1,476
Views
0
CrossRef citations to date
0
Altmetric
Original Research

CD8 T cell-mediated depletion of HBV surface-antigen-expressing, bilineal-differentiated liver carcinoma cells generates highly aggressive escape variants

, , , , , , , , & ORCID Icon show all
Article: 2215096 | Received 07 Nov 2022, Accepted 14 May 2023, Published online: 26 May 2023

References

  • Stavraka C, Rush H, Ross P. Combined hepatocellular cholangiocarcinoma (CHCC-CC): an update of genetics, molecular biology, and therapeutic interventions. J Hepatocell Carcinoma. 2018;6:11–10. doi:10.2147/JHC.S159805.
  • Llovet JM, Kelley RK, Villanueva A, Singal AG, Pikarsky E, Roayaie S, Lencioni R, Koike K, Zucman-Rossi FR. Hepatocellular carcinoma. Nat Rev Dis Primers. 2021;7(1):6. doi:10.1038/s41572-020-00240-3.
  • Lee HW, Chan H-Y. Unresolved issues of immune tolerance in chronic hepatitis B. J Gastroenterol. 2020;55(4):383–389. doi:10.1007/s00535-020-01665-z.
  • Flores JE, Thompson AJ, Ryan M, Howell J. The global impact of hepatitis b vaccination on hepatocellular carcinoma. Vaccines (Basel). 2022;10(5):793. doi:10.3390/vaccines10050793.
  • Wu CC, Chen YS, Cao L, Chen XW, Lu MJ. Hepatitis B virus infection: defective surface antigen expression and pathogenesis. World J Gastroentero. 2018;24(31):3488–3499. doi:10.3748/wjg.v24.i31.3488.
  • Li YW, Yang FC, Lu HQ, Zhang JS. Hepatocellular carcinoma and hepatitis B surface protein. World J Gastroentero. 2016;22(6):1943–1952. doi:10.3748/wjg.v22.i6.1943.
  • Zhu D, Liu L, Yang D, Fu S, Bian Y, Sun Z, He J, Su L, Zhang L, Peng H, et al. Clearing persistent extracellular antigen of hepatitis B virus: an immunomodulatory strategy to reverse tolerance for an effective therapeutic vaccination. J Immunol. 2016;196(7):3079–3087. doi:10.4049/jimmunol.1502061.
  • Wu S, Ye S, Lin X, Chen Y, Zhang Y, Jing Z, Liu W, Chen W, Lin X, Lin X. Small hepatitis B virus surface antigen promotes malignant progression of hepatocellular carcinoma via endoplasmic reticulum stress-induced FGF19/JAK2/STAT3 signaling. Cancer Lett. 2021;499:175–187. doi:10.1016/j.canlet.2020.11.032.
  • Chen H, Mu M, Liu Q, Hu H, Tian C, Zhang G, Li Y, Yang F, Lin S. Hepatocyte endoplasmic reticulum stress inhibits hepatitis B virus secretion and delays intracellular hepatitis B virus clearance after entecavir treatment. Front Med. 2021;7:589040. doi:10.3389/fmed.2020.589040.
  • Kim SY, Kyaw YY, Cheong J. Functional interaction of endoplasmic reticulum stress and hepatitis B virus in the pathogenesis of liver diseases. World J Gastroentero. 2017;23(43):7657–7665. doi:10.3748/wjg.v23.i43.7657.
  • Chisari FV, Filippi P, Buras J, McLachlan A, Popper H, Pinkert CA, Palmiter RD, Brinster RL. Structural and pathological effects of synthesis of hepatitis B virus large envelope polypeptide in transgenic mice. Proc Natl Acad Sci U S A. 1987;84(19):6909–6913. doi:10.1073/pnas.84.19.6909.
  • Deng F, Xu G, Cheng Z, Huang Y, Ma C, Luo C, Yu C, Wang J, Xu X, Liu S, et al. Hepatitis B surface antigen suppresses the activation of nuclear factor kappa B pathway via interaction with the TAK1-TAB2 complex. Front Immunol. 2021;12:618196. doi:10.3389/fimmu.2021.618196.
  • Chisari FV, Klopchin K, Moriyama T, Pasquinelli C, Dunsford HA, Sell S, Brinster RL, Palmiter RL, Palmiter RD. Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell. 1989;59(6):1145–1156. doi:10.1016/0092-8674(89)90770-8.
  • Choi YM, Lee SY, Kim BJ. Naturally occurring hepatitis B virus mutations leading to endoplasmic reticulum stress and their contribution to the progression of hepatocellular carcinoma. Int J Mol Sci. 2019;20(3):597. doi:10.3390/ijms20030597.
  • Li Y, Xia Y, Cheng X, Kleiner DE, Hewitt SM, Sproch J, Li T, Zhuang H, Liang TJ. Hepatitis B surface antigen activates unfolded protein response in forming ground glass hepatocytes of chronic hepatitis B. Viruses. 2019;11(4):386. doi:10.3390/v11040386.
  • Amaddeo G, Cao Q, Ladeiro Y, Imbeaud S, Nault JC, Jaoui D, Mathe YG, Laurent C, Laurent A, Bioulac-Sage P, et al. Integration of tumour and viral genomic characterizations in HBV-related hepatocellular carcinomas. Gut. 2015;64(5):820–829. doi:10.1136/gutjnl-2013-306228.
  • Katz SF, Lechel A, Obenauf AC, Begus-Nahrmann Y, Kraus JM, Hoffmann EM, Duda J, Eshraghi P, Hartmann D, Liss B, et al. Disruption of Trp53 in livers of mice induces formation of carcinomas with bilineal differentiation. Gastroenterology. 2012;142(5):1229–39.e3. doi:10.1053/j.gastro.2012.02.009.
  • Liu Y, Xin B, Yamamoto M, Goto M, Ooshio T, Kamikokura Y, Tanaka Hm Meng L, Mizukami Y, Okada Y, Mizukami Y, et al. Generation of combined hepatocellular-cholangiocarcinoma through transdifferentiation and dedifferentiation in p53-knockout mice. Cancer Sci. 2021;112(8):3111–3124. doi:10.1111/cas.14996.
  • Stifter K, Krieger J, Ruths L, Gout J, Mulaw M, Lechel A, Kleger A, Seufferlein T, Wagner M, Schirmbeck R. IFN-γ treatment protocol for MHC-I(lo)/PD-L1(+) pancreatic tumor cells selectively restores their TAP-mediated presentation competence and CD8 T-cell priming potential. J Immunother Cancer. 2020;8(2):e000692. doi:10.1136/jitc-2020-000692.
  • Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy S, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545–15550. doi:10.1073/pnas.0506580102.
  • Otasek D, Morris JH, Bouças J, Pico AR, Demchak B. Cytoscape Automation: empowering workflow-based network analysis. Genome Biol. 2019;20(1):185. doi:10.1186/s13059-019-1758-4.
  • Garrido F, Aptsiauri N, Doorduijn EM, Garcia Lora AM, van Hall T. The urgent need to recover MHC class I in cancers for effective immunotherapy. Curr Opin Immunol. 2016;39:44–51. doi:10.1016/j.coi.2015.12.007.
  • Harms JS, Splitter GA. Interferon-gamma inhibits transgene expression driven by SV40 or CMV promoters but augments expression driven by the mammalian MHC I promoter. Hum Gene Ther. 1995;6(10):1291–1297. doi:10.1089/hum.1995.6.10-1291.
  • Dhar GA, Saha S, Mitra P, Nag Chaudhuri R. DNA methylation and regulation of gene expression: guardian of our health. Nucleus. 2021;64(3):259–270. doi:10.1007/s13237-021-00367-y.
  • Qasim W, Brunetto M, Gehring AJ, Xue S-A, Schurich A, Khakpoor A, Zhan H, Ciccorossi P, Gilmour K, Cavallone D, et al. Immunotherapy of HCC metastases with autologous T cell receptor redirected T cells, targeting HBsAg in a liver transplant patient. J Hepatol. 2015;62(2):486–491. doi:10.1016/j.jhep.2014.10.001.
  • Tan AT, Bertoletti A. HBV-HCC treatment with mRNA electroporated HBV-TCR T cells. null. 2021;2(1):ltab026. doi:10.1093/immadv/ltab026.
  • Kim CY, Tilles JG. Purification and biophysical characterization of hepatitis B Antigen. J Clin Invest. 1973;52(5):1176–1186. doi:10.1172/JCI107284.
  • Jiang M, Broering R, Trippler M, Poggenpohl L, Fiedler M, Gerken G, Lu M, Schlaak JF. Toll-like receptor-mediated immune responses are attenuated in the presence of high levels of hepatitis B virus surface antigen. J Viral Hepat. 2014;21(12):860–872. doi:10.1111/jvh.12216.
  • Riedl P, Reiser M, Stifter K, Krieger J, Schirmbeck R. Differential presentation of endogenous and exogenous hepatitis B surface antigens influences priming of CD8(+) T cells in an epitope-specific manner. Eur J Immunol. 2014;44(7):1981–1991. doi:10.1002/eji.201343933.
  • Tout I, Loureiro D, Mansouri A, Soumelis V, Boyer N, Asselah T. Hepatitis B surface antigen seroclearance: immune mechanisms, clinical impact, importance for drug development. J Hepatol. 2020;73(2):409–422. doi:10.1016/j.jhep.2020.04.013.
  • Fumagalli V, Di Lucia P, Venzin V, Bono EB, Jordan R, Frey CR, Chisari FV, Guidotti LG, Iannacone M, Iannacone M. Serum HBsAg clearance has minimal impact on CD8+ T cell responses in mouse models of HBV infection. J Exp Med. 2020;217(11):e20200298. doi:10.1084/jem.20200298.
  • Lee W-S, Lee K-W, Heo J-S, Kim S-J, Coi S-H, Kim Y-I, Joh J-W. Comparison of combined hepatocellular and cholangiocarcinoma with hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Surg Today. 2006;36(10):892–897. doi:10.1007/s00595-006-3276-8.
  • Taguchi J, Nakashima O, Tanaka M, Hisaka T, Takazawa T, Kojiro M. A clinicopathological study on combined hepatocellular and cholangiocarcinoma. J Gastroen Hepatol. 1996;11(8):758–764. doi:10.1111/j.1440-1746.1996.tb00327.x.
  • Liu S, Zhang H, Gu C, Yin J, He Y, Xie J, Cao G. Associations between hepatitis B virus mutations and the risk of hepatocellular carcinoma: a meta-analysis. J Natl Cancer Inst. 2009;101(15):1066–1082. doi:10.1093/jnci/djp180.
  • Chu CM, Liaw YF. HBsAg seroclearance in asymptomatic carriers of high endemic areas: appreciably high rates during a long-term follow-up. Hepatology. 2007;45(5):1187–1192. doi:10.1002/hep.21612.
  • Simonetti J, Bulkow L, McMahon BJ, Homan C, Snowball M, Negus S, Williams J, Livingston SE. Clearance of hepatitis B surface antigen and risk of hepatocellular carcinoma in a cohort chronically infected with hepatitis B virus. Hepatology. 2010;51(5):1531–1537. doi:10.1002/hep.21612.
  • Moini M, Fung S. HBsAg loss as a treatment endpoint for chronic HBV infection: hBV cure. Viruses. 2022;14(4):657. doi:10.3390/v14040657.