Skip to main content
Top
Published in: Journal of Gastroenterology 3/2015

01-03-2015 | Review

MICA SNPs and the NKG2D system in virus-induced HCC

Authors: Kaku Goto, Naoya Kato

Published in: Journal of Gastroenterology | Issue 3/2015

Login to get access

Abstract

Hepatocellular carcinoma (HCC) is one of the most frequent causes of cancer-related death globally. Above well-known risk factors for HCC development ranging from various toxins to diseases such as diabetes mellitus, chronic infection with hepatitis B virus and hepatitis C virus (HCV) poses the most serious threat, constituting the cause in more than 80 % of cases. In addition to the viral genes intensively investigated, the pathophysiological importance of host genetic factors has also been greatly and increasingly appreciated. Genome-wide association studies (GWAS) comprehensively search the host genome at the single-nucleotide level, and have successfully identified the genomic region associated with a whole variety of diseases. With respect to HCC, there have been reports from several groups on single nucleotide polymorphisms (SNPs) associated with hepatocarcinogenesis, among which was our GWAS discovering MHC class I polypeptide-related sequence A (MICA) as a susceptibility gene for HCV-induced HCC. MICA is a natural killer (NK) group 2D (NKG2D) ligand, whose interaction with NKG2D triggers NK cell-mediated cytotoxicity toward the target cells, and is a key molecule in tumor immune surveillance as its expression is induced on stressed cells such as transformed tumor cells for the detection by NK cells. In this review, the latest understanding of the MICA–NKG2D system in viral HCC, particularly focused on its antitumor properties and the involvement of MICA SNPs, is summarized, followed by a discussion of targets for state-of-the-art cancer immunotherapy with personalized medicine in view.
Literature
2.
go back to reference Aravalli RN, Steer CJ, Cressman EN. Molecular mechanisms of hepatocellular carcinoma. Hepatology. 2008;48:2047–63.PubMed Aravalli RN, Steer CJ, Cressman EN. Molecular mechanisms of hepatocellular carcinoma. Hepatology. 2008;48:2047–63.PubMed
3.
go back to reference Arzumanyan A, Reis HM, Feitelson MA. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat Rev Cancer. 2013;13:123–35.PubMed Arzumanyan A, Reis HM, Feitelson MA. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat Rev Cancer. 2013;13:123–35.PubMed
4.
go back to reference Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.PubMed Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.PubMed
5.
go back to reference El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–76.PubMed El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology. 2007;132:2557–76.PubMed
6.
go back to reference Shlomai A, de Jong YP, Rice CM. Virus associated malignancies: the role of viral hepatitis in hepatocellular carcinoma. Semin Cancer Biol. 2014;26:78–88.PubMed Shlomai A, de Jong YP, Rice CM. Virus associated malignancies: the role of viral hepatitis in hepatocellular carcinoma. Semin Cancer Biol. 2014;26:78–88.PubMed
7.
go back to reference Miki D, Ochi H, Hayes CN, Aikata H, Chayama K. Hepatocellular carcinoma: towards personalized medicine. Cancer Sci. 2012;103:846–50.PubMed Miki D, Ochi H, Hayes CN, Aikata H, Chayama K. Hepatocellular carcinoma: towards personalized medicine. Cancer Sci. 2012;103:846–50.PubMed
8.
go back to reference Kato N, Ji G, Wang Y, Baba M, Hoshida Y, Otsuka M, et al. Large-scale search of single nucleotide polymorphisms for hepatocellular carcinoma susceptibility genes in patients with hepatitis C. Hepatology. 2005;42:846–53.PubMed Kato N, Ji G, Wang Y, Baba M, Hoshida Y, Otsuka M, et al. Large-scale search of single nucleotide polymorphisms for hepatocellular carcinoma susceptibility genes in patients with hepatitis C. Hepatology. 2005;42:846–53.PubMed
9.
go back to reference Manolio TA. Bringing genome-wide association findings into clinical use. Nat Rev Genet. 2013;14:549–58.PubMed Manolio TA. Bringing genome-wide association findings into clinical use. Nat Rev Genet. 2013;14:549–58.PubMed
10.
go back to reference Han ZG. Functional genomic studies: insights into the pathogenesis of liver cancer. Annu Rev Genomics Hum Genet. 2012;13:171–205.PubMed Han ZG. Functional genomic studies: insights into the pathogenesis of liver cancer. Annu Rev Genomics Hum Genet. 2012;13:171–205.PubMed
11.
go back to reference Nishida N, Kudo M. Recent advancements in comprehensive genetic analyses for human hepatocellular carcinoma. Oncology. 2013;84(Suppl 1):93–7.PubMed Nishida N, Kudo M. Recent advancements in comprehensive genetic analyses for human hepatocellular carcinoma. Oncology. 2013;84(Suppl 1):93–7.PubMed
13.
go back to reference Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R, Hosono N, et al. Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat Genet. 2011;43:455–8.PubMed Kumar V, Kato N, Urabe Y, Takahashi A, Muroyama R, Hosono N, et al. Genome-wide association study identifies a susceptibility locus for HCV-induced hepatocellular carcinoma. Nat Genet. 2011;43:455–8.PubMed
14.
go back to reference Kahraman A, Fingas CD, Syn WK, Gerken G, Canbay A. Role of stress-induced NKG2D ligands in liver diseases. Liver Int. 2012;32:370–82.PubMed Kahraman A, Fingas CD, Syn WK, Gerken G, Canbay A. Role of stress-induced NKG2D ligands in liver diseases. Liver Int. 2012;32:370–82.PubMed
15.
go back to reference Watzl C. The NKG2D receptor and its ligands-recognition beyond the “missing self”? Microbes Infect. 2003;5:31–7.PubMed Watzl C. The NKG2D receptor and its ligands-recognition beyond the “missing self”? Microbes Infect. 2003;5:31–7.PubMed
16.
go back to reference Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285:727–9.PubMed Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285:727–9.PubMed
17.
go back to reference Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A. 1996;93:12445–50.PubMedCentralPubMed Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A. 1996;93:12445–50.PubMedCentralPubMed
18.
go back to reference Bjorkstrom NK, Kekalainen E, Mjosberg J. Tissue-specific effector functions of innate lymphoid cells. Immunology. 2013;139:416–27.PubMedCentralPubMed Bjorkstrom NK, Kekalainen E, Mjosberg J. Tissue-specific effector functions of innate lymphoid cells. Immunology. 2013;139:416–27.PubMedCentralPubMed
19.
go back to reference Castello G, Scala S, Palmieri G, Curley SA, Izzo F. HCV-related hepatocellular carcinoma: from chronic inflammation to cancer. Clin Immunol. 2010;134:237–50.PubMed Castello G, Scala S, Palmieri G, Curley SA, Izzo F. HCV-related hepatocellular carcinoma: from chronic inflammation to cancer. Clin Immunol. 2010;134:237–50.PubMed
20.
go back to reference Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9:503–10.PubMed Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9:503–10.PubMed
21.
go back to reference Miletic A, Krmpotic A, Jonjic S. The evolutionary arms race between NK cells and viruses: who gets the short end of the stick? Eur J Immunol. 2013;43:867–77.PubMed Miletic A, Krmpotic A, Jonjic S. The evolutionary arms race between NK cells and viruses: who gets the short end of the stick? Eur J Immunol. 2013;43:867–77.PubMed
22.
go back to reference Cheng M, Chen Y, Xiao W, Sun R, Tian Z. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol. 2013;10:230–52.PubMedCentralPubMed Cheng M, Chen Y, Xiao W, Sun R, Tian Z. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol. 2013;10:230–52.PubMedCentralPubMed
23.
go back to reference Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986;319:675–8.PubMed Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature. 1986;319:675–8.PubMed
24.
go back to reference Marcus A, Gowen BG, Thompson TW, Iannello A, Ardolino M, Deng W, et al. Recognition of tumors by the innate immune system and natural killer cells. Adv Immunol. 2014;122:91–128.PubMedCentralPubMed Marcus A, Gowen BG, Thompson TW, Iannello A, Ardolino M, Deng W, et al. Recognition of tumors by the innate immune system and natural killer cells. Adv Immunol. 2014;122:91–128.PubMedCentralPubMed
25.
go back to reference Shabani Z, Bagheri M, Zare-Bidaki M, Hassanshahi G, Arababadi MK, Mohammadi Nejad M. NK cells in hepatitis B virus infection: a potent target for immunotherapy. Arch Virol. 2014;159:1555–65.PubMed Shabani Z, Bagheri M, Zare-Bidaki M, Hassanshahi G, Arababadi MK, Mohammadi Nejad M. NK cells in hepatitis B virus infection: a potent target for immunotherapy. Arch Virol. 2014;159:1555–65.PubMed
26.
go back to reference Kasahara M, Yoshida S. Immunogenetics of the NKG2D ligand gene family. Immunogenetics. 2012;64:855–67.PubMed Kasahara M, Yoshida S. Immunogenetics of the NKG2D ligand gene family. Immunogenetics. 2012;64:855–67.PubMed
27.
go back to reference Chan CJ, Smyth MJ, Martinet L. Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ. 2013;21:5–14.PubMedCentralPubMed Chan CJ, Smyth MJ, Martinet L. Molecular mechanisms of natural killer cell activation in response to cellular stress. Cell Death Differ. 2013;21:5–14.PubMedCentralPubMed
28.
29.
go back to reference Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene. 2008;27:5944–58.PubMed Nausch N, Cerwenka A. NKG2D ligands in tumor immunity. Oncogene. 2008;27:5944–58.PubMed
30.
go back to reference Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol. 2002;169:4098–102.PubMed Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol. 2002;169:4098–102.PubMed
31.
go back to reference Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 2002;419:734–8.PubMed Groh V, Wu J, Yee C, Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature. 2002;419:734–8.PubMed
32.
go back to reference Sun D, Wang X, Zhang H, Deng L, Zhang Y. MMP9 mediates MICA shedding in human osteosarcomas. Cell Biol Int. 2011;35:569–74.PubMed Sun D, Wang X, Zhang H, Deng L, Zhang Y. MMP9 mediates MICA shedding in human osteosarcomas. Cell Biol Int. 2011;35:569–74.PubMed
33.
go back to reference Liu G, Atteridge CL, Wang X, Lundgren AD, Wu JD. The membrane type matrix metalloproteinase MMP14 mediates constitutive shedding of MHC class I chain-related molecule A independent of a disintegrin and metalloproteinases. J Immunol. 2010;184:3346–50.PubMedCentralPubMed Liu G, Atteridge CL, Wang X, Lundgren AD, Wu JD. The membrane type matrix metalloproteinase MMP14 mediates constitutive shedding of MHC class I chain-related molecule A independent of a disintegrin and metalloproteinases. J Immunol. 2010;184:3346–50.PubMedCentralPubMed
34.
go back to reference Kohga K, Takehara T, Tatsumi T, Ishida H, Miyagi T, Hosui A, et al. Sorafenib inhibits the shedding of major histocompatibility complex class I-related chain A on hepatocellular carcinoma cells by down-regulating a disintegrin and metalloproteinase 9. Hepatology. 2010;51:1264–73.PubMed Kohga K, Takehara T, Tatsumi T, Ishida H, Miyagi T, Hosui A, et al. Sorafenib inhibits the shedding of major histocompatibility complex class I-related chain A on hepatocellular carcinoma cells by down-regulating a disintegrin and metalloproteinase 9. Hepatology. 2010;51:1264–73.PubMed
35.
go back to reference Kohga K, Takehara T, Tatsumi T, Miyagi T, Ishida H, Ohkawa K, et al. Anticancer chemotherapy inhibits MHC class I-related chain a ectodomain shedding by downregulating ADAM10 expression in hepatocellular carcinoma. Cancer Res. 2009;69:8050–7.PubMed Kohga K, Takehara T, Tatsumi T, Miyagi T, Ishida H, Ohkawa K, et al. Anticancer chemotherapy inhibits MHC class I-related chain a ectodomain shedding by downregulating ADAM10 expression in hepatocellular carcinoma. Cancer Res. 2009;69:8050–7.PubMed
36.
go back to reference Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68:6368–76.PubMed Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, et al. Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 2008;68:6368–76.PubMed
37.
go back to reference Chitadze G, Bhat J, Lettau M, Janssen O, Kabelitz D. Generation of soluble NKG2D ligands: proteolytic cleavage, exosome secretion and functional implications. Scand J Immunol. 2013;78:120–9.PubMed Chitadze G, Bhat J, Lettau M, Janssen O, Kabelitz D. Generation of soluble NKG2D ligands: proteolytic cleavage, exosome secretion and functional implications. Scand J Immunol. 2013;78:120–9.PubMed
38.
go back to reference Marten A, von Lilienfeld-Toal M, Buchler MW, Schmidt J. Soluble MIC is elevated in the serum of patients with pancreatic carcinoma diminishing gammadelta T cell cytotoxicity. Int J Cancer. 2006;119:2359–65.PubMed Marten A, von Lilienfeld-Toal M, Buchler MW, Schmidt J. Soluble MIC is elevated in the serum of patients with pancreatic carcinoma diminishing gammadelta T cell cytotoxicity. Int J Cancer. 2006;119:2359–65.PubMed
39.
go back to reference Bahram S, Bresnahan M, Geraghty DE, Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci U S A. 1994;91:6259–63.PubMedCentralPubMed Bahram S, Bresnahan M, Geraghty DE, Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci U S A. 1994;91:6259–63.PubMedCentralPubMed
40.
go back to reference Mok JW, Lee YJ, Kim JY, Lee EB, Song YW, Park MH, et al. Association of MICA polymorphism with rheumatoid arthritis patients in Koreans. Hum Immunol. 2003;64:1190–4.PubMed Mok JW, Lee YJ, Kim JY, Lee EB, Song YW, Park MH, et al. Association of MICA polymorphism with rheumatoid arthritis patients in Koreans. Hum Immunol. 2003;64:1190–4.PubMed
41.
go back to reference Mizuki N, Ota M, Kimura M, Ohno S, Ando H, Katsuyama Y, et al. Triplet repeat polymorphism in the transmembrane region of the MICA gene: a strong association of six GCT repetitions with Behçet disease. Proc Natl Acad Sci U S A. 1997;94:1298–303.PubMedCentralPubMed Mizuki N, Ota M, Kimura M, Ohno S, Ando H, Katsuyama Y, et al. Triplet repeat polymorphism in the transmembrane region of the MICA gene: a strong association of six GCT repetitions with Behçet disease. Proc Natl Acad Sci U S A. 1997;94:1298–303.PubMedCentralPubMed
42.
go back to reference Park Y, Lee H, Sanjeevi CB, Eisenbarth GS. MICA polymorphism is associated with type 1 diabetes in the Korean population. Diabetes Care. 2001;24:33–8.PubMed Park Y, Lee H, Sanjeevi CB, Eisenbarth GS. MICA polymorphism is associated with type 1 diabetes in the Korean population. Diabetes Care. 2001;24:33–8.PubMed
43.
go back to reference Tinto N, Ciacci C, Calcagno G, Gennarelli D, Spampanato A, Farinaro E, et al. Increased prevalence of celiac disease without gastrointestinal symptoms in adults MICA 5.1 homozygous subjects from the Campania area. Dig Liver Dis. 2008;40:248–52.PubMed Tinto N, Ciacci C, Calcagno G, Gennarelli D, Spampanato A, Farinaro E, et al. Increased prevalence of celiac disease without gastrointestinal symptoms in adults MICA 5.1 homozygous subjects from the Campania area. Dig Liver Dis. 2008;40:248–52.PubMed
44.
go back to reference Gong Z, Luo QZ, Lin L, Su YP, Peng HB, Du K, et al. Association of MICA gene polymorphisms with liver fibrosis in schistosomiasis patients in the Dongting Lake region. Braz J Med Biol Res. 2012;45:222–9.PubMedCentralPubMed Gong Z, Luo QZ, Lin L, Su YP, Peng HB, Du K, et al. Association of MICA gene polymorphisms with liver fibrosis in schistosomiasis patients in the Dongting Lake region. Braz J Med Biol Res. 2012;45:222–9.PubMedCentralPubMed
45.
go back to reference Tonnerre P, Gerard N, Chatelais M, Poli C, Allard S, Cury S, et al. MICA variant promotes allosensitization after kidney transplantation. J Am Soc Nephrol. 2013;24:954–66.PubMedCentralPubMed Tonnerre P, Gerard N, Chatelais M, Poli C, Allard S, Cury S, et al. MICA variant promotes allosensitization after kidney transplantation. J Am Soc Nephrol. 2013;24:954–66.PubMedCentralPubMed
46.
go back to reference Jiang X, Zou Y, Huo Z, Yu P. Association of major histocompatibility complex class I chain-related gene A microsatellite polymorphism and hepatocellular carcinoma in South China Han population. Tissue Antigens. 2011;78:143–7.PubMed Jiang X, Zou Y, Huo Z, Yu P. Association of major histocompatibility complex class I chain-related gene A microsatellite polymorphism and hepatocellular carcinoma in South China Han population. Tissue Antigens. 2011;78:143–7.PubMed
47.
go back to reference Tamaki S, Kawakami M, Yamanaka Y, Shimomura H, Imai Y, Ishida J, et al. Relationship between soluble MICA and the MICA A5.1 homozygous genotype in patients with oral squamous cell carcinoma. Clin Immunol. 2009;130:331–7.PubMed Tamaki S, Kawakami M, Yamanaka Y, Shimomura H, Imai Y, Ishida J, et al. Relationship between soluble MICA and the MICA A5.1 homozygous genotype in patients with oral squamous cell carcinoma. Clin Immunol. 2009;130:331–7.PubMed
48.
go back to reference Lu M, Xia B, Ge L, Li Y, Zhao J, Chen F. Role of major histocompatibility complex class I-related molecules A*A5.1 allele in ulcerative colitis in Chinese patients. Immunology. 2009;128:e230–6.PubMedCentralPubMed Lu M, Xia B, Ge L, Li Y, Zhao J, Chen F. Role of major histocompatibility complex class I-related molecules A*A5.1 allele in ulcerative colitis in Chinese patients. Immunology. 2009;128:e230–6.PubMedCentralPubMed
49.
go back to reference Steinle A, Li P, Morris DL, Groh V, Lanier LL, Strong RK, et al. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics. 2001;53:279–87.PubMed Steinle A, Li P, Morris DL, Groh V, Lanier LL, Strong RK, et al. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics. 2001;53:279–87.PubMed
50.
go back to reference Lopez-Hernandez R, Valdes M, Lucas D, Campillo JA, Martinez-Garcia P, Salama H, et al. Association analysis of MICA gene polymorphism and MICA-129 dimorphism with inflammatory bowel disease susceptibility in a Spanish population. Hum Immunol. 2010;71:512–4.PubMed Lopez-Hernandez R, Valdes M, Lucas D, Campillo JA, Martinez-Garcia P, Salama H, et al. Association analysis of MICA gene polymorphism and MICA-129 dimorphism with inflammatory bowel disease susceptibility in a Spanish population. Hum Immunol. 2010;71:512–4.PubMed
51.
go back to reference Raache R, Belanteur K, Amroun H, Benyahia A, Heniche A, Azzouz M, et al. Association of major histocompatibility complex class 1 chain-related gene a dimorphism with type 1 diabetes and latent autoimmune diabetes in adults in the Algerian population. Clin Vaccine Immunol. 2012;19:557–61.PubMedCentralPubMed Raache R, Belanteur K, Amroun H, Benyahia A, Heniche A, Azzouz M, et al. Association of major histocompatibility complex class 1 chain-related gene a dimorphism with type 1 diabetes and latent autoimmune diabetes in adults in the Algerian population. Clin Vaccine Immunol. 2012;19:557–61.PubMedCentralPubMed
52.
go back to reference Boukouaci W, Busson M, de Peffault Latour R, Rocha V, Suberbielle C, Bengoufa D. MICA-129 genotype, soluble MICA, and anti-MICA antibodies as biomarkers of chronic graft-versus-host disease. Blood. 2009;114:5216–24.PubMed Boukouaci W, Busson M, de Peffault Latour R, Rocha V, Suberbielle C, Bengoufa D. MICA-129 genotype, soluble MICA, and anti-MICA antibodies as biomarkers of chronic graft-versus-host disease. Blood. 2009;114:5216–24.PubMed
53.
go back to reference Kirsten H, Petit-Teixeira E, Scholz M, Hasenclever D, Hantmann H, Heider D, et al. Association of MICA with rheumatoid arthritis independent of known HLA-DRB1 risk alleles in a family-based and a case control study. Arthritis Res Ther. 2009;11:R60.PubMedCentralPubMed Kirsten H, Petit-Teixeira E, Scholz M, Hasenclever D, Hantmann H, Heider D, et al. Association of MICA with rheumatoid arthritis independent of known HLA-DRB1 risk alleles in a family-based and a case control study. Arthritis Res Ther. 2009;11:R60.PubMedCentralPubMed
54.
go back to reference Thomas DL. Global control of hepatitis C: where challenge meets opportunity. Nat Med. 2013;19:850–8.PubMed Thomas DL. Global control of hepatitis C: where challenge meets opportunity. Nat Med. 2013;19:850–8.PubMed
55.
go back to reference Strader DB, Wright T, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C. Hepatology. 2004;39:1147–71.PubMed Strader DB, Wright T, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C. Hepatology. 2004;39:1147–71.PubMed
56.
go back to reference Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology. 2004;127:S35–50.PubMed Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology. 2004;127:S35–50.PubMed
57.
58.
go back to reference Goto K, Lin W, Zhang L, Jilg N, Shao RX, Schaefer EA, et al. The AMPK-related kinase SNARK regulates hepatitis C virus replication and pathogenesis through enhancement of TGF-β signaling. J Hepatol. 2013;59:942–8.PubMed Goto K, Lin W, Zhang L, Jilg N, Shao RX, Schaefer EA, et al. The AMPK-related kinase SNARK regulates hepatitis C virus replication and pathogenesis through enhancement of TGF-β signaling. J Hepatol. 2013;59:942–8.PubMed
60.
go back to reference Kato N, Yoshida H, Ono-Nita SK, Kato J, Goto T, Otsuka M, et al. Activation of intracellular signaling by hepatitis B and C viruses: C-viral core is the most potent signal inducer. Hepatology. 2000;32:405–12.PubMed Kato N, Yoshida H, Ono-Nita SK, Kato J, Goto T, Otsuka M, et al. Activation of intracellular signaling by hepatitis B and C viruses: C-viral core is the most potent signal inducer. Hepatology. 2000;32:405–12.PubMed
61.
go back to reference Caldwell S, Park SH. The epidemiology of hepatocellular cancer: from the perspectives of public health problem to tumor biology. J Gastroenterol. 2009;44(Suppl 19):96–101.PubMed Caldwell S, Park SH. The epidemiology of hepatocellular cancer: from the perspectives of public health problem to tumor biology. J Gastroenterol. 2009;44(Suppl 19):96–101.PubMed
62.
go back to reference Otsuka M, Kishikawa T, Yoshikawa T, Ohno M, Takata A, Shibata C. The role of microRNAs in hepatocarcinogenesis: current knowledge and future prospects. J Gastroenterol. 2013;49(2):173–84.PubMed Otsuka M, Kishikawa T, Yoshikawa T, Ohno M, Takata A, Shibata C. The role of microRNAs in hepatocarcinogenesis: current knowledge and future prospects. J Gastroenterol. 2013;49(2):173–84.PubMed
63.
go back to reference Negrini M, Gramantieri L, Sabbioni S, Croce CM. microRNA involvement in hepatocellular carcinoma. Anticancer Agents Med Chem. 2011;11:500–21.PubMed Negrini M, Gramantieri L, Sabbioni S, Croce CM. microRNA involvement in hepatocellular carcinoma. Anticancer Agents Med Chem. 2011;11:500–21.PubMed
64.
go back to reference Schmidt N, Neumann-Haefelin C, Thimme R. Cellular immune responses to hepatocellular carcinoma: lessons for immunotherapy. Dig Dis. 2012;30:483–91.PubMed Schmidt N, Neumann-Haefelin C, Thimme R. Cellular immune responses to hepatocellular carcinoma: lessons for immunotherapy. Dig Dis. 2012;30:483–91.PubMed
65.
go back to reference Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T, et al. Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J Immunol. 2003;171:5423–9.PubMed Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T, et al. Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J Immunol. 2003;171:5423–9.PubMed
66.
go back to reference Lunemann S, Malone DF, Hengst J, Port K, Grabowski J, Deterding K, et al. Compromised function of natural killer cells in acute and chronic viral hepatitis. J Infect Dis. 2014;209:1362–73.PubMed Lunemann S, Malone DF, Hengst J, Port K, Grabowski J, Deterding K, et al. Compromised function of natural killer cells in acute and chronic viral hepatitis. J Infect Dis. 2014;209:1362–73.PubMed
67.
go back to reference Varchetta S, Mele D, Mantovani S, Oliviero B, Cremonesi E, Ludovisi S, et al. Impaired intrahepatic natural killer cell cytotoxic function in chronic hepatitis C virus infection. Hepatology. 2012;56:841–9.PubMed Varchetta S, Mele D, Mantovani S, Oliviero B, Cremonesi E, Ludovisi S, et al. Impaired intrahepatic natural killer cell cytotoxic function in chronic hepatitis C virus infection. Hepatology. 2012;56:841–9.PubMed
69.
go back to reference Glassner A, Eisenhardt M, Kramer B, Korner C, Coenen M, Sauerbruch T, et al. NK cells from HCV-infected patients effectively induce apoptosis of activated primary human hepatic stellate cells in a TRAIL-, FasL- and NKG2D-dependent manner. Lab Invest. 2012;92:967–77.PubMed Glassner A, Eisenhardt M, Kramer B, Korner C, Coenen M, Sauerbruch T, et al. NK cells from HCV-infected patients effectively induce apoptosis of activated primary human hepatic stellate cells in a TRAIL-, FasL- and NKG2D-dependent manner. Lab Invest. 2012;92:967–77.PubMed
70.
go back to reference Korangy F, Hochst B, Manns MP, Greten TF. Immune responses in hepatocellular carcinoma. Dig Dis. 2010;28:150–4.PubMed Korangy F, Hochst B, Manns MP, Greten TF. Immune responses in hepatocellular carcinoma. Dig Dis. 2010;28:150–4.PubMed
71.
go back to reference Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009;50:799–807.PubMed Hoechst B, Voigtlaender T, Ormandy L, Gamrekelashvili J, Zhao F, Wedemeyer H, et al. Myeloid derived suppressor cells inhibit natural killer cells in patients with hepatocellular carcinoma via the NKp30 receptor. Hepatology. 2009;50:799–807.PubMed
72.
go back to reference Cai L, Zhang Z, Zhou L, Wang H, Fu J, Zhang S, et al. Functional impairment in circulating and intrahepatic NK cells and relative mechanism in hepatocellular carcinoma patients. Clin Immunol. 2008;129:428–37.PubMed Cai L, Zhang Z, Zhou L, Wang H, Fu J, Zhang S, et al. Functional impairment in circulating and intrahepatic NK cells and relative mechanism in hepatocellular carcinoma patients. Clin Immunol. 2008;129:428–37.PubMed
73.
go back to reference Sene D, Levasseur F, Abel M, Lambert M, Camous X, Hernandez C, et al. Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog. 2010;6:e1001184.PubMedCentralPubMed Sene D, Levasseur F, Abel M, Lambert M, Camous X, Hernandez C, et al. Hepatitis C virus (HCV) evades NKG2D-dependent NK cell responses through NS5A-mediated imbalance of inflammatory cytokines. PLoS Pathog. 2010;6:e1001184.PubMedCentralPubMed
74.
go back to reference Kamimura H, Yamagiwa S, Tsuchiya A, Takamura M, Matsuda Y, Ohkoshi S, et al. Reduced NKG2D ligand expression in hepatocellular carcinoma correlates with early recurrence. J Hepatol. 2012;56:381–8.PubMed Kamimura H, Yamagiwa S, Tsuchiya A, Takamura M, Matsuda Y, Ohkoshi S, et al. Reduced NKG2D ligand expression in hepatocellular carcinoma correlates with early recurrence. J Hepatol. 2012;56:381–8.PubMed
75.
go back to reference Wen C, He X, Ma H, Hou N, Wei C, Song T, et al. Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell Mol Immunol. 2008;5:475–8.PubMedCentralPubMed Wen C, He X, Ma H, Hou N, Wei C, Song T, et al. Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell Mol Immunol. 2008;5:475–8.PubMedCentralPubMed
76.
go back to reference Kim H, Bose SK, Meyer K, Ray R. Hepatitis C virus impairs natural killer cell mediated augmentation of complement synthesis. J Virol. 2014;88:2564–71.PubMedCentralPubMed Kim H, Bose SK, Meyer K, Ray R. Hepatitis C virus impairs natural killer cell mediated augmentation of complement synthesis. J Virol. 2014;88:2564–71.PubMedCentralPubMed
77.
go back to reference Jinushi M, Takehara T, Tatsumi T, Hiramatsu N, Sakamori R, Yamaguchi S, et al. Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas. J Hepatol. 2005;43:1013–20.PubMed Jinushi M, Takehara T, Tatsumi T, Hiramatsu N, Sakamori R, Yamaguchi S, et al. Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas. J Hepatol. 2005;43:1013–20.PubMed
78.
go back to reference Lopez-Vazquez A, Rodrigo L, Mina-Blanco A, Martinez-Borra J, Fuentes D, Rodriguez M, et al. Extended human leukocyte antigen haplotype EH18.1 influences progression to hepatocellular carcinoma in patients with hepatitis C virus infection. J Infect Dis. 2004;189:957–63.PubMed Lopez-Vazquez A, Rodrigo L, Mina-Blanco A, Martinez-Borra J, Fuentes D, Rodriguez M, et al. Extended human leukocyte antigen haplotype EH18.1 influences progression to hepatocellular carcinoma in patients with hepatitis C virus infection. J Infect Dis. 2004;189:957–63.PubMed
79.
go back to reference Lo PH, Urabe Y, Kumar V, Tanikawa C, Koike K, Kato N, et al. Identification of a functional variant in the MICA promoter which regulates MICA expression and increases HCV-related hepatocellular carcinoma risk. PLoS One. 2013;8:e61279.PubMedCentralPubMed Lo PH, Urabe Y, Kumar V, Tanikawa C, Koike K, Kato N, et al. Identification of a functional variant in the MICA promoter which regulates MICA expression and increases HCV-related hepatocellular carcinoma risk. PLoS One. 2013;8:e61279.PubMedCentralPubMed
80.
go back to reference Ngamruengphong S, Patel T. Molecular evolution of genetic susceptibility to hepatocellular carcinoma. Dig Dis Sci. 2014;59:986–91.PubMed Ngamruengphong S, Patel T. Molecular evolution of genetic susceptibility to hepatocellular carcinoma. Dig Dis Sci. 2014;59:986–91.PubMed
81.
go back to reference Lange CM, Bibert S, Dufour JF, Cellerai C, Cerny A, Heim MH, et al. Comparative genetic analyses point to HCP5 as susceptibility locus for HCV-associated hepatocellular carcinoma. J Hepatol. 2013;59:504–9.PubMed Lange CM, Bibert S, Dufour JF, Cellerai C, Cerny A, Heim MH, et al. Comparative genetic analyses point to HCP5 as susceptibility locus for HCV-associated hepatocellular carcinoma. J Hepatol. 2013;59:504–9.PubMed
82.
go back to reference Motomura T, Ono Y, Shirabe K, Fukuhara T, Konishi H, Mano Y, et al. Neither MICA nor DEPDC5 genetic polymorphisms correlate with hepatocellular carcinoma recurrence following hepatectomy. HPB Surg. 2012;2012:185496.PubMedCentralPubMed Motomura T, Ono Y, Shirabe K, Fukuhara T, Konishi H, Mano Y, et al. Neither MICA nor DEPDC5 genetic polymorphisms correlate with hepatocellular carcinoma recurrence following hepatectomy. HPB Surg. 2012;2012:185496.PubMedCentralPubMed
83.
go back to reference Feitelson MA, Bonamassa B, Arzumanyan A. The roles of hepatitis B virus-encoded X protein in virus replication and the pathogenesis of chronic liver disease. Expert Opin Ther Targets. 2014;18:293–306.PubMed Feitelson MA, Bonamassa B, Arzumanyan A. The roles of hepatitis B virus-encoded X protein in virus replication and the pathogenesis of chronic liver disease. Expert Opin Ther Targets. 2014;18:293–306.PubMed
84.
go back to reference Li Y, Wang JJ, Gao S, Liu Q, Bai J, Zhao XQ, et al. Decreased peripheral natural killer cells activity in the immune activated stage of chronic hepatitis B. PLoS One. 2014;9:e86927.PubMedCentralPubMed Li Y, Wang JJ, Gao S, Liu Q, Bai J, Zhao XQ, et al. Decreased peripheral natural killer cells activity in the immune activated stage of chronic hepatitis B. PLoS One. 2014;9:e86927.PubMedCentralPubMed
85.
go back to reference Peppa D, Micco L, Javaid A, Kennedy PT, Schurich A, Dunn C, et al. Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog. 2010;6:e1001227.PubMedCentralPubMed Peppa D, Micco L, Javaid A, Kennedy PT, Schurich A, Dunn C, et al. Blockade of immunosuppressive cytokines restores NK cell antiviral function in chronic hepatitis B virus infection. PLoS Pathog. 2010;6:e1001227.PubMedCentralPubMed
86.
go back to reference Chen Y, Wei H, Sun R, Tian Z. Impaired function of hepatic natural killer cells from murine chronic HBsAg carriers. Int Immunopharmacol. 2005;5:1839–52.PubMed Chen Y, Wei H, Sun R, Tian Z. Impaired function of hepatic natural killer cells from murine chronic HBsAg carriers. Int Immunopharmacol. 2005;5:1839–52.PubMed
87.
go back to reference Rehermann B. Pathogenesis of chronic viral hepatitis: differential roles of T cells and NK cells. Nat Med. 2013;19:859–68.PubMed Rehermann B. Pathogenesis of chronic viral hepatitis: differential roles of T cells and NK cells. Nat Med. 2013;19:859–68.PubMed
88.
go back to reference Sun C, Fu B, Gao Y, Liao X, Sun R, Tian Z, et al. TGF-beta1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog. 2012;8:e1002594.PubMedCentralPubMed Sun C, Fu B, Gao Y, Liao X, Sun R, Tian Z, et al. TGF-beta1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog. 2012;8:e1002594.PubMedCentralPubMed
89.
go back to reference Zwirner NW, Fuertes MB, Girart MV, Domaica CI, Rossi LE. Cytokine-driven regulation of NK cell functions in tumor immunity: role of the MICA-NKG2D system. Cytokine Growth Factor Rev. 2007;18:159–70.PubMed Zwirner NW, Fuertes MB, Girart MV, Domaica CI, Rossi LE. Cytokine-driven regulation of NK cell functions in tumor immunity: role of the MICA-NKG2D system. Cytokine Growth Factor Rev. 2007;18:159–70.PubMed
90.
go back to reference Chen Y, Cheng M, Tian Z, Hepatitis B. virus down-regulates expressions of MHC class I molecules on hepatoplastoma cell line. Cell Mol Immunol. 2006;3:373–8.PubMed Chen Y, Cheng M, Tian Z, Hepatitis B. virus down-regulates expressions of MHC class I molecules on hepatoplastoma cell line. Cell Mol Immunol. 2006;3:373–8.PubMed
91.
go back to reference Tang KF, Chen M, Xie J, Song GB, Shi YS, Liu Q, et al. Inhibition of hepatitis B virus replication by small interference RNA induces expression of MICA in HepG2.2.15 cells. Med Microbiol Immunol. 2009;198:27–32.PubMed Tang KF, Chen M, Xie J, Song GB, Shi YS, Liu Q, et al. Inhibition of hepatitis B virus replication by small interference RNA induces expression of MICA in HepG2.2.15 cells. Med Microbiol Immunol. 2009;198:27–32.PubMed
92.
go back to reference Wu J, Zhang XJ, Shi KQ, Chen YP, Ren YF, Song YJ, et al. Hepatitis B surface antigen inhibits MICA and MICB expression via induction of cellular miRNAs in hepatocellular carcinoma cells. Carcinogenesis. 2013;35:155–63.PubMed Wu J, Zhang XJ, Shi KQ, Chen YP, Ren YF, Song YJ, et al. Hepatitis B surface antigen inhibits MICA and MICB expression via induction of cellular miRNAs in hepatocellular carcinoma cells. Carcinogenesis. 2013;35:155–63.PubMed
93.
go back to reference Kishikawa T, Otsuka M, Yoshikawa T, Ohno M, Takata A, Shibata C, et al. Regulation of the expression of the liver cancer susceptibility gene MICA by microRNAs. Sci Rep. 2013;3:2739.PubMedCentralPubMed Kishikawa T, Otsuka M, Yoshikawa T, Ohno M, Takata A, Shibata C, et al. Regulation of the expression of the liver cancer susceptibility gene MICA by microRNAs. Sci Rep. 2013;3:2739.PubMedCentralPubMed
94.
go back to reference Kumar V, Yi Lo PH, Sawai H, Kato N, Takahashi A, Deng Z. Soluble MICA and a MICA variation as possible prognostic biomarkers for HBV-induced hepatocellular carcinoma. PLoS One. 2012;7:e44743.PubMedCentralPubMed Kumar V, Yi Lo PH, Sawai H, Kato N, Takahashi A, Deng Z. Soluble MICA and a MICA variation as possible prognostic biomarkers for HBV-induced hepatocellular carcinoma. PLoS One. 2012;7:e44743.PubMedCentralPubMed
95.
go back to reference Tong HV, Toan NL, Song LH, Bock CT, Kremsner PG, Velavan TP. Hepatitis B virus-induced hepatocellular carcinoma: functional roles of MICA variants. J Viral Hepat. 2013;20:687–98.PubMed Tong HV, Toan NL, Song LH, Bock CT, Kremsner PG, Velavan TP. Hepatitis B virus-induced hepatocellular carcinoma: functional roles of MICA variants. J Viral Hepat. 2013;20:687–98.PubMed
96.
go back to reference Li JJ, Pan K, Gu MF, Chen MS, Zhao JJ, Wang H, et al. Prognostic value of soluble MICA levels in the serum of patients with advanced hepatocellular carcinoma. Chin J Cancer. 2013;32:141–8.PubMedCentralPubMed Li JJ, Pan K, Gu MF, Chen MS, Zhao JJ, Wang H, et al. Prognostic value of soluble MICA levels in the serum of patients with advanced hepatocellular carcinoma. Chin J Cancer. 2013;32:141–8.PubMedCentralPubMed
97.
go back to reference Ou DP, Tao YM, Tang FQ, Yang LY. The hepatitis B virus X protein promotes hepatocellular carcinoma metastasis by upregulation of matrix metalloproteinases. Int J Cancer. 2007;120:1208–14.PubMed Ou DP, Tao YM, Tang FQ, Yang LY. The hepatitis B virus X protein promotes hepatocellular carcinoma metastasis by upregulation of matrix metalloproteinases. Int J Cancer. 2007;120:1208–14.PubMed
98.
go back to reference Yu FL, Liu HJ, Lee JW, Liao MH, Shih WL. Hepatitis B virus X protein promotes cell migration by inducing matrix metalloproteinase-3. J Hepatol. 2005;42:520–7.PubMed Yu FL, Liu HJ, Lee JW, Liao MH, Shih WL. Hepatitis B virus X protein promotes cell migration by inducing matrix metalloproteinase-3. J Hepatol. 2005;42:520–7.PubMed
99.
go back to reference Lara-Pezzi E, Gomez-Gaviro MV, Galvez BG, Mira E, Iniguez MA, Fresno M, et al. The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression. J Clin Invest. 2002;110:1831–8.PubMedCentralPubMed Lara-Pezzi E, Gomez-Gaviro MV, Galvez BG, Mira E, Iniguez MA, Fresno M, et al. The hepatitis B virus X protein promotes tumor cell invasion by inducing membrane-type matrix metalloproteinase-1 and cyclooxygenase-2 expression. J Clin Invest. 2002;110:1831–8.PubMedCentralPubMed
100.
go back to reference Kim JR, Kim CH. Association of a high activity of matrix metalloproteinase-9 to low levels of tissue inhibitors of metalloproteinase-1 and -3 in human hepatitis B-viral hepatoma cells. Int J Biochem Cell Biol. 2004;36:2293–306.PubMed Kim JR, Kim CH. Association of a high activity of matrix metalloproteinase-9 to low levels of tissue inhibitors of metalloproteinase-1 and -3 in human hepatitis B-viral hepatoma cells. Int J Biochem Cell Biol. 2004;36:2293–306.PubMed
101.
go back to reference Chung TW, Lee YC, Kim CH. Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3 K/AKT pathways: involvement of invasive potential. FASEB J. 2004;18:1123–5.PubMed Chung TW, Lee YC, Kim CH. Hepatitis B viral HBx induces matrix metalloproteinase-9 gene expression through activation of ERK and PI-3 K/AKT pathways: involvement of invasive potential. FASEB J. 2004;18:1123–5.PubMed
102.
go back to reference Karacki PS, Gao X, Thio CL, Thomas DL, Goedert JJ, Vlahov D, et al. MICA and recovery from hepatitis C virus and hepatitis B virus infections. Genes Immun. 2004;5:261–6.PubMed Karacki PS, Gao X, Thio CL, Thomas DL, Goedert JJ, Vlahov D, et al. MICA and recovery from hepatitis C virus and hepatitis B virus infections. Genes Immun. 2004;5:261–6.PubMed
103.
go back to reference Chen K, Shi W, Xin Z, Wang H, Zhu X, Wu X, et al. Replication of genome wide association studies on hepatocellular carcinoma susceptibility Loci in a chinese population. PLoS One. 2013;8:e77315.PubMedCentralPubMed Chen K, Shi W, Xin Z, Wang H, Zhu X, Wu X, et al. Replication of genome wide association studies on hepatocellular carcinoma susceptibility Loci in a chinese population. PLoS One. 2013;8:e77315.PubMedCentralPubMed
104.
go back to reference Al-Qahtani AA, Al-Anazi M, Abdo AA, Sanai FM, Al-Hamoudi W, Alswat KA, et al. Genetic variation at -1878 (rs2596542) in MICA gene region is associated with chronic hepatitis B virus infection in Saudi Arabian patients. Exp Mol Pathol. 2013;95:255–8.PubMed Al-Qahtani AA, Al-Anazi M, Abdo AA, Sanai FM, Al-Hamoudi W, Alswat KA, et al. Genetic variation at -1878 (rs2596542) in MICA gene region is associated with chronic hepatitis B virus infection in Saudi Arabian patients. Exp Mol Pathol. 2013;95:255–8.PubMed
105.
go back to reference Guan YS, He Q. Role of antiviral therapy in the management of hepatocellular carcinoma. Anticancer Drugs. 2013;24:337–43.PubMed Guan YS, He Q. Role of antiviral therapy in the management of hepatocellular carcinoma. Anticancer Drugs. 2013;24:337–43.PubMed
106.
go back to reference Fletcher SP. Delaney WEt. New therapeutic targets and drugs for the treatment of chronic hepatitis B. Semin Liver Dis. 2013;33:130–7.PubMed Fletcher SP. Delaney WEt. New therapeutic targets and drugs for the treatment of chronic hepatitis B. Semin Liver Dis. 2013;33:130–7.PubMed
107.
go back to reference Kurokawa M, Hiramatsu N, Oze T, Yakushijin T, Miyazaki M, Hosui A, et al. Long-term effect of lamivudine treatment on the incidence of hepatocellular carcinoma in patients with hepatitis B virus infection. J Gastroenterol. 2012;47:577–85.PubMed Kurokawa M, Hiramatsu N, Oze T, Yakushijin T, Miyazaki M, Hosui A, et al. Long-term effect of lamivudine treatment on the incidence of hepatocellular carcinoma in patients with hepatitis B virus infection. J Gastroenterol. 2012;47:577–85.PubMed
108.
go back to reference Manns MP, von Hahn T. Novel therapies for hepatitis C—one pill fits all? Nat Rev Drug Discov. 2013;12:595–610.PubMed Manns MP, von Hahn T. Novel therapies for hepatitis C—one pill fits all? Nat Rev Drug Discov. 2013;12:595–610.PubMed
109.
go back to reference Ogawa E, Furusyo N, Kajiwara E, Takahashi K, Nomura H, Maruyama T, et al. Efficacy of pegylated interferon alpha-2b and ribavirin treatment on the risk of hepatocellular carcinoma in patients with chronic hepatitis C: a prospective, multicenter study. J Hepatol. 2013;58:495–501.PubMed Ogawa E, Furusyo N, Kajiwara E, Takahashi K, Nomura H, Maruyama T, et al. Efficacy of pegylated interferon alpha-2b and ribavirin treatment on the risk of hepatocellular carcinoma in patients with chronic hepatitis C: a prospective, multicenter study. J Hepatol. 2013;58:495–501.PubMed
110.
go back to reference Chotiyaputta W, Lok AS. Hepatitis B virus variants. Nat Rev Gastroenterol Hepatol. 2009;6:453–62.PubMed Chotiyaputta W, Lok AS. Hepatitis B virus variants. Nat Rev Gastroenterol Hepatol. 2009;6:453–62.PubMed
111.
go back to reference Abu-Amara M, Feld JJ. Does antiviral therapy for chronic hepatitis B reduce the risk of hepatocellular carcinoma? Semin Liver Dis. 2013;33:157–66.PubMed Abu-Amara M, Feld JJ. Does antiviral therapy for chronic hepatitis B reduce the risk of hepatocellular carcinoma? Semin Liver Dis. 2013;33:157–66.PubMed
112.
go back to reference Papatheodoridis GV, Manolakopoulos S, Touloumi G, Vourli G, Raptopoulou-Gigi M, Vafiadis-Zoumbouli I, et al. Virological suppression does not prevent the development of hepatocellular carcinoma in HBeAg-negative chronic hepatitis B patients with cirrhosis receiving oral antiviral(s) starting with lamivudine monotherapy: results of the nationwide HEPNET. Greece cohort study. Gut. 2011;60:1109–16.PubMed Papatheodoridis GV, Manolakopoulos S, Touloumi G, Vourli G, Raptopoulou-Gigi M, Vafiadis-Zoumbouli I, et al. Virological suppression does not prevent the development of hepatocellular carcinoma in HBeAg-negative chronic hepatitis B patients with cirrhosis receiving oral antiviral(s) starting with lamivudine monotherapy: results of the nationwide HEPNET. Greece cohort study. Gut. 2011;60:1109–16.PubMed
113.
go back to reference Salvatierra K, Fareleski S, Forcada A, Lopez-Labrador FX. Hepatitis C virus resistance to new specifically-targeted antiviral therapy: a public health perspective. World J Virol. 2013;2:6–15.PubMedCentralPubMed Salvatierra K, Fareleski S, Forcada A, Lopez-Labrador FX. Hepatitis C virus resistance to new specifically-targeted antiviral therapy: a public health perspective. World J Virol. 2013;2:6–15.PubMedCentralPubMed
114.
go back to reference Morgan RL, Baack B, Smith BD, Yartel A, Pitasi M, Falck-Ytter Y. Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma: a meta-analysis of observational studies. Ann Intern Med. 2013;158:329–37.PubMed Morgan RL, Baack B, Smith BD, Yartel A, Pitasi M, Falck-Ytter Y. Eradication of hepatitis C virus infection and the development of hepatocellular carcinoma: a meta-analysis of observational studies. Ann Intern Med. 2013;158:329–37.PubMed
115.
go back to reference Miamen AG, Dong H, Roberts LR. Immunotherapeutic approaches to hepatocellular carcinoma treatment. Liver Cancer. 2012;1:226–37.PubMedCentralPubMed Miamen AG, Dong H, Roberts LR. Immunotherapeutic approaches to hepatocellular carcinoma treatment. Liver Cancer. 2012;1:226–37.PubMedCentralPubMed
116.
go back to reference Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunother. Sci. 2013;342:1432–3. Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunother. Sci. 2013;342:1432–3.
117.
go back to reference Lavanchy D. Viral hepatitis: global goals for vaccination. J Clin Virol. 2012;55:296–302.PubMed Lavanchy D. Viral hepatitis: global goals for vaccination. J Clin Virol. 2012;55:296–302.PubMed
119.
go back to reference Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, Benali S, et al. Chronic hepatitis C: future treatment. Clin Pharmacol. 2014;6:1–17.PubMedCentralPubMed Wendt A, Adhoute X, Castellani P, Oules V, Ansaldi C, Benali S, et al. Chronic hepatitis C: future treatment. Clin Pharmacol. 2014;6:1–17.PubMedCentralPubMed
120.
go back to reference Gao Q, Shi Y, Wang X, Zhou J, Qiu S, Fan J. Translational medicine in hepatocellular carcinoma. Front Med. 2012;6:122–33.PubMed Gao Q, Shi Y, Wang X, Zhou J, Qiu S, Fan J. Translational medicine in hepatocellular carcinoma. Front Med. 2012;6:122–33.PubMed
121.
go back to reference Ohira M, Nishida S, Tryphonopoulos P, Tekin A, Selvaggi G, Moon J, et al. Clinical-scale isolation of interleukin-2-stimulated liver natural killer cells for treatment of liver transplantation with hepatocellular carcinoma. Cell Transplant. 2012;21:1397–406.PubMed Ohira M, Nishida S, Tryphonopoulos P, Tekin A, Selvaggi G, Moon J, et al. Clinical-scale isolation of interleukin-2-stimulated liver natural killer cells for treatment of liver transplantation with hepatocellular carcinoma. Cell Transplant. 2012;21:1397–406.PubMed
123.
go back to reference Zhang C, Zhang J, Niu J, Zhou Z, Tian Z. Interleukin-12 improves cytotoxicity of natural killer cells via upregulated expression of NKG2D. Hum Immunol. 2008;69:490–500.PubMed Zhang C, Zhang J, Niu J, Zhou Z, Tian Z. Interleukin-12 improves cytotoxicity of natural killer cells via upregulated expression of NKG2D. Hum Immunol. 2008;69:490–500.PubMed
124.
go back to reference Xia X, Li X, Feng G, Zheng C, Liang H, Zhou G. Intra-arterial interleukin-12 gene delivery combined with chemoembolization: anti-tumor effect in a rabbit hepatocellular carcinoma (HCC) model. Acta Radiol. 2013;54:684–9.PubMed Xia X, Li X, Feng G, Zheng C, Liang H, Zhou G. Intra-arterial interleukin-12 gene delivery combined with chemoembolization: anti-tumor effect in a rabbit hepatocellular carcinoma (HCC) model. Acta Radiol. 2013;54:684–9.PubMed
125.
go back to reference Chang CJ, Chen YH, Huang KW, Cheng HW, Chan SF, Tai KF, et al. Combined GM-CSF and IL-12 gene therapy synergistically suppresses the growth of orthotopic liver tumors. Hepatology. 2007;45:746–54.PubMed Chang CJ, Chen YH, Huang KW, Cheng HW, Chan SF, Tai KF, et al. Combined GM-CSF and IL-12 gene therapy synergistically suppresses the growth of orthotopic liver tumors. Hepatology. 2007;45:746–54.PubMed
126.
go back to reference Ullrich E, Koch J, Cerwenka A, Steinle A. New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology. 2013;2:e26097.PubMedCentralPubMed Ullrich E, Koch J, Cerwenka A, Steinle A. New prospects on the NKG2D/NKG2DL system for oncology. Oncoimmunology. 2013;2:e26097.PubMedCentralPubMed
127.
go back to reference Armeanu S, Bitzer M, Lauer UM, Venturelli S, Pathil A, Krusch M, et al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res. 2005;65:6321–9.PubMed Armeanu S, Bitzer M, Lauer UM, Venturelli S, Pathil A, Krusch M, et al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res. 2005;65:6321–9.PubMed
128.
go back to reference Worns MA. Systemic therapy and synergies by combination. Dig Dis. 2013;31:104–11.PubMed Worns MA. Systemic therapy and synergies by combination. Dig Dis. 2013;31:104–11.PubMed
129.
go back to reference Armeanu S, Krusch M, Baltz KM, Weiss TS, Smirnow I, Steinle A, et al. Direct and natural killer cell-mediated antitumor effects of low-dose bortezomib in hepatocellular carcinoma. Clin Cancer Res. 2008;14:3520–8.PubMed Armeanu S, Krusch M, Baltz KM, Weiss TS, Smirnow I, Steinle A, et al. Direct and natural killer cell-mediated antitumor effects of low-dose bortezomib in hepatocellular carcinoma. Clin Cancer Res. 2008;14:3520–8.PubMed
130.
go back to reference Kim GP, Mahoney MR, Szydlo D, Mok TS, Marshke R, Holen K, et al. An international, multicenter phase II trial of bortezomib in patients with hepatocellular carcinoma. Invest New Drugs. 2012;30:387–94.PubMedCentralPubMed Kim GP, Mahoney MR, Szydlo D, Mok TS, Marshke R, Holen K, et al. An international, multicenter phase II trial of bortezomib in patients with hepatocellular carcinoma. Invest New Drugs. 2012;30:387–94.PubMedCentralPubMed
131.
go back to reference Van Belle TL, von Herrath MG. The role of the activating receptor NKG2D in autoimmunity. Mol Immunol. 2009;47:8–11.PubMed Van Belle TL, von Herrath MG. The role of the activating receptor NKG2D in autoimmunity. Mol Immunol. 2009;47:8–11.PubMed
132.
go back to reference Chen Y, Wei H, Sun R, Dong Z, Zhang J, Tian Z. Increased susceptibility to liver injury in hepatitis B virus transgenic mice involves NKG2D-ligand interaction and natural killer cells. Hepatology. 2007;46:706–15.PubMed Chen Y, Wei H, Sun R, Dong Z, Zhang J, Tian Z. Increased susceptibility to liver injury in hepatitis B virus transgenic mice involves NKG2D-ligand interaction and natural killer cells. Hepatology. 2007;46:706–15.PubMed
133.
go back to reference Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol. 2005;5:215–29.PubMed Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol. 2005;5:215–29.PubMed
134.
go back to reference Zhang Z, Zhang S, Zou Z, Shi J, Zhao J, Fan R, et al. Hypercytolytic activity of hepatic natural killer cells correlates with liver injury in chronic hepatitis B patients. Hepatology. 2011;53:73–85.PubMedCentralPubMed Zhang Z, Zhang S, Zou Z, Shi J, Zhao J, Fan R, et al. Hypercytolytic activity of hepatic natural killer cells correlates with liver injury in chronic hepatitis B patients. Hepatology. 2011;53:73–85.PubMedCentralPubMed
135.
go back to reference Dunn C, Brunetto M, Reynolds G, Christophides T, Kennedy PT, Lampertico P, et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J Exp Med. 2007;204:667–80.PubMedCentralPubMed Dunn C, Brunetto M, Reynolds G, Christophides T, Kennedy PT, Lampertico P, et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J Exp Med. 2007;204:667–80.PubMedCentralPubMed
136.
go back to reference Ahlenstiel G, Titerence RH, Koh C, Edlich B, Feld JJ, Rotman Y, et al. Natural killer cells are polarized toward cytotoxicity in chronic hepatitis C in an interferon-alfa-dependent manner. Gastroenterology. 2010;138(325–35):e1–2.PubMed Ahlenstiel G, Titerence RH, Koh C, Edlich B, Feld JJ, Rotman Y, et al. Natural killer cells are polarized toward cytotoxicity in chronic hepatitis C in an interferon-alfa-dependent manner. Gastroenterology. 2010;138(325–35):e1–2.PubMed
137.
go back to reference Okamoto Y, Shinjo K, Shimizu Y, Sano T, Yamao K, Gao W, et al. Hepatitis virus infection affects DNA methylation in mice with humanized livers. Gastroenterology. 2014;146:562–72.PubMed Okamoto Y, Shinjo K, Shimizu Y, Sano T, Yamao K, Gao W, et al. Hepatitis virus infection affects DNA methylation in mice with humanized livers. Gastroenterology. 2014;146:562–72.PubMed
138.
go back to reference Zou Y, Chen T, Han M, Wang H, Yan W, Song G, et al. Increased killing of liver NK cells by Fas/Fas ligand and NKG2D/NKG2D ligand contributes to hepatocyte necrosis in virus-induced liver failure. J Immunol. 2010;184:466–75.PubMed Zou Y, Chen T, Han M, Wang H, Yan W, Song G, et al. Increased killing of liver NK cells by Fas/Fas ligand and NKG2D/NKG2D ligand contributes to hepatocyte necrosis in virus-induced liver failure. J Immunol. 2010;184:466–75.PubMed
139.
go back to reference Kahraman A, Schlattjan M, Kocabayoglu P, Yildiz-Meziletoglu S, Schlensak M, Fingas CD, et al. Major histocompatibility complex class I-related chains A and B (MIC A/B): a novel role in nonalcoholic steatohepatitis. Hepatology. 2010;51:92–102.PubMed Kahraman A, Schlattjan M, Kocabayoglu P, Yildiz-Meziletoglu S, Schlensak M, Fingas CD, et al. Major histocompatibility complex class I-related chains A and B (MIC A/B): a novel role in nonalcoholic steatohepatitis. Hepatology. 2010;51:92–102.PubMed
140.
go back to reference Rosmorduc O, Fartoux L. HCC and NASH: how strong is the clinical demonstration? Clin Res Hepatol Gastroenterol. 2012;36:202–8.PubMed Rosmorduc O, Fartoux L. HCC and NASH: how strong is the clinical demonstration? Clin Res Hepatol Gastroenterol. 2012;36:202–8.PubMed
141.
go back to reference Cox ST, Madrigal JA, Saudemont A. Diversity and characterization of polymorphic 5′ promoter haplotypes of MICA and MICB genes. Tissue Antigens. 2014. doi:10.1111/tan.12400. Cox ST, Madrigal JA, Saudemont A. Diversity and characterization of polymorphic 5′ promoter haplotypes of MICA and MICB genes. Tissue Antigens. 2014. doi:10.​1111/​tan.​12400.
142.
go back to reference Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31:413–41.PubMedCentralPubMed Raulet DH, Gasser S, Gowen BG, Deng W, Jung H. Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol. 2013;31:413–41.PubMedCentralPubMed
144.
go back to reference Hoshida Y, Fuchs BC, Tanabe KK. Genomic risk of hepatitis C-related hepatocellular carcinoma. J Hepatol. 2012;56:729–30.PubMed Hoshida Y, Fuchs BC, Tanabe KK. Genomic risk of hepatitis C-related hepatocellular carcinoma. J Hepatol. 2012;56:729–30.PubMed
145.
go back to reference Della Corte C, Aghemo A, Colombo M. Individualized hepatocellular carcinoma risk: the challenges for designing successful chemoprevention strategies. World J Gastroenterol. 2013;19:1359–71.PubMedCentralPubMed Della Corte C, Aghemo A, Colombo M. Individualized hepatocellular carcinoma risk: the challenges for designing successful chemoprevention strategies. World J Gastroenterol. 2013;19:1359–71.PubMedCentralPubMed
146.
go back to reference Delaney WEt. Molecular virology of chronic hepatitis B and C: parallels, contrasts and impact on drug development and treatment outcome. Antiviral Res. 2013;99:34–48.PubMed Delaney WEt. Molecular virology of chronic hepatitis B and C: parallels, contrasts and impact on drug development and treatment outcome. Antiviral Res. 2013;99:34–48.PubMed
147.
go back to reference Liver EAftSot. EASL clinical practice guidelines: management of hepatitis C virus infection. J Hepatol. 2014;60:392–420. Liver EAftSot. EASL clinical practice guidelines: management of hepatitis C virus infection. J Hepatol. 2014;60:392–420.
148.
Metadata
Title
MICA SNPs and the NKG2D system in virus-induced HCC
Authors
Kaku Goto
Naoya Kato
Publication date
01-03-2015
Publisher
Springer Japan
Published in
Journal of Gastroenterology / Issue 3/2015
Print ISSN: 0944-1174
Electronic ISSN: 1435-5922
DOI
https://doi.org/10.1007/s00535-014-1000-9

Other articles of this Issue 3/2015

Journal of Gastroenterology 3/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.