The advances in immunotherapy for hepatocellular carcinoma

Fan Zhang , Yumin Li

Hepatoma Research ›› 2020, Vol. 6 : 40

PDF
Hepatoma Research ›› 2020, Vol. 6:40 DOI: 10.20517/2394-5079.2020.20
Review
Review

The advances in immunotherapy for hepatocellular carcinoma

Author information +
History +
PDF

Abstract

Hepatocellular carcinoma (HCC) is one of the malignant tumors with higher incidence and mortality worldwide. Recently, significant progress has been made in uncovering immunotherapy in HCC, for instance programmed death-1, cytotoxic T-lymphocyte antigen 4, chimeric antigen receptor T-cell therapy, T cell receptor T cell therapy, dendritic cell vaccine, and cytokine-induced killer cells. This paper reviews the advances in immunotherapy and focuses on the results of many of preclinical studies and clinical trials in the field, as well as some of the promising therapeutic strategies for HCC in the future.

Keywords

HCC / PD-1 / PD-L1 / CTLA-4 / CAR-T / T cell receptor / DC / CIK

Cite this article

Download citation ▾
Fan Zhang, Yumin Li. The advances in immunotherapy for hepatocellular carcinoma. Hepatoma Research, 2020, 6: 40 DOI:10.20517/2394-5079.2020.20

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Bray F,Soerjomataram I,Torre LA.Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries..CA Cancer J Clin2018;68:394-424

[2]

Tian Y,Qiu W,Zhang Z.ER-residential Nogo-B accelerates NAFLD-associated HCC mediated by metabolic reprogramming of oxLDL lipophagy..Nat Commun2019;10:3391 PMCID:PMC6662851

[3]

Papatheodoridis GV,Hansen BE,Lampertico P.Risk of hepatocellular carcinoma in chronic hepatitis B: assessment and modification with current antiviral therapy..J Hepatol2015;62:956-67

[4]

Singal AG,Mehta N,Pillai A.Direct-acting antiviral therapy for hepatitis C virus infection is associated with increased survival in patients with a history of hepatocellular carcinoma..Gastroenterology2019;157:1253-63.e2 PMCID:PMC6815711

[5]

Yang JD,Gores GJ,Plymoth A.A global view of hepatocellular carcinoma: trends, risk, prevention and management..Nat Rev Gastroenterol Hepatol2019;16:589-604 PMCID:PMC6813818

[6]

Desert R,Canal F,Desille M.Human hepatocellular carcinomas with a periportal phenotype have the lowest potential for early recurrence after curative resection..Hepatology2017;66:1502-18

[7]

Bruix J,Reig M.Insights into the success and failure of systemic therapy for hepatocellular carcinoma..Nat Rev Gastroenterol Hepatol2019;16:617-30

[8]

Topalian SL,Brahmer JR,Smith DC.Safety, activity, and immune correlates of anti-PD-1 antibody in cancer..N Engl J Med2012;366:2443-54 PMCID:PMC3544539

[9]

Mason R,Ingles Garces A.Current and emerging systemic therapies for cutaneous metastatic melanoma..Expert Opin Pharmacother2019;20:1135-52

[10]

Administration UFaD. FDA approves tisagenlecleucel for B-cell ALL and tocilizumab for cytokine release syndrome. 2017. Available from: https://www.fda.gov/Drugs/InformationOnDrugs/ApprovedDrugs/ucm606540.htm [Last accessed on 16 Jun 2020]

[11]

Agata Y,Nishimura H,Tsubata T.Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes..Int Immunol1996;8:765-72

[12]

Latchman Y,Chernova T,Borde M.PD-L2 is a second ligand for PD-1 and inhibits T cell activation..Nat Immunol2001;2:261-8

[13]

Freeman GJ,Iwai Y,Chernova T.Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation..J Exp Med2000;192:1027-34 PMCID:PMC2193311

[14]

Finkelmeier F,Trojan J.Nivolumab for the treatment of hepatocellular carcinoma..Expert Rev Anticancer Ther2018;18:1169-75

[15]

Yarchoan M,Luan L,Sharma RB.Characterization of the Immune Microenvironment in Hepatocellular Carcinoma..Clin Cancer Res2017;23:7333-9 PMCID:PMC5881396

[16]

Mocan T,Craciun R,Leucuta DC.Programmed cell death protein-1 (PD-1)/programmed death-ligand-1 (PD-L1) axis in hepatocellular carcinoma: prognostic and therapeutic perspectives..Clin Transl Oncol2019;21:702-12

[17]

Shi F,Zeng Z,Liu ZW.PD-1 and PD-L1 upregulation promotes CD8(+) T-cell apoptosis and postoperative recurrence in hepatocellular carcinoma patients..Int J Cancer2011;128:887-96

[18]

Long J,Pan XF,Wan HH.Expression of programmed death ligand-1 and programmed death 1 in hepatocellular carcinoma and its clinical significance..J Cancer Res Ther2018;14:S1188-92

[19]

Ma LJ,Dong LQ,Duan M.Clinical significance of PD-1/PD-Ls gene amplification and overexpression in patients with hepatocellular carcinoma..Theranostics2018;8:5690-702 PMCID:PMC6276293

[20]

Jung HI,Ji S,Bae SH.Overexpression of PD-L1 and PD-L2 is associated with poor prognosis in patients with hepatocellular carcinoma..Cancer Res Treat2017;49:246-54 PMCID:PMC5266389

[21]

Liu CQ,Zhou ZG,Yu XJ.Expression patterns of programmed death ligand 1 correlate with different microenvironments and patient prognosis in hepatocellular carcinoma..Br J Cancer2018;119:80-8 PMCID:PMC6035200

[22]

Chang H,Kim A,Kim WB.Expression and prognostic significance of programmed death protein 1 and programmed death ligand-1, and cytotoxic T lymphocyte-associated molecule-4 in hepatocellular carcinoma..Apmis2017;125:690-8

[23]

Gabrielson A,Wang H,Kallakury B.Intratumoral CD3 and CD8 T-cell densities associated with relapse-free survival in HCC..Cancer Immunol Res2016;4:419-30 PMCID:PMC5303359

[24]

Huang CY,Luo GY,Li YQ.Relationship between PD-L1 expression and CD8+ T-cell immune responses in hepatocellular carcinoma..J Immunother2017;40:323-33

[25]

Umemoto Y,Matsumoto Y,Matono R.Prognostic impact of programmed cell death 1 ligand 1 expression in human leukocyte antigen class I-positive hepatocellular carcinoma after curative hepatectomy..J Gastroenterol2015;50:65-75

[26]

Chang B,Wei H,Zhu D.The correlation and prognostic value of serum levels of soluble programmed death protein 1 (sPD-1) and soluble programmed death-ligand 1 (sPD-L1) in patients with hepatocellular carcinoma..Cancer Immunol Immunother2019;68:353-63 PMCID:PMC6426820

[27]

Cheng HY,Chuang YH,Jan MC.Circulating programmed death-1 as a marker for sustained high hepatitis B viral load and risk of hepatocellular carcinoma..PLoS One2014;9:e95870 PMCID:PMC4245192

[28]

Li N,Li F,Han Q.Circulating soluble programmed death-1 levels may differentiate immune-tolerant phase from other phases and hepatocellular carcinoma from other clinical diseases in chronic hepatitis B virus infection..Oncotarget2017;8:46020-33 PMCID:PMC5542245

[29]

Liang L,Zhang F.The suppressive effect of co-inhibiting PD-1 and CTLA-4 expression on H22 hepatomas in mice..Cell Mol Biol Lett2018;23:58 PMCID:PMC6295075

[30]

Song B,Meng F.T cell inflammation profile after surgical resection may predict tumor recurrence in HBV-related hepatocellular carcinoma..Int Immunopharmacol2016;41:35-41

[31]

Liu F,Zhou S,Sun N.Blocking Tim-3 or/and PD-1 reverses dysfunction of tumor-infiltrating lymphocytes in HBV-related hepatocellular carcinoma..Bull Cancer2018;105:493-501

[32]

He G,Zhou J,Chen Y.Peritumoural neutrophils negatively regulate adaptive immunity via the PD-L1/PD-1 signalling pathway in hepatocellular carcinoma..J Exp Clin Cancer Res2015;34:141 PMCID:PMC4652417

[33]

El-Khoueiry AB,Yau T,Kudo M.Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): an open-label, non-comparative, phase 1/2 dose escalation and expansion trial..Lancet2017;389:2492-502

[34]

Finkelmeier F,Perkhofer L,Trojan J.Feasibility and safety of nivolumab in advanced hepatocellular carcinoma: real-life experience from three German centers..J Cancer Res Clin Oncol2019;145:253-9

[35]

Zhu AX,Edeline J,Ogasawara S.Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): a non-randomised, open-label phase 2 trial..Lancet Oncol2018;19:940-52

[36]

Marquardt JU,Czauderna C.The changing landscape of systemic treatment of advanced hepatocellular carcinoma: new targeted agents and immunotherapies..Target Oncol2019;14:115-23

[37]

Qin SK,Meng ZQ,Chai XL.A randomized multicentered phase II study to evaluate SHR-1210 (PD-1 antibody) in subjects with advanced hepatocellular carcinoma (HCC) who failed or intolerable to prior systemic treatment..Ann Oncol2018;29:viii719-20

[38]

Llopiz D,Villanueva L,Silva L.Enhanced anti-tumor efficacy of checkpoint inhibitors in combination with the histone deacetylase inhibitor Belinostat in a murine hepatocellular carcinoma model..Cancer Immunol Immunother2019;68:379-93

[39]

Li H,Liu S,Zhang B.Programmed cell death-1 (PD-1) checkpoint blockade in combination with a mammalian target of rapamycin inhibitor restrains hepatocellular carcinoma growth induced by hepatoma cell-intrinsic PD-1..Hepatology2017;66:1920-33

[40]

Chen ML,Lu WC,Yu SL.Sorafenib relieves cell-intrinsic and cell-extrinsic inhibitions of effector T cells in tumor microenvironment to augment antitumor immunity..Int J Cancer2014;134:319-31

[41]

Kimura T,Ozawa Y,Ito J.Immunomodulatory activity of lenvatinib contributes to antitumor activity in the Hepa1-6 hepatocellular carcinoma model..Cancer Sci2018;109:3993-4002 PMCID:PMC6272102

[42]

Butty V,Sabeti P,Benoist C.Signatures of strong population differentiation shape extended haplotypes across the human CD28, CTLA4, and ICOS costimulatory genes..Proc Natl Acad Sci USA2007;104:570-5 PMCID:PMC1766426

[43]

Esensten JH,Chopra G,Bluestone JA.CD28 costimulation: from mechanism to therapy..Immunity2016;44:973-88 PMCID:PMC4932896

[44]

Valk E,Schneider H.CTLA-4 trafficking and surface expression..Trends Immunol2008;29:272-9 PMCID:PMC4186961

[45]

Yang J,Chen Y,Liu C.Association of CTLA-4 tagging polymorphisms and haplotypes with hepatocellular carcinoma risk: a case-control study..Medicine (Baltimore)2019;98:e16266 PMCID:PMC6709186

[46]

Wang C,Zhao L.Association of cytotoxic T-lymphocyte antigen-4 + 49A/G gene polymorphism with hepatocellular carcinoma risk in Chinese..J Cancer Res Ther2018;14:S1117-20

[47]

Hu L,Chen X,Liu L.CTLA-4 gene polymorphism +49 A/G contributes to genetic susceptibility to two infection-related cancers-hepatocellular carcinoma and cervical cancer..Hum Immunol2010;71:888-91

[48]

Gu X,Zhou F,Wang H.+49G > A polymorphism in the cytotoxic T-lymphocyte antigen-4 gene increases susceptibility to hepatitis B-related hepatocellular carcinoma in a male Chinese population..Hum Immunol2010;71:83-7

[49]

Sangro B,de la Mata M,Garralda E.A clinical trial of CTLA-4 blockade with tremelimumab in patients with hepatocellular carcinoma and chronic hepatitis C..J Hepatol2013;59:81-8

[50]

Duffy AG,Makorova-Rusher O,Wedemeyer H.Tremelimumab in combination with ablation in patients with advanced hepatocellular carcinoma..J Hepatol2017;66:545-51 PMCID:PMC5316490

[51]

Ribas A,Lopez-Berestein G,Bulanhagui CA.Antitumor activity in melanoma and anti-self responses in a phase I trial with the anti-cytotoxic T lymphocyte-associated antigen 4 monoclonal antibody CP-675,206..J Clin Oncol2005;23:8968-77

[52]

Antonia S,Balmanoukian A,Sanborn RE.Safety and antitumour activity of durvalumab plus tremelimumab in non-small cell lung cancer: a multicentre, phase 1b study..Lancet Oncol2016;17:299-308 PMCID:PMC5500167

[53]

Xie C,Mabry-Hrones D,Levy E.Tremelimumab in combination with microwave ablation in patients with refractory biliary tract cancer..Hepatology2019;69:2048-60 PMCID:PMC6461476

[54]

Agdashian D,Xie C,Pratt D.The effect of anti-CTLA4 treatment on peripheral and intra-tumoral T cells in patients with hepatocellular carcinoma..Cancer Immunol Immunother2019;68:599-608 PMCID:PMC6662600

[55]

Mohty M,Malard F,Bazarbachi A.CD19 chimeric antigen receptor-T cells in B-cell leukemia and lymphoma: current status and perspectives..Leukemia2019;33:2767-78

[56]

Wilkie S,Foster J,Julien S.Retargeting of human T cells to tumor-associated MUC1: the evolution of a chimeric antigen receptor..J Immunol2008;180:4901-9

[57]

Zhao L.Engineered T cell therapy for cancer in the clinic..Front Immunol2019;10:2250 PMCID:PMC6798078

[58]

Sadelain M,Riddell S.Therapeutic T cell engineering..Nature2017;545:423-31 PMCID:PMC5632949

[59]

Gao H,Tu H,Jiang H.Development of T cells redirected to glypican-3 for the treatment of hepatocellular carcinoma..Clin Cancer Res2014;20:6418-28

[60]

Chen C,Jiang H,Gao H.Development of T cells carrying two complementary chimeric antigen receptors against glypican-3 and asialoglycoprotein receptor 1 for the treatment of hepatocellular carcinoma..Cancer Immunol Immunother2017;66:475-89

[61]

Pan Z,Shi B,Shi Z.Increased antitumor activities of glypican-3-specific chimeric antigen receptor-modified T cells by coexpression of a soluble PD1-CH3 fusion protein..Cancer Immunol Immunother2018;67:1621-34

[62]

Zhou F,Yu X.Glypican-3: a promising biomarker for hepatocellular carcinoma diagnosis and treatment..Med Res Rev2018;38:741-67

[63]

Baumhoer D,Stadlmann S,Diamantis EK.Glypican 3 expression in human nonneoplastic, preneoplastic, and neoplastic tissues: a tissue microarray analysis of 4,387 tissue samples..Am J Clin Pathol2008;129:899-906

[64]

Zhai B,Gao H,Jiang H.A phase I study of anti-GPC3 chimeric antigen receptor modified T cells (GPC3 CAR-T) in Chinese patients with refractory or relapsed GPC3 + hepatocellular carcinoma (r/r GPC3 + HCC)..J Clin Oncol2017;35:3049

[65]

He Y,Mizejewski GJ.Engineering α-fetoprotein-based gene vaccines to prevent and treat hepatocellular carcinoma: review and future prospects..Immunotherapy2014;6:725-36 PMCID:PMC4151252

[66]

Nakagawa H,Kobayashi E,Hamana H.Association between high-avidity T-cell receptors, induced by α-fetoprotein-derived peptides, and anti-tumor effects in patients with hepatocellular carcinoma..Gastroenterology2017;152:1395-406.e10

[67]

Liu H,Xiang J,Green S.Targeting alpha-fetoprotein (AFP)-MHC complex with CAR T-cell therapy for liver cancer..Clin Cancer Res2017;23:478-88

[68]

Parkhurst MR,Langan RC,Nathan DA.T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis..Mol Ther2011;19:620-6 PMCID:PMC3048186

[69]

Xu Y,Horan LH,Liu L.A novel antibody-TCR (AbTCR) platform combines Fab-based antigen recognition with gamma/delta-TCR signaling to facilitate T-cell cytotoxicity with low cytokine release..Cell Discov2018;4:62 PMCID:PMC6242878

[70]

Lin KR,Jin YB,Pan YM.T cell receptor repertoire profiling predicts the prognosis of HBV-associated hepatocellular carcinoma..Cancer Med2018;7:3755-62 PMCID:PMC6089190

[71]

Qasim W,Gehring AJ,Schurich A.Immunotherapy of HCC metastases with autologous T cell receptor redirected T cells, targeting HBsAg in a liver transplant patient..J Hepatol2015;62:486-91

[72]

Brechot C,Louise A,Tiollais P.Presence of integrated hepatitis B virus DNA sequences in cellular DNA of human hepatocellular carcinoma..Nature1980;286:533-5

[73]

Gehring AJ,Ho ZZ,Ruedl C.Engineering virus-specific T cells that target HBV infected hepatocytes and hepatocellular carcinoma cell lines..J Hepatol2011;55:103-10

[74]

Tan AT,Lee Krishnamoorthy T,Chua A.Use of expression profiles of HBV-DNA integrated into genomes of hepatocellular carcinoma cells to select T cells for immunotherapy..Gastroenterology2019;156:1862-76.e9

[75]

Spear TT,Roszkowski JJ,Simms PE.TCR gene-modified T cells can efficiently treat established hepatitis C-associated hepatocellular carcinoma tumors..Cancer Immunol Immunother2016;65:293-304 PMCID:PMC4887146

[76]

Zhu W,Wang L,Jiang X.Identification of alpha-fetoprotein-specific T-cell receptors for hepatocellular carcinoma immunotherapy..Hepatology2018;68:574-89

[77]

Dargel C,Hasreiter J,Bockmann JH.T cells engineered to express a T-cell receptor specific for glypican-3 to recognize and kill hepatoma cells in vitro and in mice..Gastroenterology2015;149:1042-52

[78]

Yin XY,Lai YR,Huang JF.Prognostic significances of tumor-infiltrating S-100 positive dendritic cells and lymphocytes in patients with hepatocellular carcinoma..Hepatogastroenterology2003;50:1281-4

[79]

Cai XY,Qiu SJ,Wu ZQ.Dendritic cell infiltration and prognosis of human hepatocellular carcinoma..J Cancer Res Clin Oncol2006;132:293-301

[80]

Ladhams A,Sing G,Fielding G.Treatment of non-resectable hepatocellular carcinoma with autologous tumor-pulsed dendritic cells..J Gastroenterol Hepatol2002;17:889-96

[81]

Lee WC,Hung CF,Lia CR.Vaccination of advanced hepatocellular carcinoma patients with tumor lysate-pulsed dendritic cells: a clinical trial..J Immunother2005;28:496-504

[82]

Palmer DH,Mirza N,Ahmed F.A phase II study of adoptive immunotherapy using dendritic cells pulsed with tumor lysate in patients with hepatocellular carcinoma..Hepatology2009;49:124-32

[83]

El Ansary M,Elhamid SA,Aboelkasem F.Immunotherapy by autologous dendritic cell vaccine in patients with advanced HCC..J Cancer Res Clin Oncol2013;139:39-48 PMCID:PMC5223882

[84]

Kakumu S,Ishikawa T,Tagaya T.Decreased function of peripheral blood dendritic cells in patients with hepatocellular carcinoma with hepatitis B and C virus infection..J Gastroenterol Hepatol2000;15:431-6

[85]

Tan XH,Liu C,Shao XT.Immunization with dendritic cells infected with human AFP adenovirus vector effectively elicits immunity against mouse hepatocellular carcinomas..Zhonghua Zhong Liu Za Zhi2006;28:13-6

[86]

Yang JY,Xue Y,Liu WC.Improvement of dendritic-based vaccine efficacy against hepatitis B virus-related hepatocellular carcinoma by two tumor-associated antigen gene-infected dendritic cells..Hum Immunol2010;71:255-62

[87]

Shi M,Chen WW,Zhang B.Hepatitis B virus (HBV) antigen-pulsed monocyte-derived dendritic cells from HBV-associated hepatocellular carcinoma patients significantly enhance specific T cell responses in vitro..Clin Exp Immunol2007;147:277-86 PMCID:PMC1810470

[88]

Guo DW,Hou XZ,Jiang XF.Glypican3 in genetically modified human monocyte-derived dendritic cells induced specific cytotoxity against glypican3 overexpressing human hepatocellular carcinoma cells in vitro..Saudi Med J2008;29:1235-40

[89]

Tada F,Hirooka M,Hiasa Y.Phase I/II study of immunotherapy using tumor antigen-pulsed dendritic cells in patients with hepatocellular carcinoma..Int J Oncol2012;41:1601-9 PMCID:PMC3583872

[90]

Lee JH,Lee M,Song JS.A phase I/IIa study of adjuvant immunotherapy with tumour antigen-pulsed dendritic cells in patients with hepatocellular carcinoma..Br J Cancer2015;113:1666-76 PMCID:PMC4702003

[91]

Ge C,Wang Q,Lu Y.Improved efficacy of therapeutic vaccination with dendritic cells pulsed with tumor cell lysate against hepatocellular carcinoma by introduction of 2 tandem repeats of microbial HSP70 peptide epitope 407-426 and OK-432..Int Immunopharmacol2011;11:2200-7

[92]

Nakamoto Y,Kitahara M,Sakai Y.Prolonged recurrence-free survival following OK432-stimulated dendritic cell transfer into hepatocellular carcinoma during transarterial embolization..Clin Exp Immunol2011;163:165-77 PMCID:PMC3043307

[93]

Maeda Y,Matsui H,Tamesa T.Dendritic cells transfected with heat-shock protein 70 messenger RNA for patients with hepatitis C virus-related hepatocellular carcinoma: a phase 1 dose escalation clinical trial..Cancer Immunol Immunother2015;64:1047-56

[94]

Chen C,Zhang YT,Zhou N.Effect of dendritic cell-based immunotherapy on hepatocellular carcinoma: a systematic review and meta-analysis..Cytotherapy2018;20:975-89

[95]

Ninomiya T,Masumoto T,Onji M.Dendritic cells with immature phenotype and defective function in the peripheral blood from patients with hepatocellular carcinoma..J Hepatol1999;31:323-31

[96]

Chen S,Tanimoto K,Iuchi H.Absence of CD83-positive mature and activated dendritic cells at cancer nodules from patients with hepatocellular carcinoma: relevance to hepatocarcinogenesis..Cancer Lett2000;148:49-57

[97]

Iwashita Y,Tahara K,Chen CL.Potent stimuli combined with lipopolysaccaride and IFNgamma may improve immunotherapy against HCC by increasing the maturation and subsequent immune response of the dendritic cells..Cancer Biother Radiopharm2003;18:1-6

[98]

Gonzalez-Carmona MA,Timmerman A,Kornek M.CD40ligand-expressing dendritic cells induce regression of hepatocellular carcinoma by activating innate and acquired immunity in vivo..Hepatology2008;48:157-68

[99]

Chan RC,Wang YD,Xie Y.Transduction of dendritic cells with recombinant adenovirus encoding HCA661 activates autologous cytotoxic T lymphocytes to target hepatoma cells..Br J Cancer2004;90:1636-43 PMCID:PMC2409703

[100]

Peng W,Ma Y,Wang X.Dendritic cells transfected with PEG10 recombinant adenovirus elicit anti-tumor immune response in vitro and in vivo..Vaccine2011;29:3501-6

[101]

Vogt A,Lukacs-Kornek V,Raskopf E.Improving immunotherapy of hepatocellular carcinoma (HCC) using dendritic cells (DC) engineered to express IL-12 in vivo..Liver Int2014;34:447-61

[102]

Choi YJ,Park YS,Yang KM.EpCAM peptide-primed dendritic cell vaccination confers significant anti-tumor immunity in hepatocellular carcinoma cells..PLoS One2018;13:e0190638 PMCID:PMC5752035

[103]

Yang X,Hu Z.Dendritic cells transduced with TEM8 recombinant adenovirus prevents hepatocellular carcinoma angiogenesis and inhibits cells growth..Vaccine2010;28:7130-5

[104]

Su H,Zheng L,Zhang L.Immunotherapy based on dendritic cells pulsed with CTPFoxM1 fusion protein protects against the development of hepatocellular carcinoma..Oncotarget2016;7:48401-11 PMCID:PMC5217026

[105]

Zerbini A,Fagnoni F,Pizzi MG.Increased immunostimulatory activity conferred to antigen-presenting cells by exposure to antigen extract from hepatocellular carcinoma after radiofrequency thermal ablation..J Immunother2008;31:271-82

[106]

Hu Z,Zhou S,Duan S.Mouse IP-10 gene delivered by folate-modified chitosan nanoparticles and dendritic/tumor cells fusion vaccine effectively inhibit the growth of hepatocellular carcinoma in mice..Theranostics2017;7:1942-52 PMCID:PMC5479281

[107]

Lee JH,Lim YS,Song TJ.Adjuvant immunotherapy with autologous cytokine-induced killer cells for hepatocellular carcinoma..Gastroenterology2015;148:1383-91.e6

[108]

Jung NC,Choi HJ,Song JY.Dendritic cell immunotherapy combined with cytokine-induced killer cells effectively suppresses established hepatocellular carcinomas in mice..Immunol Invest2016;45:553-65

[109]

Chen BA,Sun ZY,Gao C.Killing activity in DC and CIK co-culture against hepatocarcinoma cells..Zhongguo Shi Yan Xue Ye Xue Za Zhi2006;14:543-6

[110]

Qiu Y,Yun MM,Zhang RM.Hepatocellular carcinoma-specific immunotherapy with synthesized alpha1,3- galactosyl epitope-pulsed dendritic cells and cytokine-induced killer cells..World J Gastroenterol2011;17:5260-6 PMCID:PMC3247689

[111]

Niu LZ,Zeng JY,Liao MT.Combination treatment with comprehensive cryoablation and immunotherapy in metastatic hepatocellular cancer..World J Gastroenterol2013;19:3473-80 PMCID:PMC3683687

[112]

Yoon JS,Lee JH,Kim SW.Adjuvant cytokine-induced killer cell immunotherapy for hepatocellular carcinoma: a propensity score-matched analysis of real-world data..BMC Cancer2019;19:523 PMCID:PMC6543598

[113]

Lee JH,Lim YS,Song TJ.Sustained efficacy of adjuvant immunotherapy with cytokine-induced killer cells for hepatocellular carcinoma: an extended 5-year follow-up..Cancer Immunol Immunother2019;68:23-32 PMCID:PMC6326973

[114]

Guo W,Wu D.Dendritic cell-cytokine induced killer cell immunotherapy combined with transcatheter arterial chemoembolization for hepatocellular carcinoma: safety and efficacy..Nan Fang Yi Ke Da Xue Xue Bao2014;34:674-8

[115]

He G,Huo H,Zhu Z.TACE combined with dendritic cells and cytokine-induced killer cells in the treatment of hepatocellular carcinoma: a meta-analysis..Int Immunopharmacol2016;40:436-42

[116]

Zhou Z,Weng L.Clinical efficacy of DC-CIK combined with sorafenib in the treatment of advanced hepatocellular carcinoma..J Buon2019;24:615-21

[117]

Gonzalez-Carmona MA,Hoffmann P,Sievers E.Patient-derived dendritic cells transduced with an a-fetoprotein-encoding adenovirus and co-cultured with autologous cytokine-induced lymphocytes induce a specific and strong immune response against hepatocellular carcinoma cells..Liver Int2006;26:369-79

[118]

Yu X,Zhang T,Xie Y.Enhanced cytotoxicity of IL-24 gene-modified dendritic cells co-cultured with cytokine-induced killer cells to hepatocellular carcinoma cells..Int J Hematol2010;92:276-82

[119]

Wang Y,Mu H,Chen X.Enhanced specific antitumor immunity of dendritic cells transduced with the glypican 3 gene and co-cultured with cytokine-induced killer cells against hepatocellular carcinoma cells..Mol Med Rep2015;11:3361-7 PMCID:PMC4368068

PDF

94

Accesses

0

Citation

Detail

Sections
Recommended

/