Hepatitis virus infection affects DNA methylation in mice with humanized livers

Gastroenterology

Volumn 146, Issue 2, 2014, Pages 562-572

  Okamoto, Yasuyuki ^a,b   Shinjo, Keiko ^a   Shimizu, Yasuhiro ^a   Sano, Tsuyoshi ^a   Yamao, Kenji ^a   Gao, Wentao ^c   Fujii, Makiko ^a   Osada, Hirotaka ^a   Sekido, Yoshitaka ^a   Murakami, Shuko ^b   Tanaka, Yasuhito ^b   Joh, Takashi ^b   Sato, Shinya ^b   Takahashi, Satoru ^b   Wakita, Takaji ^d   Zhu, Jingde ^e   Issa, Jean Pierre J ^f   Kondo, Yutaka ^a,g  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^c NANJING MEDICAL UNIVERSITY   (China)

^d NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^e SHANGHAI JIAO TONG UNIVERSITY   (China)

^f TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Epigenetic; Gene Regulation; Inflammatory Response; Liver Cancer

Indexed keywords

CYCLINE; ESTROGEN RECEPTOR ALPHA; GAMMA INTERFERON; GANGLIOTETRAOSYLCERAMIDE; GANGLIOTETRAOSYLCERAMIDE ANTIBODY; KI 67 ANTIGEN; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UROKINASE; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ELOVL FATTY ACID ELONGASE 3 GENE; ESTROGEN RECEPTOR ALPHA GENE; GAMMA INTERFERON GENE; HEPATITIS B; HEPATITIS C; HEPATOMA CELL; INNATE IMMUNITY; KUPFFER CELL; LINE1 GENE; LIVER CELL; LIVER CELL CARCINOMA; LIVER REGENERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PYROSEQUENCING; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A GENE; SCID MOUSE; TRANSCRIPTION FACTOR HOXA6 GENE; TRANSGENE; UROKINASE GENE; VIRUS CELL INTERACTION; ZINC FINGER PROTEIN 385A GENE;

EPIGENETIC; ESR1; ESTROGEN RECEPTOR 1; GENE REGULATION; HBV; HBX; HCC; HCV; HEPATITIS B VIRUS; HEPATITIS B VIRUS X; HEPATITIS C VIRUS; HEPATOCELLULAR CARCINOMA; HOMEOBOX A6; HOXA6; IFN; INFLAMMATORY RESPONSE; INTERFERON; LIVER CANCER; MCAM; METHYLATED CPG ISLAND AMPLIFICATION MICROARRAY; NATURAL KILLER; NK; PCNA; PROLIFERATING CELL NUCLEAR ANTIGEN; RAS ASSOCIATION DOMAIN FAMILY 1 ISOFORM A; RASSF1A; REACTIVE OXYGEN SPECIES; ROS; SCID; SEVERE COMBINED IMMUNODEFICIENT;

ADOLESCENT; ADULT; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CHILD; CHILD, PRESCHOOL; CHIMERISM; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HEPATITIS B; HEPATITIS C; HUMANS; IMMUNITY, INNATE; KILLER CELLS, NATURAL; LIVER; LIVER NEOPLASMS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, SCID; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA; YOUNG ADULT;

EID: 84892759791     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2013.10.056     Document Type: Article

References (39)

1. S.S. Thorgeirsson, and J.W. Grisham Molecular pathogenesis of human hepatocellular carcinoma Nat Genet 31 2002 339 346
2. S.B. Baylin, J.G. Herman, and J.R. Graff et al. Alterations in DNA methylation: a fundamental aspect of neoplasia Adv Cancer Res 72 1998 141 196
3. P.A. Jones, and S.B. Baylin The fundamental role of epigenetic events in cancer Nat Rev Genet 3 2002 415 428
4. Y. Kondo, Y. Kanai, and M. Sakamoto et al. Genetic instability and aberrant DNA methylation in chronic hepatitis and cirrhosis - a comprehensive study of loss of heterozygosity and microsatellite instability at 39 loci and DNA hypermethylation on 8 CpG islands in microdissected specimens from patients with hepatocellular carcinoma Hepatology 32 2000 970 999
5. J. Yu, M. Ni, and J. Xu et al. Methylation profiling of twenty promoter-CpG islands of genes which may contribute to hepatocellular carcinogenesis BMC Cancer 2 2002 29
6. S. Lee, H.J. Lee, and J.H. Kim et al. Aberrant CpG island hypermethylation along multistep hepatocarcinogenesis Am J Pathol 163 2003 1371 1378
7. U. Schagdarsurengin, L. Wilkens, and D. Steinemann et al. Frequent epigenetic inactivation of the RASSF1A gene in hepatocellular carcinoma Oncogene 22 2003 1866 1871
8. W. Gao, Y. Kondo, and L. Shen et al. Variable DNA methylation patterns associated with progression of disease in hepatocellular carcinomas Carcinogenesis 29 2008 1901 1910
9. I.Y. Park, B.H. Sohn, and E. Yu et al. Aberrant epigenetic modifications in hepatocarcinogenesis induced by hepatitis B virus X protein Gastroenterology 132 2007 1476 1494
10. J.K. Jung, P. Arora, and J.S. Pagano et al. Expression of DNA methyltransferase 1 is activated by hepatitis B virus X protein via a regulatory circuit involving the p16INK4a-cyclin D1-CDK 4/6-pRb-E2F1 pathway Cancer Res 67 2007 5771 5778
11. D.L. Zheng, L. Zhang, and N. Cheng et al. Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A J Hepatol 50 2009 377 587
12. M.R. Higgs, H. Lerat, and J.M. Pawlotsky Downregulation of Gadd45beta expression by hepatitis C virus leads to defective cell cycle arrest Cancer Res 70 2010 4901 4911
13. D.F. Mercer, D.E. Schiller, and J.F. Elliott et al. Hepatitis C virus replication in mice with chimeric human livers Nat Med 7 2001 927 933
14. H. Barth, E. Robinet, and T.J. Liang et al. Mouse models for the study of HCV infection and virus-host interactions J Hepatol 49 2008 134 142
15. P. Meuleman, L. Libbrecht, and R. De Vos et al. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera Hepatology 41 2005 847 856
16. M. Sugiyama, Y. Tanaka, and F. Kurbanov et al. Direct cytopathic effects of particular hepatitis B virus genotypes in severe combined immunodeficiency transgenic with urokinase-type plasminogen activator mouse with human hepatocytes Gastroenterology 136 2009 652 662 e3
17. T. Wakita, T. Pietschmann, and T. Kato et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat Med 11 2005 791 796
18. N. Choudhry, F. Petry, and N. van Rooijen et al. A protective role for interleukin 18 in interferon gamma-mediated innate immunity to Cryptosporidium parvum that is independent of natural killer cells J Infect Dis 206 2012 117 124
19. N. Nishida, T. Nagasaka, and T. Nishimura et al. Aberrant methylation of multiple tumor suppressor genes in aging liver, chronic hepatitis, and hepatocellular carcinoma Hepatology 47 2008 908 918
20. J. Zhong, P. Gastaminza, and G. Cheng et al. Robust hepatitis C virus infection in vitro Proc Natl Acad Sci U S A 102 2005 9294 9299
21. A.S. Yang, M.R. Estecio, and K. Doshi et al. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements Nucleic Acids Res 32 2004 e38
22. M. Toyota, C. Ho, and N. Ahuja et al. Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification Cancer Res 59 1999 2307 2312
23. J.P. Issa Epigenetic variation and cellular Darwinism Nat Genet 43 2011 724 726
24. B. Rehermann, and M. Nascimbeni Immunology of hepatitis B virus and hepatitis C virus infection Nat Rev Immunol 5 2005 215 229
25. N. Krohn, S. Kapoor, and Y. Enami et al. Hepatocyte transplantation- induced liver inflammation is driven by cytokines-chemokines associated with neutrophils and Kupffer cells Gastroenterology 136 2009 1806 1817
26. M. Kasai, T. Yoneda, and S. Habu et al. In vivo effect of anti-asialo GM1 antibody on natural killer activity Nature 291 1981 334 335
27. Y. Watanabe, O. Suzuki, and T. Haruyama et al. Interferon-gamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis J Cell Biochem 89 2003 244 253
28. M.D. Wheeler Endotoxin and Kupffer cell activation in alcoholic liver disease Alcohol Res Health 27 2003 300 306
29. C. Berasain, J. Castillo, and M.J. Perugorria et al. Inflammation and liver cancer: new molecular links Ann N Y Acad Sci 1155 2009 206 221
30. M.J. Bouchard, and S. Navas-Martin Hepatitis B and C virus hepatocarcinogenesis: lessons learned and future challenges Cancer Lett 305 2011 123 143
31. C.J. Horras, C.L. Lamb, and K.A. Mitchell Regulation of hepatocyte fate by interferon-gamma Cytokine Growth Factor Rev 22 2011 35 43
32. A. Wullaert, G. van Loo, and K. Heyninck et al. Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond Endocr Rev 28 2007 365 386
33. E. Vivier, E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini Functions of natural killer cells Nat Immunol 9 2008 503 510
34. T. Niwa, T. Tsukamoto, and T. Toyoda et al. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells Cancer Res 70 2010 1430 1440
35. K. Hur, T. Niwa, and T. Toyoda et al. Insufficient role of cell proliferation in aberrant DNA methylation induction and involvement of specific types of inflammation Carcinogenesis 32 2012 35 41
36. M. Katsurano, T. Niwa, and Y. Yasui et al. Early-stage formation of an epigenetic field defect in a mouse colitis model, and non-essential roles of T- and B-cells in DNA methylation induction Oncogene 31 2012 342 351
37. H.M. O'Hagan, W. Wang, and S. Sen et al. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands Cancer Cell 20 2011 606 619
38. S.O. Lim, J.M. Gu, and M.S. Kim et al. Epigenetic changes induced by reactive oxygen species in hepatocellular carcinoma: methylation of the E-cadherin promoter Gastroenterology 135 2008 2128 2140 2140 e1-8
39. K.D. Hansen, W. Timp, and H.C. Bravo et al. Increased methylation variation in epigenetic domains across cancer types Nat Genet 43 2011 768 775