatocellular carcinoma via HIF-1α/VEGFA. PLoS One. 2012;7(5):e37266. doi:10.1371/journal.pone.0037266
   PubMed Web of Science ®Google Scholar
• Xu M, Xie XH, Xie XY, et al. Sorafenib suppresses the rapid progress of hepatocellular carcinoma after insufficient radiofrequency ablation therapy: an experiment in vivo. Acta Radiol. 2013;54(2):199–204. doi:10.1258/ar.2012.120249
   PubMed Web of Science ®Google Scholar
• Wu L, Fu Z, Zhou S, et al. HIF-1α and HIF-2α: siblings in promoting angiogenesis of residual hepatocellular carcinoma after high-intensity focused ultrasound ablation. PLoS One. 2014;9(2):e88913. doi:10.1371/journal.pone.0088913
   PubMed Web of Science ®Google Scholar
• Rozenblum N, Zeira E, Scaiewicz V, et al. Oncogenesis: an “Off-Target” effect of radiofrequency ablation. Radiology. 2015;276(2):426–432. doi:10.1148/radiol.2015141695
   PubMed Web of Science ®Google Scholar
• Shi L, Wang J, Ding N, et al. Inflammation induced by incomplete radiofrequency ablation accelerates tumor progression and hinders PD-1 immunotherapy. Nat Commun. 2019;10(1):5421. doi:10.1038/s41467-019-13204-3
   PubMed Web of Science ®Google Scholar
• Sun C, Bai M, Ke W, Wang X, Zhao X, Lu Z. The HSP90 inhibitor, XL888, enhanced cell apoptosis via downregulating STAT3 after insufficient radiofrequency ablation in hepatocellular carcinoma. Life Sci. 2021;282:119762. doi:10.1016/j.lfs.2021.119762
   PubMed Web of Science ®Google Scholar
• Ke S, Ding XM, Kong J, et al. Low temperature of radiofrequency ablation at the target sites can facilitate rapid progression of residual hepatic VX2 carcinoma. J Transl Med. 2010;8:73. doi:10.1186/1479-5876-8-73
   PubMed Web of Science ®Google Scholar
• Dai H, Jia G, Wang H, Yang J, Jiang H, Chu M. Epidermal growth factor receptor transactivation is involved in the induction of human hepatoma SMMC7721 cell proliferation by insufficient radiofrequency ablation. Oncol Lett. 2017;14(2):2463–2467. doi:10.3892/ol.2017.6463
   PubMed Web of Science ®Google Scholar
• Thompson SM, Jondal DE, Butters KA, et al. Heat stress induced, ligand-independent MET and EGFR signalling in hepatocellular carcinoma. Int J Hyperthermia. 2018;34(6):812–823. doi:10.1080/02656736.2017.1385859
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang Y, Wang J, Gu H. Amarogentin inhibits liver cancer cell angiogenesis after insufficient radiofrequency ablation via affecting stemness and the p53-dependent VEGFA/Dll4/Notch1 pathway. Biomed Res Int. 2020;2020:5391058. doi:10.1155/2020/5391058
   PubMed Web of Science ®Google Scholar
• Kong J, Kong L, Kong J, et al. After insufficient radiofrequency ablation, tumor-associated endothelial cells exhibit enhanced angiogenesis and promote invasiveness of residual hepatocellular carcinoma. J Transl Med. 2012;10:230. doi:10.1186/1479-5876-10-230
   PubMed Web of Science ®Google Scholar
• Obara K, Matsumoto N, Okamoto M, et al. Insufficient radiofrequency ablation therapy may induce further malignant transformation of hepatocellular carcinoma. Hepatol Int. 2008;2(1):116–123. doi:10.1007/s12072-007-9040-3
   PubMed Web of Science ®Google Scholar
• Nijkamp MW, van der Bilt JD, de Bruijn MT, et al. Accelerated perinecrotic outgrowth of colorectal liver metastases following radiofrequency ablation is a hypoxia-driven phenomenon. Ann Surg. 2009;249(5):814–823. doi:10.1097/SLA.0b013e3181a38ef5
   PubMed Web of Science ®Google Scholar
• Nieto MA, Huang RY, Jackson RA, Thiery JP. EMT: 2016. Cell. 2016;166(1):21–45. doi:10.1016/j.cell.2016.06.028
   PubMed Web of Science ®Google Scholar
• Singh M, Yelle N, Venugopal C, Singh SK. EMT: mechanisms and therapeutic implications. Pharmacol Ther. 2018;182:80–94. doi:10.1016/j.pharmthera.2017.08.009
   PubMed Web of Science ®Google Scholar
• Pastushenko I, Blanpain C. EMT transition states during tumor progression and metastasis. Trends Cell Biol. 2019;29(3):212–226. doi:10.1016/j.tcb.2018.12.001
   PubMed Web of Science ®Google Scholar
• Lu W, Kang Y. Epithelial-mesenchymal plasticity in cancer progression and metastasis. Dev Cell. 2019;49(3):361–374. doi:10.1016/j.devcel.2019.04.010
   PubMed Web of Science ®Google Scholar
• Tashiro E, Henmi S, Odake H, Ino S, Imoto M. Involvement of the MEK/ERK pathway in EGF-induced E-cadherin down-regulation. Biochem Biophys Res Commun. 2016;477(4):801–806. doi:10.1016/j.bbrc.2016.06.138
   PubMed Web of Science ®Google Scholar
• Tian YC, Chen YC, Chang CT, et al. Epidermal growth factor and transforming growth factor-beta1 enhance HK-2 cell migration through a synergistic increase of matrix metalloproteinase and sustained activation of ERK signaling pathway. Exp Cell Res. 2007;313(11):2367–2377. doi:10.1016/j.yexcr.2007.03.022
   PubMed Web of Science ®Google Scholar
• Uttamsingh S, Bao X, Nguyen KT, et al. Synergistic effect between EGF and TGF-beta1 in inducing oncogenic properties of intestinal epithelial cells. Oncogene. 2008;27(18):2626–2634. doi:10.1038/sj.onc.1210915
   PubMed Web of Science ®Google Scholar
• Lu L, Zhang Q, Wu K, et al. Hepatitis C virus NS3 protein enhances cancer cell invasion by activating matrix metalloproteinase-9 and cyclooxygenase-2 through ERK/p38/NF-κB signal cascade. Cancer Lett. 2015;356(2Pt B):470–478. doi:10.1016/j.canlet.2014.09.027
   PubMed Web of Science ®Google Scholar
• Ren D, Yang Q, Dai Y, et al. Oncogenic miR-210-3p promotes prostate cancer cell EMT and bone metastasis via NF-κB signaling pathway. Mol Cancer. 2017;16(1):117. doi:10.1186/s12943-017-0688-6
   PubMed Web of Science ®Google Scholar
• Georgakopoulos-Soares I, Chartoumpekis DV, Kyriazopoulou V, Zaravinos A. EMT factors and metabolic pathways in cancer. Front Oncol. 2020;10:499. doi:10.3389/fonc.2020.00499
   PubMed Web of Science ®Google Scholar
• Serrano-Gomez SJ, Maziveyi M, Alahari SK. Regulation of epithelial-mesenchymal transition through epigenetic and post-translational modifications. Mol Cancer. 2016;15(1):18. doi:10.1186/s12943-016-0502-x
   PubMed Web of Science ®Google Scholar
• Li T, Xie J, Shen C, et al. Amplification of long noncoding RNA ZFAS1 promotes metastasis in hepatocellular carcinoma. Cancer Res. 2015;75(15):3181–3191. doi:10.1158/0008-5472.CAN-14-3721
   PubMed Web of Science ®Google Scholar
• Batlle E, Clevers H. Cancer stem cells revisited. Nat Med. 2017;23(10):1124–1134. doi:10.1038/nm.4409
   PubMed Web of Science ®Google Scholar
• Eun K, Ham SW, Kim H. Cancer stem cell heterogeneity: origin and new perspectives on CSC targeting. BMB Rep. 2017;50(3):117–125. doi:10.5483/BMBRep.2017.50.3.222
   PubMed Web of Science ®Google Scholar
• Park DJ, Sung PS, Kim JH, et al. EpCAM-high liver cancer stem cells resist natural killer cell-mediated cytotoxicity by upregulating CEACAM1. J Immunother Cancer. 2020;8(1):e000301. doi:10.1136/jitc-2019-000301
   PubMed Web of Science ®Google Scholar
• Yin T, Wang G, He S, Liu Q, Sun J, Wang Y. Human cancer cells with stem cell-like phenotype exhibit enhanced sensitivity to the cytotoxicity of IL-2 and IL-15 activated natural killer cells. Cell Immunol. 2016;300:41–45. doi:10.1016/j.cellimm.2015.11.009
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhu P, Luo J, et al. LncRNA HAND2-AS1 promotes liver cancer stem cell self-renewal via BMP signaling. EMBO J. 2019;38(17):e101110. doi:10.15252/embj.2018101110
   PubMed Web of Science ®Google Scholar
• Li X, He S, Ma B. Autophagy and autophagy-related proteins in cancer. Mol Cancer. 2020;19(1):12. doi:10.1186/s12943-020-1138-4
   PubMed Web of Science ®Google Scholar
• Amaravadi RK, Kimmelman AC, Debnath J. Targeting autophagy in cancer: recent advances and future directions. Cancer Discov. 2019;9(9):1167–1181. doi:10.1158/2159-8290.CD-19-0292
   PubMed Web of Science ®Google Scholar
• Eskelinen EL. The dual role of autophagy in cancer. Curr Opin Pharmacol. 2011;11(4):294–300. doi:10.1016/j.coph.2011.03.009
   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. doi:10.1038/s41388-017-0046-6
   PubMed Web of Science ®Google Scholar
• Rosenfeldt MT, Ryan KM. The multiple roles of autophagy in cancer. Carcinogenesis. 2011;32(7):955–963. doi:10.1093/carcin/bgr031
   PubMed Web of Science ®Google Scholar
• Rao S, Tortola L, Perlot T, et al. A dual role for autophagy in a murine model of lung cancer. Nat Commun. 2014;5:3056. doi:10.1038/ncomms4056
   PubMed Web of Science ®Google Scholar
• Yang S, Yang L, Li X, et al. New insights into autophagy in hepatocellular carcinoma: mechanisms and therapeutic strategies. Am J Cancer Res. 2019;9(7):1329–1353.
   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;61(3):617–625. doi:10.1016/j.jhep.2014.04.043
   PubMed Web of Science ®Google Scholar
• Zhao Y, Gong S, Shunmei E, Zou J. Induction of macroautophagy by heat. Mol Biol Rep. 2009;36(8):2323–2327. doi:10.1007/s11033-009-9451-4
   PubMed Web of Science ®Google Scholar
• Wu J, Liu T, Rios Z, Mei Q, Lin X, Cao S. Heat shock proteins and cancer. Trends Pharmacol Sci. 2017;38(3):226–256. doi:10.1016/j.tips.2016.11.009
   PubMed Web of Science ®Google Scholar
• Richter K, Haslbeck M, Buchner J. The heat shock response: life on the verge of death. Mol Cell. 2010;40(2):253–266. doi:10.1016/j.molcel.2010.10.006
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Burns TF. Targeting heat shock proteins in cancer: a promising therapeutic approach. Int J Mol Sci. 2017;18(9):1978. doi:10.3390/ijms18091978
   PubMed Web of Science ®Google Scholar
• Jolly C, Morimoto RI. Role of the heat shock response and molecular chaperones in oncogenesis and cell death. J Natl Cancer Inst. 2000;92(19):1564–1572. doi:10.1093/jnci/92.19.1564
   PubMedGoogle Scholar
• Fuller KJ, Issels RD, Slosman DO, Guillet JG, Soussi T, Polla BS. Cancer and the heat shock response. Eur j Cancer. 1994;30a(12):1884–1891. doi:10.1016/0959-8049(94)00362-9
   PubMed Web of Science ®Google Scholar
• Leng AM, Liu T, Yang J, et al. The apoptotic effect and associated signalling of HSP90 inhibitor 17-DMAG in hepatocellular carcinoma cells. Cell Biol Int. 2012;36(10):893–899. doi:10.1042/CBI20110473
   PubMed Web of Science ®Google Scholar
• Wang B, Chen L, Ni Z, et al. Hsp90 inhibitor 17-AAG sensitizes Bcl-2 inhibitor (-)-gossypol by suppressing ERK-mediated protective autophagy and Mcl-1 accumulation in hepatocellular carcinoma cells. Exp Cell Res. 2014;328(2):379–387. doi:10.1016/j.yexcr.2014.08.039
   PubMed Web of Science ®Google Scholar
• Guo K, Kang NX, Li Y, et al. Regulation of HSP27 on NF-kappaB pathway activation may be involved in metastatic hepatocellular carcinoma cells apoptosis. BMC Cancer. 2009;9:100. doi:10.1186/1471-2407-9-100
   PubMed Web of Science ®Google Scholar
• Binnewies M, Roberts EW, Kersten K, et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat Med. 2018;24(5):541–550. doi:10.1038/s41591-018-0014-x
   PubMed Web of Science ®Google Scholar
• Taube JM, Galon J, Sholl LM, et al. Implications of the tumor immune microenvironment for staging and therapeutics. Mod pathol. 2018;31(2):214–234. doi:10.1038/modpathol.2017.156
   PubMed Web of Science ®Google Scholar
• El-Kenawi A, Hänggi K, Ruffell B. The immune microenvironment and cancer metastasis. Cold Spring Harb Perspect Med. 2020;10(4):a037424. doi:10.1101/cshperspect.a037424
   PubMed Web of Science ®Google Scholar
• Shen S, Peng H, Wang Y, et al. Screening for immune-potentiating antigens from hepatocellular carcinoma patients after radiofrequency ablation by serum proteomic analysis. BMC Cancer. 2018;18(1):117. doi:10.1186/s12885-018-4011-8
   PubMed Web of Science ®Google Scholar
• Zerbini A, Pilli M, Penna A, et al. Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. Cancer Res. 2006;66(2):1139–1146. doi:10.1158/0008-5472.CAN-05-2244
   PubMed Web of Science ®Google Scholar
• Mizukoshi E, Yamashita T, Arai K, et al. Enhancement of tumor-associated antigen-specific T cell responses by radiofrequency ablation of hepatocellular carcinoma. Hepatology. 2013;57(4):1448–1457. doi:10.1002/hep.26153
   PubMed Web of Science ®Google Scholar
• Duffy AG, Ulahannan SV, Makorova-Rusher O, et al. Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma. J Hepatol. 2017;66(3):545–551. doi:10.1016/j.jhep.2016.10.029
   PubMed Web of Science ®Google Scholar
• Xie C, Duffy AG, Mabry-Hrones D, et al. Tremelimumab in combination with microwave ablation in patients with refractory biliary tract cancer. Hepatology. 2019;69(5):2048–2060. doi:10.1002/hep.30482
   PubMed Web of Science ®Google Scholar
• Zhang L, Wang J, Jiang J, Zhang M, Shen J. CTLA-4 blockade suppresses progression of residual tumors and improves survival after insufficient radiofrequency ablation in a subcutaneous murine hepatoma model. Cardiovasc Intervent Radiol. 2020;43(9):1353–1361. doi:10.1007/s00270-020-02505-6
   PubMed Web of Science ®Google Scholar
• Shi L, Chen L, Wu C, et al. PD-1 blockade boosts radiofrequency ablation-elicited adaptive immune responses against tumor. Clin Cancer Res. 2016;22(5):1173–1184. doi:10.1158/1078-0432.CCR-15-1352
   PubMed Web of Science ®Google Scholar
• Bastani S, Akbarzadeh M, Rastgar Rezaei Y, et al. Melatonin as a therapeutic agent for the inhibition of hypoxia-induced tumor progression: a description of possible mechanisms involved. Int J Mol Sci. 2021;22(19):10874. doi:10.3390/ijms221910874
   PubMed Web of Science ®Google Scholar
• Mazure NM, Pouysségur J. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol. 2010;22(2):177–180. doi:10.1016/j.ceb.2009.11.015
   PubMed Web of Science ®Google Scholar
• Schito L, Semenza GL. Hypoxia-inducible factors: master regulators of cancer progression. Trends Cancer. 2016;2(12):758–770. doi:10.1016/j.trecan.2016.10.016
   PubMed Web of Science ®Google Scholar
• Mimeault M, Batra SK. Hypoxia-inducing factors as master regulators of stemness properties and altered metabolism of cancer- and metastasis-initiating cells. J Cell Mol Med. 2013;17(1):30–54. doi:10.1111/jcmm.12004
   PubMed Web of Science ®Google Scholar
• Schödel J, Grampp S, Maher ER, et al. Hypoxia, hypoxia-inducible transcription factors, and renal cancer. Eur Urol. 2016;69(4):646–657. doi:10.1016/j.eururo.2015.08.007
   PubMed Web of Science ®Google Scholar
• Li M, Hao B, Zhang M, et al. Melatonin enhances radiofrequency-induced NK antitumor immunity, causing cancer metabolism reprogramming and inhibition of multiple pulmonary tumor development. Signal Transduct Targeted Ther. 2021;6(1):330. doi:10.1038/s41392-021-00745-7
   PubMed Web of Science ®Google Scholar
• Yamada S, Utsunomiya T, Morine Y, et al. Expressions of hypoxia-inducible factor-1 and epithelial cell adhesion molecule are linked with aggressive local recurrence of hepatocellular carcinoma after radiofrequency ablation therapy. Ann Surg Oncol. 2014;21(Suppl 3):S436–42. doi:10.1245/s10434-014-3575-z
   PubMed Web of Science ®Google Scholar
• Zhu H, Zhang S. Hypoxia inducible factor-1α/vascular endothelial growth factor signaling activation correlates with response to radiotherapy and its inhibition reduces hypoxia-induced angiogenesis in lung cancer. J Cell Biochem. 2018;119(9):7707–7718. doi:10.1002/jcb.27120
   PubMed Web of Science ®Google Scholar
• Ahluwalia A, Tarnawski AS. Critical role of hypoxia sensor–HIF-1α in VEGF gene activation. Implications for angiogenesis and tissue injury healing. Curr Med Chem. 2012;19(1):90–97.
   PubMed Web of Science ®Google Scholar
• Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med. 2002;8(4 Suppl):S62–S67. doi:10.1016/S1471-4914(02)02317-1
   PubMed Web of Science ®Google Scholar
• Le A, Cooper CR, Gouw AM, et al. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci USA. 2010;107(5):2037–2042. doi:10.1073/pnas.0914433107
   PubMed Web of Science ®Google Scholar
• Zhang L, Wang JN, Tang JM, et al. VEGF is essential for the growth and migration of human hepatocellular carcinoma cells. Mol Biol Rep. 2012;39(5):5085–5093. doi:10.1007/s11033-011-1304-2
   PubMed Web of Science ®Google Scholar
• Fernando NH, Hurwitz HI. Inhibition of vascular endothelial growth factor in the treatment of colorectal cancer. Semin Oncol. 2003;30(3 Suppl 6):39–50. doi:10.1016/S0093-7754(03)00124-6
   PubMed Web of Science ®Google Scholar
• Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407(6801):242–248. doi:10.1038/35025215
   PubMed Web of Science ®Google Scholar
• Sharma BK, Srinivasan R, Chawla YK, Chakraborti A. Vascular endothelial growth factor: evidence for autocrine signaling in hepatocellular carcinoma cell lines affecting invasion. Indian J Cancer. 2016;53(4):542–547. doi:10.4103/0019-509X.204765
   PubMed Web of Science ®Google Scholar
• Moon WS, Rhyu KH, Kang MJ, et al. Overexpression of VEGF and angiopoietin 2: a key to high vascularity of hepatocellular carcinoma? Mod pathol. 2003;16(6):552–557. doi:10.1097/01.MP.0000071841.17900.69
   PubMed Web of Science ®Google Scholar
• Jiang T, Zhang X, Ding J, Duan B, Lu S. Inflammation and cancer: inhibiting the progression of residual hepatic VX2 carcinoma by anti-inflammatory drug after incomplete radiofrequency ablation. Int J Clin Exp Pathol. 2015;8(11):13945–13956.
   PubMed Web of Science ®Google Scholar
• Liu Z, Dai H, Jia G, Li Y, Liu X, Ren W. Insufficient radiofrequency ablation promotes human hepatoma SMMC7721 cell proliferation by stimulating vascular endothelial growth factor overexpression. Oncol Lett. 2015;9(4):1893–1896. doi:10.3892/ol.2015.2966
   PubMed Web of Science ®Google Scholar
• Zhang Q, Kong J, Dong S, Xu W, Sun W. Metformin exhibits the anti-proliferation and anti-invasion effects in hepatocellular carcinoma cells after insufficient radiofrequency ablation. Cancer Cell Int. 2017;17(1):48. doi:10.1186/s12935-017-0418-6
   PubMed Web of Science ®Google Scholar
• Shiota G, Okano J, Kawasaki H, Kawamoto T, Nakamura T. Serum hepatocyte growth factor levels in liver diseases: clinical implications. Hepatology. 1995;21(1):106–112. doi:10.1002/hep.1840210119
   PubMed Web of Science ®Google Scholar
• Yu J, Chen GG, Lai PBS. Targeting hepatocyte growth factor/c-mesenchymal-epithelial transition factor axis in hepatocellular carcinoma: rationale and therapeutic strategies. Med Res Rev. 2021;41(1):507–524. doi:10.1002/med.21738
   PubMed Web of Science ®Google Scholar
• Nakayama N, Kashiwazaki H, Kobayashi N, et al. Hepatocyte growth factor and c-met expression in Long-Evans Cinnamon rats with spontaneous hepatitis and hepatoma. Hepatology. 1996;24(3):596–602. doi:10.1002/hep.510240323
   PubMed Web of Science ®Google Scholar
• Giordano S, Columbano A. Met as a therapeutic target in HCC: facts and hopes. J Hepatol. 2014;60(2):442–452. doi:10.1016/j.jhep.2013.09.009
   PubMed Web of Science ®Google Scholar
• Jia G, Li F, Tong R, et al. c-Met/MAPK pathway promotes the malignant progression of residual hepatocellular carcinoma cells after insufficient radiofrequency ablation. Med Oncol. 2020;37(12):117. doi:10.1007/s12032-020-01444-z
   PubMed Web of Science ®Google Scholar
• Fabregat I, Moreno-Càceres J, Sánchez A, et al. TGF-β signalling and liver disease. FEBS J. 2016;283(12):2219–2232. doi:10.1111/febs.13665
   PubMed Web of Science ®Google Scholar
• Russell WE, Coffey RJ Jr., Ouellette AJ, Moses HL. Type beta transforming growth factor reversibly inhibits the early proliferative response to partial hepatectomy in the rat. Proc Natl Acad Sci U S A. 1988;85(14):5126–5130. doi:10.1073/pnas.85.14.5126
   PubMed Web of Science ®Google Scholar
• Gonzalez-Sanchez E, Vaquero J, Férnandez-Barrena MG, et al. The TGF-β pathway: a pharmacological target in hepatocellular carcinoma? Cancers. 2021;13(13):3248. doi:10.3390/cancers13133248
   PubMed Web of Science ®Google Scholar
• Iwahashi S, Shimada M, Utsunomiya T, et al. Epithelial-mesenchymal transition-related genes are linked to aggressive local recurrence of hepatocellular carcinoma after radiofrequency ablation. Cancer Lett. 2016;375(1):47–50. doi:10.1016/j.canlet.2016.02.041
   PubMed Web of Science ®Google Scholar
• Llovet JM, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359(4):378–390. doi:10.1056/NEJMoa0708857
   PubMed Web of Science ®Google Scholar
• Cheng AL, Kang YK, Chen Z, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a Phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2009;10(1):25–34. doi:10.1016/S1470-2045(08)70285-7
   PubMed Web of Science ®Google Scholar
• Nagai T, Arao T, Furuta K, et al. Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Mol Cancer Ther. 2011;10(1):169–177. doi:10.1158/1535-7163.MCT-10-0544
   PubMed Web of Science ®Google Scholar
• Silva VR, Neves SP, Santos LS, Dias RB, Bezerra DP. Challenges and therapeutic opportunities of autophagy in cancer therapy. Cancers. 2020;12(11):3461. doi:10.3390/cancers12113461
   PubMed Web of Science ®Google Scholar
• Ferreira PMP, Sousa RWR, Ferreira JRO, Bezerra DP. Chloroquine and hydroxychloroquine in antitumor therapies based on autophagy-related mechanisms. Pharmacol Res. 2021;168:105582. doi:10.1016/j.phrs.2021.105582
   PubMed Web of Science ®Google Scholar
• Wu Y, Zhou BP. Inflammation: a driving force speeds cancer metastasis. Cell Cycle. 2009;8(20):3267–3273. doi:10.4161/cc.8.20.9699
   PubMed Web of Science ®Google Scholar
• Rajput S, Wilber A. Roles of inflammation in cancer initiation, progression, and metastasis. Front Biosci. 2010;2:176–183. doi:10.2741/s55
   Google Scholar
• Dromi SA, Walsh MP, Herby S, et al. Radiofrequency ablation induces antigen-presenting cell infiltration and amplification of weak tumor-induced immunity. Radiology. 2009;251(1):58–66. doi:10.1148/radiol.2511072175
   PubMed Web of Science ®Google Scholar
• Zhang R, Ma M, Dong G, et al. Increased matrix stiffness promotes tumor progression of residual hepatocellular carcinoma after insufficient heat treatment. Cancer Sci. 2017;108(9):1778–1786. doi:10.1111/cas.13322
   PubMed Web of Science ®Google Scholar
• Yoon JH, Lee JM, Klotz E, et al. Prediction of local tumor progression after Radiofrequency Ablation (RFA) of hepatocellular carcinoma by assessment of ablative margin using Pre-RFA MRI and Post-RFA CT registration. Korean j Radiol. 2018;19(6):1053–1065. doi:10.3348/kjr.2018.19.6.1053
   PubMed Web of Science ®Google Scholar
• Kim YS, Lee WJ, Rhim H, Lim HK, Choi D, Lee JY. The minimal ablative margin of radiofrequency ablation of hepatocellular carcinoma (> 2 and < 5 cm) needed to prevent local tumor progression: 3D quantitative assessment using CT image fusion. AJR Am J Roentgenol. 2010;195(3):758–765. doi:10.2214/AJR.09.2954
   PubMed Web of Science ®Google Scholar
• Wang X, Sofocleous CT, Erinjeri JP, et al. Margin size is an independent predictor of local tumor progression after ablation of colon cancer liver metastases. Cardiovasc Intervent Radiol. 2013;36(1):166–175. doi:10.1007/s00270-012-0377-1
   PubMed Web of Science ®Google Scholar
• Okusaka T, Okada S, Ueno H, et al. Satellite lesions in patients with small hepatocellular carcinoma with reference to clinicopathologic features. Cancer. 2002;95(9):1931–1937. doi:10.1002/cncr.10892
   PubMed Web of Science ®Google Scholar
• Kim YS, Lim HK, Rhim H, Lee MW. Ablation of hepatocellular carcinoma. Best Pract Res Clin Gastroenterol. 2014;28(5):897–908. doi:10.1016/j.bpg.2014.08.011
   PubMed Web of Science ®Google Scholar
• Kan X, Zhang F, Zhou G, et al. Interventional real-time optical imaging guidance for complete tumor ablation. Proc Natl Acad Sci U S A. 2021;118(41). doi:10.1073/pnas.2113028118
   Web of Science ®Google Scholar
• Lee DH, Lee JM. Recent advances in the image-guided tumor ablation of liver malignancies: radiofrequency ablation with multiple electrodes, real-time multimodality fusion imaging, and new energy sources. Korean j Radiol. 2018;19(4):545–559. doi:10.3348/kjr.2018.19.4.545
   PubMed Web of Science ®Google Scholar
• Baglieri J, Brenner DA, Kisseleva T. The role of fibrosis and liver-associated fibroblasts in the pathogenesis of hepatocellular carcinoma. Int J Mol Sci. 2019;20(7):1723. doi:10.3390/ijms20071723
   PubMed Web of Science ®Google Scholar
• Khan HA, Ahmad MZ, Khan JA, Arshad MI. Crosstalk of liver immune cells and cell death mechanisms in different murine models of liver injury and its clinical relevance. HBPD Int. 2017;16(3):245–256. doi:10.1016/S1499-3872(17)60014-6
   Web of Science ®Google Scholar