Innate immune cells and their interaction with T cells in hepatocellular carcinoma (Review)
- Authors:
- Guo-Qing Hong
- Dong Cai
- Jian-Ping Gong
- Xing Lai
-
Affiliations: Department of Hepatobiliary and Thyroid Breast Surgery, Tongnan District People's Hospital, Chongqing 402660, P.R. China, Department of Hepatobiliary Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P.R. China - Published online on: November 19, 2020 https://doi.org/10.3892/ol.2020.12319
- Article Number: 57
-
Copyright: © Hong et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI | |
Villanueva A: Hepatocellular carcinoma. N Engl J Med. 380:1450–1462. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kulik L and El-Serag H: Epidemiology and management of hepatocellular carcinoma. Gastroenterology. 156:477–491.e1. 2019. View Article : Google Scholar : PubMed/NCBI | |
Yang JD, Hainaut P, Gores GJ, Amadou A, Plymoth A and Roberts LR: A global view of hepatocellular carcinoma: Trends, risk, prevention and management. Nat Rev Gastroenterol Hepatol. 16:589–604. 2019. View Article : Google Scholar : PubMed/NCBI | |
Macek Jilkova Z, Aspord C and Decaens T: Predictive factors for response to PD-1/PD-L1 checkpoint inhibition in the field of hepatocellular carcinoma: Current status and challenges. Cancers (Basel). 11:15542019. View Article : Google Scholar | |
El-Khoueiry AB, Sangro B, Yau T, Crocenzi TS, Kudo M, Hsu C, Kim TY, Choo SP, Trojan J, Welling TH, et al: Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): An open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet. 389:2492–2502. 2017. View Article : Google Scholar : PubMed/NCBI | |
Syn NL, Teng MWL, Mok TSK and Soo RA: De-novo and acquired resistance to immune checkpoint targeting. Lancet Oncol. 18:e731–e741. 2017. View Article : Google Scholar : PubMed/NCBI | |
Jenne CN and Kubes P: Immune surveillance by the liver. Nat Immunol. 14:996–1006. 2013. View Article : Google Scholar : PubMed/NCBI | |
Ringelhan M, Pfister D, O'Connor T, Pikarsky E and Heikenwalder M: The immunology of hepatocellular carcinoma. Nat Immunol. 19:222–232. 2018. View Article : Google Scholar : PubMed/NCBI | |
Greten T, Wang X and Korangy F: Current concepts of immune based treatments for patients with HCC: From basic science to novel treatment approaches. Gut. 64:842–848. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wherry EJ and Kurachi M: Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol. 15:486–499. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, et al: Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature. 479:547–551. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cheng JT, Deng YN, Yi HM, Wang GY, Fu BS, Chen WJ, Liu W, Tai Y, Peng YW and Zhang Q: Hepatic carcinoma-associated fibroblasts induce IDO-producing regulatory dendritic cells through IL-6-mediated STAT3 activation. Oncogenesis. 5:e1982016. View Article : Google Scholar : PubMed/NCBI | |
Steinman R and Cohn Z: Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 137:1142–1162. 1973. View Article : Google Scholar : PubMed/NCBI | |
Benites BD, Alvarez MC and Saad STO: Small particles, Big effects: The interplay between exosomes and dendritic cells in antitumor immunity and immunotherapy. Cells. 8:16482019. View Article : Google Scholar | |
Osada T, Clay T, Hobeika A, Lyerly HK and Morse MA: NK cell activation by dendritic cell vaccine: A mechanism of action for clinical activity. Cancer Immunol Immunother. 55:1122–1131. 2006. View Article : Google Scholar : PubMed/NCBI | |
Shang N, Figini M, Shangguan J, Wang B, Sun C, Pan L, Ma Q and Zhang Z: Dendritic cells based immunotherapy. Am J Cancer Res. 7:2091–2102. 2017.PubMed/NCBI | |
Chen S: Absence of CD83-positive mature and activated dendritic cells at cancer nodules from patients with hepatocellular carcinoma: Relevance to hepatocarcinogenesis. Cancer Lett. 148:49–57. 2000. View Article : Google Scholar : PubMed/NCBI | |
Cai XY, Gao Q, Qiu SJ, Ye SL, Wu ZQ, Fan J and Tang ZY: Dendritic cell infiltration and prognosis of human hepatocellular carcinoma. J Cancer Res Clin Oncol. 132:293–301. 2006. View Article : Google Scholar : PubMed/NCBI | |
Shibolet O, Alper R, Zlotogarov L, Thalenfeld B, Engelhardt D, Rabbani E and Ilan Y: NKT and CD8 lymphocytes mediate suppression of hepatocellular carcinoma growth via tumor antigen-pulsed dendritic cells. Int J Cancer. 106:236–243. 2003. View Article : Google Scholar : PubMed/NCBI | |
Chen YX, Man K, Ling GS, Chen Y, Sun BS, Cheng Q, Wong OH, Lo CK, Ng IO, Chan LC, et al: A crucial role for dendritic cell (DC) IL-10 in inhibiting successful DC-based immunotherapy: Superior antitumor immunity against hepatocellular carcinoma evoked by DC devoid of IL-10. J Immunol. 179:6009–6015. 2007. View Article : Google Scholar : PubMed/NCBI | |
Tatsumi T, Takehara T, Kanto T, Miyagi T, Kuzushita N, Sugimoto Y, Jinushi M, Kasahara A, Sasaki Y, Hori M and Hayashi N: Administration of interleukin-12 enhances the therapeutic efficacy of dendritic cell-based tumor vaccines in mouse hepatocellular carcinoma. Cancer Res. 61:7563–7567. 2001.PubMed/NCBI | |
Rai V, Abdo J, Alsuwaidan AN, Agrawal S, Sharma P and Agrawal DK: Cellular and molecular targets for the immunotherapy of hepatocellular carcinoma. Mol Cell Biochem. 437:13–36. 2018. View Article : Google Scholar : PubMed/NCBI | |
Santos PM, Menk AV, Shi J, Tsung A, Delgoffe GM and Butterfield LH: Tumor-derived alpha-fetoprotein suppresses fatty acid metabolism and oxidative phosphorylation in dendritic cells. Cancer Immunol Res. 7:1001–1012. 2019. View Article : Google Scholar : PubMed/NCBI | |
Han Y, Chen Z, Yang Y, Jiang Z, Gu Y, Liu Y, Lin C, Pan Z, Yu Y, Jiang M, et al: Human CD14+ CTLA-4+ regulatory dendritic cells suppress T-cell response by cytotoxic T-lymphocyte antigen-4-dependent IL-10 and indoleamine-2,3-dioxygenase production in hepatocellular carcinoma. Hepatology. 59:567–579. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zeng Z, Yao WJ, Xu X, Xu GQ, Long JH, Wang X, Wen ZY and Chien S: Hepatocellular carcinoma cells deteriorate the biophysical properties of dendritic cells. Cell Biochem Biophys. 55:33–43. 2009. View Article : Google Scholar : PubMed/NCBI | |
Qian BZ and Pollard JW: Macrophage diversity enhances tumor progression and metastasis. Cell. 141:39–51. 2010. View Article : Google Scholar : PubMed/NCBI | |
Vitale I, Manic G, Coussens L, Kroemer G and Galluzzi L: Macrophages and metabolism in the tumor microenvironment. Cell Metab. 30:36–50. 2019. View Article : Google Scholar : PubMed/NCBI | |
Mantovani A and Sica A: Macrophages, innate immunity and cancer: Balance, tolerance, and diversity. Curr Opin Immunol. 22:231–237. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yeung OW, Lo CM, Ling CC, Qi X, Geng W, Li CX, Ng KT, Forbes SJ, Guan XY, Poon RT, et al: Alternatively activated (M2) macrophages promote tumour growth and invasiveness in hepatocellular carcinoma. J Hepatol. 62:607–616. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kang FB, Wang L, Li D, Zhang YG and Sun DX: Hepatocellular carcinomas promote tumor-associated macrophage M2-polarization via increased B7-H3 expression. Oncol Rep. 33:274–282. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Ye YC, Chen Y, Zhao JL, Gao CC, Han H, Liu WC and Qin HY: Crosstalk between hepatic tumor cells and macrophages via Wnt/β-catenin signaling promotes M2-like macrophage polarization and reinforces tumor malignant behaviors. Cell Death Dis. 9:7932018. View Article : Google Scholar : PubMed/NCBI | |
Yin Z, Ma T, Lin Y, Lu X, Zhang C, Chen S and Jian Z: IL-6/STAT3 pathway intermediates M1/M2 macrophage polarization during the development of hepatocellular carcinoma. J Cell Biochem. 119:9419–9432. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ye Y, Xu Y, Lai Y, He W, Li Y, Wang R, Luo X, Chen R and Chen T: Long non-coding RNA cox-2 prevents immune evasion and metastasis of hepatocellular carcinoma by altering M1/M2 macrophage polarization. J Cell Biochem. 119:2951–2963. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zong Z, Zou J, Mao R, Ma C, Li N, Wang J, Wang X, Zhou H, Zhang L and Shi Y: M1 macrophages induce PD-L1 expression in hepatocellular carcinoma cells through IL-1β signaling. Front Immunol. 10:16432019. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Zhang Q, Lou Y, Fu Q, Chen Q, Wei T, Yang J, Tang J, Wang J, Chen Y, et al: Hypoxia-inducible factor-1alpha/interleukin-1beta signaling enhances hepatoma epithelial-mesenchymal transition through macrophages in a hypoxic-inflammatory microenvironment. Hepatology. 67:1872–1889. 2018. View Article : Google Scholar : PubMed/NCBI | |
Fu XT, Dai Z, Song K, Zhang ZJ, Zhou ZJ, Zhou SL, Zhao YM, Xiao YS, Sun QM, Ding ZB and Fan J: Macrophage-secreted IL-8 induces epithelial-mesenchymal transition in hepatocellular carcinoma cells by activating the JAK2/STAT3/Snail pathway. Int J Oncol. 46:587–596. 2015. View Article : Google Scholar : PubMed/NCBI | |
Capece D, Fischietti M, Verzella D, Gaggiano A, Cicciarelli G, Tessitore A, Zazzeroni F and Alesse E: The inflammatory microenvironment in hepatocellular carcinoma: A pivotal role for tumor-associated macrophages. Biomed Res Int. 2013:1872042013. View Article : Google Scholar : PubMed/NCBI | |
Fu XT, Song K, Zhou J, Shi YH, Liu WR, Shi GM, Gao Q, Wang XY, Ding ZB and Fan J: Tumor-associated macrophages modulate resistance to oxaliplatin via inducing autophagy in hepatocellular carcinoma. Cancer Cell Int. 19:712019. View Article : Google Scholar : PubMed/NCBI | |
Tacke F: Targeting hepatic macrophages to treat liver diseases. J Hepatol. 66:1300–1312. 2017. View Article : Google Scholar : PubMed/NCBI | |
Dou L, Shi X, He X and Gao Y: Macrophage phenotype and function in liver disorder. Front Immunol. 10:31122019. View Article : Google Scholar : PubMed/NCBI | |
Naugler W, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy A and Karin M: Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science. 317:121–124. 2007. View Article : Google Scholar : PubMed/NCBI | |
Martínez-Cardona C, Lozano-Ruiz B, Bachiller V, Peiró G, Algaba-Chueca F, Gómez-Hurtado I, Such J, Zapater P, Francés R and González-Navajas J: AIM2 deficiency reduces the development of hepatocellular carcinoma in mice. Int J Cancer. 143:2997–3007. 2018. View Article : Google Scholar : PubMed/NCBI | |
Miura K, Ohnishi H, Morimoto N, Minami S, Ishioka M, Watanabe S, Tsukui M, Takaoka Y, Nomoto H, Isoda N and Yamamoto H: Ezetimibe suppresses development of liver tumors by inhibiting angiogenesis in mice fed a high-fat diet. Cancer Sci. 110:771–783. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wu H, Zhong Z, Wang A, Yuan C, Ning K, Hu H, Wang C and Yin X: LncRNA FTX represses the progression of non-alcoholic fatty liver disease to hepatocellular carcinoma via regulating the M1/M2 polarization of Kupffer cells. Cancer Cell Int. 20:2662020. View Article : Google Scholar : PubMed/NCBI | |
Kuang DM, Zhao Q, Wu Y, Peng C, Wang J, Xu Z, Yin XY and Zheng L: Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J Hepatol. 54:948–955. 2011. View Article : Google Scholar : PubMed/NCBI | |
Gomez D, Farid S, Malik HZ, Young AL, Toogood GJ, Lodge JPA and Prasad KR: Preoperative neutrophil-to-lymphocyte ratio as a prognostic predictor after curative resection for hepatocellular carcinoma. World J Surg. 32:1757–1762. 2008. View Article : Google Scholar : PubMed/NCBI | |
Li YW, Qiu SJ, Fan J, Zhou J, Gao Q, Xiao YS and Xu YF: Intratumoral neutrophils: A poor prognostic factor for hepatocellular carcinoma following resection. J Hepatol. 54:497–505. 2011. View Article : Google Scholar : PubMed/NCBI | |
Li L, Xu L, Yan J, Zhen ZJ, Ji Y, Liu CQ, Lau WY, Zheng L and Xu J: CXCR2-CXCL1 axis is correlated with neutrophil infiltration and predicts a poor prognosis in hepatocellular carcinoma. J Exp Clin Cancer Res. 34:1292015. View Article : Google Scholar : PubMed/NCBI | |
Zhou SL, Dai Z, Zhou ZJ, Wang XY, Yang GH, Wang Z, Huang XW, Fan J and Zhou J: Overexpression of CXCL5 mediates neutrophil infiltration and indicates poor prognosis for hepatocellular carcinoma. Hepatology. 56:2242–2254. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lu C, Rong D, Zhang B, Zheng W, Wang X, Chen Z and Tang W: Current perspectives on the immunosuppressive tumor microenvironment in hepatocellular carcinoma: Challenges and opportunities. Mol Cancer. 18:1302019. View Article : Google Scholar : PubMed/NCBI | |
He M, Peng A, Huang XZ, Shi DC, Wang JC, Zhao Q, Lin H, Kuang DM, Ke PF and Lao XM: Peritumoral stromal neutrophils are essential for c-Met-elicited metastasis in human hepatocellular carcinoma. Oncoimmunology. 5:e12198282016. View Article : Google Scholar : PubMed/NCBI | |
Wilson CL, Jurk D, Fullard N, Banks P, Page A, Luli S, Elsharkawy AM, Gieling RG, Chakraborty JB, Fox C, et al: NFκB1 is a suppressor of neutrophil-driven hepatocellular carcinoma. Nat Commun. 6:68182015. View Article : Google Scholar : PubMed/NCBI | |
Jorch SK and Kubes P: An emerging role for neutrophil extracellular traps in noninfectious disease. Nat Med. 23:279–287. 2017. View Article : Google Scholar : PubMed/NCBI | |
van der Windt DJ, Sud V, Zhang H, Varley PR, Goswami J, Yazdani HO, Tohme S, Loughran P, O'Doherty RM, Minervini MI, et al: Neutrophil extracellular traps promote inflammation and development of hepatocellular carcinoma in nonalcoholic steatohepatitis. Hepatology. 68:1347–1360. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yang LY, Luo Q, Lu L, Zhu WW, Sun HT, Wei R, Lin ZF, Wang XY, Wang CQ, Lu M, et al: Increased neutrophil extracellular traps promote metastasis potential of hepatocellular carcinoma via provoking tumorous inflammatory response. J Hematol Oncol. 13:32020. View Article : Google Scholar : PubMed/NCBI | |
Fulkerson P: Transcription factors in eosinophil development and as therapeutic targets. Front Med (Lausanne). 4:1152017. View Article : Google Scholar : PubMed/NCBI | |
Bernsmeier C, van der Merwe S and Périanin A: Innate immune cells in cirrhosis. J Hepatol. 73:186–201. 2020. View Article : Google Scholar : PubMed/NCBI | |
Grisaru-Tal S, Itan M, Klion A and Munitz A: A new dawn for eosinophils in the tumour microenvironment. Nat Rev Cancer. 10:594–607. 2020. View Article : Google Scholar | |
Kataoka S, Konishi Y, Nishio Y, Fujikawa-Adachi K and Tominaga A: Antitumor activity of eosinophils activated by IL-5 and eotaxin against hepatocellular carcinoma. DNA Cell Biol. 23:549–560. 2004. View Article : Google Scholar : PubMed/NCBI | |
Steel JL, Kim KH, Dew MA, Unruh ML, Antoni MH, Olek MC, Geller DA, Carr BI, Butterfield LH and Gamblin TC: Cancer-related symptom clusters, eosinophils, and survival in hepatobiliary cancer: An exploratory study. J Pain Symptom Manage. 39:859–871. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gabrilovich D, Ostrand-Rosenberg S and Bronte V: Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 12:253–268. 2012. View Article : Google Scholar : PubMed/NCBI | |
Arihara F, Mizukoshi E, Kitahara M, Takata Y, Arai K, Yamashita T, Nakamoto Y and Kaneko S: Increase in CD14+HLA-DR-/low myeloid-derived suppressor cells in hepatocellular carcinoma patients and its impact on prognosis. Cancer Immunol Immunother. 62:1421–1430. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, Lehner F, Manns M, Greten T and Korangy F: Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 50:799–807. 2009. View Article : Google Scholar : PubMed/NCBI | |
Hu C, Gan J, Zhang R, Cheng Y and Huang G: Up-regulated myeloid-derived suppressor cell contributes to hepatocellular carcinoma development by impairing dendritic cell function. Scand J Gastroenterol. 46:156–164. 2011. View Article : Google Scholar : PubMed/NCBI | |
Lu L, Chang C and Hsu C: Targeting myeloid-derived suppressor cells in the treatment of hepatocellular carcinoma: Current state and future perspectives. J Hepatocell Carcinoma. 6:71–84. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chiu DK, Tse AP, Xu IM, Di Cui J, Lai RK, Li LL, Koh HY, Tsang FH, Wei LL, Wong CM, et al: Hypoxia inducible factor HIF-1 promotes myeloid-derived suppressor cells accumulation through ENTPD2/CD39L1 in hepatocellular carcinoma. Nat Commun. 8:5172017. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Liu Z, Wang J, Yu J, Li Z, Yang H, Tang J and Chen Z: Receptor-interacting protein kinase 3 deficiency recruits myeloid-derived suppressor cells to hepatocellular carcinoma through the chemokine (C-X-C Motif) ligand 1-chemokine (C-X-C Motif) receptor 2 axis. Hepatology. 70:1564–1581. 2019. View Article : Google Scholar : PubMed/NCBI | |
Xu M, Zhao Z, Song J, Lan X, Lu S, Chen M, Wang Z, Chen W, Fan X, Wu F, et al: Interactions between interleukin-6 and myeloid-derived suppressor cells drive the chemoresistant phenotype of hepatocellular cancer. Exp Cell Res. 351:142–149. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sonnenberg GF and Hepworth MR: Functional interactions between innate lymphoid cells and adaptive immunity. Nat Rev Immunol. 19:599–613. 2019. View Article : Google Scholar : PubMed/NCBI | |
Warner K and Ohashi PS: ILC regulation of T cell responses in inflammatory diseases and cancer. Semin Immunol. 41:1012842019. View Article : Google Scholar : PubMed/NCBI | |
Han X, Huang T and Han J: Cytokines derived from innate lymphoid cells assist Helicobacter hepaticus to aggravate hepatocellular tumorigenesis in viral transgenic mice. Gut Pathog. 11:232019. View Article : Google Scholar : PubMed/NCBI | |
Cai L, Zhang Z, Zhou L, Wang H, Fu J, Zhang S, Shi M, Zhang H, Yang Y, Wu H, et al: Functional impairment in circulating and intrahepatic NK cells and relative mechanism in hepatocellular carcinoma patients. Clin Immunol. 129:428–437. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wu Y, Kuang DM, Pan WD, Wan YL, Lao XM, Wang D, Li XF and Zheng L: Monocyte/macrophage-elicited natural killer cell dysfunction in hepatocellular carcinoma is mediated by CD48/2B4 interactions. Hepatology. 57:1107–1116. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tatsumi T and Takehara T: Impact of natural killer cells on chronic hepatitis C and hepatocellular carcinoma. Hepatol Res. 46:416–422. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bugide S, Green MR and Wajapeyee N: Inhibition of Enhancer of zeste homolog 2 (EZH2) induces natural killer cell-mediated eradication of hepatocellular carcinoma cells. Proc Natl Acad Sci USA. 115:E3509–E3518. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Hao X, Sun R, Wei H and Tian Z: Natural killer cell-derived interferon-gamma promotes hepatocellular carcinoma through the epithelial cell adhesion molecule-epithelial-to-mesenchymal transition axis in hepatitis B virus transgenic mice. Hepatology. 69:1735–1750. 2019. View Article : Google Scholar : PubMed/NCBI | |
Luo Q, Luo W, Zhu Q, Huang H, Peng H, Liu R, Xie M, Li S, Li M, Hu X and Zou Y: Tumor-derived soluble MICA obstructs the NKG2D pathway to restrain NK cytotoxicity. Aging Dis. 11:118–128. 2020. View Article : Google Scholar : PubMed/NCBI | |
Vujanovic L, Stahl EC, Pardee AD, Geller DA, Tsung A, Watkins SC, Gibson GA, Storkus WJ and Butterfield LH: Tumor-derived α-fetoprotein directly drives human natural killer-cell activation and subsequent cell death. Cancer Immunol Res. 5:493–502. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mossanen J, Kohlhepp M, Wehr A, Krenkel O, Liepelt A, Roeth A, Möckel D, Heymann F, Lammers T, Gassler N, et al: CXCR6 inhibits hepatocarcinogenesis by promoting natural killer T- and CD4 T-cell-dependent control of senescence. Gastroenterology. 156:1877–1889.e4. 2019. View Article : Google Scholar : PubMed/NCBI | |
Miyagi T, Takehara T, Tatsumi T, Kanto T, Suzuki T, Jinushi M, Sugimoto Y, Sasaki Y, Hori M and Hayashi N: CD1d-mediated stimulation of natural killer T cells selectively activates hepatic natural killer cells to eliminate experimentally disseminated hepatoma cells in murine liver. Int J Cancer. 106:81–89. 2003. View Article : Google Scholar : PubMed/NCBI | |
Vivier E, Ugolini S, Blaise D, Chabannon C and Brossay L: Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol. 12:239–252. 2012. View Article : Google Scholar : PubMed/NCBI | |
Xiao Y, Gao Q, Xu X, Li Y, Ju M, Cai M, Dai C, Hu J, Qiu S, Zhou J and Fan J: Combination of intratumoral invariant natural killer T cells and interferon-gamma is associated with prognosis of hepatocellular carcinoma after curative resection. PLoS One. 8:e703452013. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Gingold J and Su X: Immunomodulatory TGF-β signaling in hepatocellular carcinoma. Trends Mol Med. 25:1010–1023. 2019. View Article : Google Scholar : PubMed/NCBI | |
Li J, Lee Y, Li Y, Jiang Y, Lu H, Zang W, Zhao X, Liu L, Chen Y, Tan H, et al: Co-inhibitory molecule B7 superfamily member 1 expressed by tumor-infiltrating myeloid cells induces dysfunction of anti-tumor CD8+ T cells. Immunity. 48:773–786.e5. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hiroishi K, Eguchi J, Baba T, Shimazaki T, Ishii S, Hiraide A, Sakaki M, Doi H, Uozumi S, Omori R, et al: Strong CD8(+) T-cell responses against tumor-associated antigens prolong the recurrence-free interval after tumor treatment in patients with hepatocellular carcinoma. J Gastroenterol. 45:451–458. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zong L, Peng H, Sun C, Li F, Zheng M, Chen Y, Wei H, Sun R and Tian Z: Breakdown of adaptive immunotolerance induces hepatocellular carcinoma in HBsAg-tg mice. Nat Commun. 10:2212019. View Article : Google Scholar : PubMed/NCBI | |
Sachdeva M: Immunology of hepatocellular carcinoma. World J Hepatol. 7:2080–2090. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lu Z, Zuo B, Jing R, Gao X, Rao Q, Liu Z, Qi H, Guo H and Yin H: Dendritic cell-derived exosomes elicit tumor regression in autochthonous hepatocellular carcinoma mouse models. J Hepatol. 67:739–748. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sconocchia G, Eppenberger S, Spagnoli GC, Tornillo L, Droeser R, Caratelli S, Ferrelli F, Coppola A, Arriga R, Lauro D, et al: NK cells and T cells cooperate during the clinical course of colorectal cancer. Oncoimmunology. 3:e9521972014. View Article : Google Scholar : PubMed/NCBI | |
Li X, Yao W, Yuan Y, Chen P, Li B, Li J, Chu R, Song H, Xie D, Jiang X and Wang H: Targeting of tumour-infiltrating macrophages via CCL2/CCR2 signalling as a therapeutic strategy against hepatocellular carcinoma. Gut. 66:157–167. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Song Y, Lin D, Lei L, Mei Y, Jin Z, Gong H, Zhu Y, Hu B, Zhang Y, et al: NCR− group 3 innate lymphoid cells orchestrate IL-23/IL-17 axis to promote hepatocellular carcinoma development. EBioMedicine. 41:333–344. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liu CQ, Xu J, Zhou ZG, Jin LL, Yu XJ, Xiao G, Lin J, Zhuang SM, Zhang YJ and Zheng L: Expression patterns of programmed death ligand 1 correlate with different microenvironments and patient prognosis in hepatocellular carcinoma. Br J Cancer. 119:80–88. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lim T, Chew V, Sieow J, Goh S, Yeong J, Soon A and Ricciardi-Castagnoli P: PD-1 expression on dendritic cells suppresses CD8 T cell function and antitumor immunity. Oncoimmunology. 5:e10851462016. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Fan L, Yu H, Zhang J, He Y, Feng D, Wang F, Li X, Liu Q, Li Y, et al: Endoplasmic reticulum stress causes liver cancer cells to release exosomal miR-23a-3p and up-regulate programmed death ligand 1 expression in macrophages. Hepatology. 70:241–258. 2019.PubMed/NCBI | |
Mossanen JC, Kohlhepp M, Wehr A, Krenkel O, Liepelt A, Roeth AA, Mockel D, Heymann F, Lammers T, Gassler N, et al: CXCR6 inhibits hepatocarcinogenesis by promoting natural killer T- and CD4+ T-cell-dependent control of senescence. Gastroenterology. 156:1877–1889.e4. 2019. View Article : Google Scholar : PubMed/NCBI | |
Shigeta K, Datta M, Hato T, Kitahara S, Chen IX, Matsui A, Kikuchi H, Mamessier E, Aoki S, Ramjiawan RR, et al: Dual programmed death receptor-1 and vascular endothelial growth factor receptor-2 blockade promotes vascular normalization and enhances antitumor immune responses in hepatocellular carcinoma. Hepatology. 71:1247–1261. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhou Y, Xu X, Ding J, Jing X, Wang F, Wang Y and Wang P: Dynamic changes of T-cell subsets and their relation with tumor recurrence after microwave ablation in patients with hepatocellular carcinoma. J Cancer Res Ther. 14:40–45. 2018. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Jiang Z and Zhang L: Dual effect of T helper cell 17 (Th17) and regulatory T cell (Treg) in liver pathological process: From occurrence to end stage of disease. Int Immunopharmacol. 69:50–59. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kondo Y and Shimosegawa T: Significant roles of regulatory T cells and myeloid derived suppressor cells in hepatitis B virus persistent infection and hepatitis B virus-related HCCs. Int J Mol Sci. 16:3307–3322. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wu Q, Zhou W, Yin S, Zhou Y, Chen T, Qian J, Su R, Hong L, Lu H, Zhang F, et al: Blocking triggering receptor expressed on myeloid cells-1-positive tumor-associated macrophages induced by hypoxia reverses immunosuppression and anti-programmed cell death ligand 1 resistance in liver cancer. Hepatology. 70:198–214. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhou SL, Zhou ZJ, Hu ZQ, Huang XW, Wang Z, Chen EB, Fan J, Cao Y, Dai Z and Zhou J: Tumor-associated neutrophils recruit macrophages and T-regulatory cells to promote progression of hepatocellular carcinoma and resistance to sorafenib. Gastroenterology. 150:1646–1658.e7. 2016. View Article : Google Scholar : PubMed/NCBI | |
Murphy K and Reiner S: The lineage decisions of helper T cells. Nat Rev Immunol. 2:933–944. 2002. View Article : Google Scholar : PubMed/NCBI | |
Geginat J, Paroni M, Maglie S, Alfen J, Kastirr I, Gruarin P, De Simone M, Pagani M and Abrignani S: Plasticity of human CD4 T cell subsets. Front Immunol. 5:6302014. View Article : Google Scholar : PubMed/NCBI | |
Mirchandani AS, Besnard AG, Yip E, Scott C, Bain CC, Cerovic V, Salmond RJ and Liew FY: Type 2 innate lymphoid cells drive CD4+ Th2 cell responses. J Immunol. 192:2442–2448. 2014. View Article : Google Scholar : PubMed/NCBI | |
Shen G, Krienke S, Schiller P, Nießen A, Neu S, Eckstein V, Schiller M, Lorenz H-M and Tykocinski LO: Microvesicles released by apoptotic human neutrophils suppress proliferation and IL-2/IL-2 receptor expression of resting T helper cells. Eur J Immunol. 47:900–910. 2017. View Article : Google Scholar : PubMed/NCBI | |
Duffy A, Ulahannan S, Makorova-Rusher O, Rahma O, Wedemeyer H, Pratt D, Davis J, Hughes M, Heller T, ElGindi M, et al: Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma. J Hepatol. 66:545–551. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lee JH, Lee JH, Lim YS, Yeon JE, Song TJ, Yu SJ, Gwak GY, Kim KM, Kim YJ, Lee JW and Yoon JH: Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma. Gastroenterology. 148:1383–1391.e6. 2015. View Article : Google Scholar : PubMed/NCBI | |
Okusaka T and Ikeda M: Immunotherapy for hepatocellular carcinoma: Current status and future perspectives. ESMO Open. 3:e0004552018. View Article : Google Scholar : PubMed/NCBI | |
Guerra AD, Yeung OWH, Qi X, Kao WJ and Man K: The anti-tumor effects of M1 macrophage-loaded poly (ethylene glycol) and gelatin-based hydrogels on hepatocellular carcinoma. Theranostics. 7:3732–3744. 2017. View Article : Google Scholar : PubMed/NCBI | |
Jiang W, Zhang C, Tian Z and Zhang J: hIL-15 gene-modified human natural killer cells (NKL-IL15) augments the anti-human hepatocellular carcinoma effect in vivo. Immunobiology. 219:547–553. 2014. View Article : Google Scholar : PubMed/NCBI | |
Palmer DH, Midgley RS, Mirza N, Torr EE, Ahmed F, Steele JC, Steven NM, Kerr DJ, Young LS and Adams DH: A phase II study of adoptive immunotherapy using dendritic cells pulsed with tumor lysate in patients with hepatocellular carcinoma. Hepatology. 49:124–132. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lee JH, Tak WY, Lee Y, Heo MK, Song JS, Kim HY, Park SY, Bae SH, Lee JH, Heo J, et al: Adjuvant immunotherapy with autologous dendritic cells for hepatocellular carcinoma, randomized phase II study. Oncoimmunology. 6:e13283352017. View Article : Google Scholar : PubMed/NCBI | |
Sawada Y, Yoshikawa T, Shimomura M, Iwama T, Endo I and Nakatsura T: Programmed death-1 blockade enhances the antitumor effects of peptide vaccine-induced peptide-specific cytotoxic T lymphocytes. Int J Oncol. 46:28–36. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gao H, Li K, Tu H, Pan X, Jiang H, Shi B, Kong J, Wang H, Yang S, Gu J and Li Z: Development of T cells redirected to glypican-3 for the treatment of hepatocellular carcinoma. Clin Cancer Res. 20:6418–6428. 2014. View Article : Google Scholar : PubMed/NCBI | |
Majzner R and Mackall C: Clinical lessons learned from the first leg of the CAR T cell journey. Nat Med. 25:1341–1355. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kole C, Charalampakis N, Tsakatikas S, Vailas M, Moris D, Gkotsis E, Kykalos S, Karamouzis M and Schizas D: Immunotherapy for hepatocellular carcinoma: A 2021 update. Cancers (Basel). 12:E28592020. View Article : Google Scholar : PubMed/NCBI | |
Chang C, Dinh T, Lee Y, Wang F, Sung Y, Yu P, Chiu S, Shih Y, Wu C, Huang Y, et al: Nanoparticle delivery of MnO2 and anti-angiogenic therapy to overcome hypoxia-driven tumor escape and suppress hepatocellular carcinoma. ACS Appl Mater Interfaces. 12:44407–44419. 2020. View Article : Google Scholar : PubMed/NCBI | |
Tian H, Zhu X, Lv Y, Jiao Y and Wang G: Glucometabolic reprogramming in the hepatocellular carcinoma microenvironment: Cause and effect. Cancer Manag Res. 12:5957–5974. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Lou Y, Bai X and Liang T: Intratumoral heterogeneity of hepatocellular carcinoma: From single-cell to population-based studies. World J Gastroenterol. 26:3720–3736. 2020. View Article : Google Scholar : PubMed/NCBI | |
Liu F, Qin L, Liao Z, Song J, Yuan C, Liu Y, Wang Y, Xu H, Zhang Q, Pei Y, et al: Microenvironment characterization and multi-omics signatures related to prognosis and immunotherapy response of hepatocellular carcinoma. Exp Hematol Oncol. 9:102020. View Article : Google Scholar : PubMed/NCBI | |
Xiong X, Kuang H, Ansari S, Liu T, Gong J, Wang S, Zhao XY, Ji Y, Li C, Guo L, et al: Landscape of intercellular crosstalk in healthy and NASH liver revealed by single-cell secretome gene analysis. Mol Cell. 75:644–660.e5. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, He Y, Luo N, Patel SJ, Han Y, Gao R, Modak M, Carotta S, Haslinger C, Kind D, et al: Landscape and dynamics of single immune cells in hepatocellular carcinoma. Cell. 179:829–845.e20. 2019. View Article : Google Scholar : PubMed/NCBI | |
Caruso S, O'Brien D, Cleary S, Roberts L and Zucman-Rossi J: Genetics of HCC: Novel approaches to explore molecular diversity. Hepatology. May 28–2020.(Epub ahead of print). View Article : Google Scholar |