Chronic hepatitis B virus and hepatitis C virus infections and cancer: Synergy between viral and host factors

Clinical Microbiology and Infection

Volumn 21, Issue 11, 2015, Pages 969-974

  Schinzari, V ^a   Barnaba, V ^a,b   Piconese, S ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b Pasteur Institute   (Italy)

Author keywords

Chronic inflammation; Hepatitis B virus; Hepatitis C virus; Hepatocellular carcinoma; Tumours

Indexed keywords

HOST FACTOR; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 23; INTERLEUKIN 6; LYMPHOTOXIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; UNTRANSLATED RNA;

CHROMOSOMAL INSTABILITY; CHRONIC HEPATITIS B; CHRONIC HEPATITIS C; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN; INTESTINE FLORA; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; VIRUS GENOME; VIRUS INTERFERENCE; CARCINOMA, HEPATOCELLULAR; COMPLICATION; HEPACIVIRUS; HEPATITIS B; HOST PATHOGEN INTERACTION; LIVER NEOPLASMS; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY;

CARCINOMA, HEPATOCELLULAR; HEPACIVIRUS; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; HOST-PATHOGEN INTERACTIONS; HUMANS; LIVER NEOPLASMS;

EID: 84945456479     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2015.06.026     Document Type: Review

References (73)

1. El-Serag H.B. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 2012, 142:1264-1273. e1261.
2. Levrero M., Pollicino T., Petersen J., Belloni L., Raimondo G., Dandri M. Control of cccDNA function in hepatitis B virus infection. J Hepatol 2009, 51:581-592.
3. Abu-Amara M., Feld J.J. Does antiviral therapy for chronic hepatitis B reduce the risk of hepatocellular carcinoma?. Semin Liver Dis 2013, 33:157-166.
4. Lau C.C., Sun T., Ching A.K., He M., Li J.W., Wong A.M., et al. Viral-human chimeric transcript predisposes risk to liver cancer development and progression. Cancer Cell 2014, 25:335-349.
5. Li X., Zhang J., Yang Z., Kang J., Jiang S., Zhang T., et al. The function of targeted host genes determines the oncogenicity of HBV integration in hepatocellular carcinoma. J Hepatol 2014, 60:975-984.
6. Sung W.K., Zheng H., Li S., Chen R., Liu X., Li Y., et al. Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 2012, 44:765-769.
7. Chen C.J., Yang H.I., Su J., Jen C.L., You S.L., Lu S.N., et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 2006, 295:65-73.
8. Di Bisceglie A.M. Hepatitis B and hepatocellular carcinoma. Hepatology 2009, 49:S56-S60.
9. Yang H.I., Yuen M.F., Chan H.L., Han K.H., Chen P.J., Kim D.Y., et al. Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol 2011, 12:568-574.
10. Pollicino T., Saitta C. Occult hepatitis B virus and hepatocellular carcinoma. World J Gastroenterol 2014, 20:5951-5961.
11. Raimondo G., Allain J.P., Brunetto M.R., Buendia M.A., Chen D.S., Colombo M., et al. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 2008, 49:652-657.
12. Raimondo G., Caccamo G., Filomia R., Pollicino T. Occult HBV infection. Semin Immunopathol 2013, 35:39-52.
13. Squadrito G., Cacciola I., Alibrandi A., Pollicino T., Raimondo G. Impact of occult hepatitis B virus infection on the outcome of chronic hepatitis C. J Hepatol 2013, 59:696-700.
14. Torbenson M., Thomas D.L. Occult hepatitis B. Lancet Infect Dis 2002, 2:479-486.
15. Wu S.C., Chang S.C., Wu H.Y., Liao P.J., Chang M.F. Hepatitis C virus NS5a protein down-regulates the expression of spindle gene ASPM through PKR-p38 signaling pathway. J Biol Chem 2008, 283:29396-29404.
16. Chen C.J., Yang H.I., Iloeje U.H. Hepatitis B virus DNA levels and outcomes in chronic hepatitis B. Hepatology 2009, 49:S72-S84.
17. Ni Y.H., Chang M.H., Wang K.J., Hsu H.Y., Chen H.L., Kao J.H., et al. Clinical relevance of hepatitis B virus genotype in children with chronic infection and hepatocellular carcinoma. Gastroenterology 2004, 127:1733-1738.
18. Fang Z.L., Sabin C.A., Dong B.Q., Ge L.Y., Wei S.C., Chen Q.Y., et al. HBV A1762T, G1764A mutations are a valuable biomarker for identifying a subset of male HBsAg carriers at extremely high risk of hepatocellular carcinoma: a prospective study. Am J Gastroenterol 2008, 103:2254-2262.
19. Yang H.I., Yeh S.H., Chen P.J., Iloeje U.H., Jen C.L., Su J., et al. Associations between hepatitis B virus genotype and mutants and the risk of hepatocellular carcinoma. J Natl Cancer Inst 2008, 100:1134-1143.
20. Chen B.F., Liu C.J., Jow G.M., Chen P.J., Kao J.H., Chen D.S. High prevalence and mapping of pre-S deletion in hepatitis B virus carriers with progressive liver diseases. Gastroenterology 2006, 130:1153-1168.
21. Arzumanyan A., Reis H.M., Feitelson M.A. Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma. Nat Rev Cancer 2013, 13:123-135.
22. Kao C.F., Chen S.Y., Chen J.Y., Wu Lee Y.H. Modulation of p53 transcription regulatory activity and post-translational modification by hepatitis C virus core protein. Oncogene 2004, 23:2472-2483.
23. Wang X.W., Forrester K., Yeh H., Feitelson M.A., Gu J.R., Harris C.C. Hepatitis B virus X protein inhibits p53 sequence-specific DNA binding, transcriptional activity, and association with transcription factor ercc3. Proc Natl Acad Sci USA 1994, 91:2230-2234.
24. Merquiol E., Uzi D., Mueller T., Goldenberg D., Nahmias Y., Xavier R.J., et al. HCV causes chronic endoplasmic reticulum stress leading to adaptation and interference with the unfolded protein response. PloS One 2011, 6:e24660.
25. Yang B., Bouchard M.J. The hepatitis B virus Xprotein elevates cytosolic calcium signals by modulating mitochondrial calcium uptake. J Virol 2012, 86:313-327.
26. Ke P.Y., Chen S.S. Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J Clin Invest 2011, 121:37-56.
27. Li J., Liu Y., Wang Z., Liu K., Wang Y., Liu J., et al. Subversion of cellular autophagy machinery by hepatitis B virus for viral envelopment. J Virol 2011, 85:6319-6333.
28. Abe M., Koga H., Yoshida T., Masuda H., Iwamoto H., Sakata M., et al. Hepatitis C virus core protein upregulates the expression of vascular endothelial growth factor via the nuclear factor-κB/hypoxia-inducible factor-1α axis under hypoxic conditions. Hepatol Res 2012, 42:591-600.
29. Moon E.J., Jeong C.H., Jeong J.W., Kim K.R., Yu D.Y., Murakami S., et al. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1α. FASEB J 2004, 18:382-384.
30. Vrancken K., Paeshuyse J., Liekens S. Angiogenic activity of hepatitis B and C viruses. Antivir Chem Chemother 2012, 22:159-170.
31. Zhai B., Sun X.Y. Mechanisms of resistance to sorafenib and the corresponding strategies in hepatocellular carcinoma. World J Hepatol 2013, 5:345-352.
32. Akkari L., Gregoire D., Floc'h N., Moreau M., Hernandez C., Simonin Y., et al. Hepatitis C viral protein NS5a induces EMT and participates in oncogenic transformation of primary hepatocyte precursors. J Hepatol 2012, 57:1021-1028.
33. Arzumanyan A., Friedman T., Kotei E., Ng I.O., Lian Z., Feitelson M.A. Epigenetic repression of e-cadherin expression by hepatitis B virus X antigen in liver cancer. Oncogene 2012, 31:563-572.
34. Lee D.K., Park S.H., Yi Y., Choi S.G., Lee C., Parks W.T., et al. The hepatitis B virus encoded oncoprotein px amplifies TGF-β family signaling through direct interaction with SMAD4: potential mechanism of hepatitis B virus-induced liver fibrosis. Genes Dev 2001, 15:455-466.
35. Villanueva A., Llovet J.M. Liver cancer in 2013: mutational landscape of HCC-the end of the beginning. Nat Rev Clin Oncol 2014, 11:73-74.
36. Street A., Macdonald A., McCormick C., Harris M. Hepatitis C virus NS5a-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular β-catenin and stimulation of β-catenin-responsive transcription. J Virol 2005, 79:5006-5016.
37. Yamashita T., Budhu A., Forgues M., Wang X.W. Activation of hepatic stem cell marker EPCAM by WNT-β-catenin signaling in hepatocellular carcinoma. Cancer Res 2007, 67:10831-10839.
38. Kaidi A., Williams A.C., Paraskeva C. Interaction between β-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol 2007, 9:210-217.
39. Tong C.M., Ma S., Guan X.Y. Biology of hepatic cancer stem cells. J Gastroenterol Hepatol 2011, 26:1229-1237.
40. Benegiamo G., Vinciguerra M., Mazzoccoli G., Piepoli A., Andriulli A., Pazienza V. DNA methyltransferases 1 and 3b expression in HUH-7 cells expressing HCV core protein of different genotypes. Dig Dis Sci 2012, 57:1598-1603.
41. Huang J., Wang Y., Guo Y., Sun S. Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 2010, 52:60-70.
42. Rongrui L., Na H., Zongfang L., Fanpu J., Shiwen J. Epigenetic mechanism involved in the HBV/HCV-related hepatocellular carcinoma tumorigenesis. Curr Pharmaceut Des. 2014, 20:1715-1725.
43. Fan H.X., Tang H. Complex interactions between microRNAs and hepatitis B/C viruses. World J Gastroenterol 2014, 20:13477-13492.
44. He Y., Meng X.M., Huang C., Wu B.M., Zhang L., Lv X.W., et al. Long noncoding RNAs: novel insights into hepatocelluar carcinoma. Cancer Lett 2014, 344:20-27.
45. Bandiera S., Pfeffer S., Baumert T.F., Zeisel M.B. Mir-122-a key factor and therapeutic target in liver disease. J Hepatol 2015, 62:448-457.
46. Luna J.M., Scheel T.K., Danino T., Shaw K.S., Mele A., Fak J.J., et al. Hepatitis C virus RNA functionally sequesters MIR-122. Cell 2015, 160:1099-1110.
47. Li C., Wang Y., Wang S., Wu B., Hao J., Fan H., et al. Hepatitis B virus mRNA-mediated mir-122 inhibition upregulates PTTG1-binding protein, which promotes hepatocellular carcinoma tumor growth and cell invasion. J Virol 2013, 87:2193-2205.
48. Wu C.Y., Lin J.T., Ho H.J., Su C.W., Lee T.Y., Wang S.Y., et al. Association of nucleos(t)ide analogue therapy with reduced risk of hepatocellular carcinoma in patients with chronic hepatitis B: a nationwide cohort study. Gastroenterology 2014, 147:143-151. e145.
49. FitzSimons D., Hendrickx G., Vorsters A., Van Damme P. Hepatitis B vaccination: a completed schedule enough to control HBV lifelong? Milan, Italy, 17-18 November 2011. Vaccine 2013, 31:584-590.
50. Luongo M., Critelli R., Grottola A., Gitto S., Bernabucci V., Bevini M., et al. Acute hepatitis B caused by a vaccine-escape HBV strain in vaccinated subject: sequence analysis and therapeutic strategy. J Clin Virol 2015, 62:89-91.
51. Barnaba V. Hepatitis C virus infection: a "liaison a trois" amongst the virus, the host, and chronic low-level inflammation for human survival. J Hepatol 2010, 53:752-761.
52. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
53. Guidotti L.G., Chisari F.V. Immunobiology and pathogenesis of viral hepatitis. Annu Rev Pathol 2006, 1:23-61.
54. Rehermann B., Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol 2005, 5:215-229.
55. McGivern D.R., Lemon S.M. Virus-specific mechanisms of carcinogenesis in hepatitis C virus associated liver cancer. Oncogene 2011, 30:1969-1983.
56. Haybaeck J., Zeller N., Wolf M.J., Weber A., Wagner U., Kurrer M.O., et al. A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 2009, 16:295-308.
57. Simonin Y., Vegna S., Akkari L., Grégoire D., Antoine E., Piette J., et al. Lymphotoxin signaling is initiated by the viral polymerase in HCV-linked tumorigenesis. PLoS Pathogens 2013, 9.
58. Dolganiuc A., Oak S., Kodys K., Golenbock D.T., Finberg R.W., Kurt-Jones E., et al. Hepatitis C core and nonstructural 3 proteins trigger toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 2004, 127:1513-1524.
59. Sato Y., Kato J., Takimoto R., Takada K., Kawano Y., Miyanishi K., et al. Hepatitis C virus core protein promotes proliferation of human hepatoma cells through enhancement of transforming growth factor α expression via activation of nuclear factor-κB. Gut 2006, 55:1801-1808.
60. Naugler W.E., Sakurai T., Kim S., Maeda S., Kim K., Elsharkawy A.M., et al. Gender disparity in liver cancer due to sex differences in myd88-dependent IL-6 production. Science 2007, 317:121-124.
61. Wong V.W., Yu J., Cheng A.S., Wong G.L., Chan H.Y., Chu E.S., et al. High serum interleukin-6 level predicts future hepatocellular carcinoma development in patients with chronic hepatitis B. Int J Cancer 2009, 124:2766-2770.
62. Nakagawa H., Maeda S., Yoshida H., Tateishi R., Masuzaki R., Ohki T., et al. Serum IL-6 levels and the risk for hepatocarcinogenesis in chronic hepatitis C patients: an analysis based on gender differences. Int J Cancer 2009, 125:2264-2269.
63. El-Serag H.B., Rudolph K.L. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132:2557-2576.
64. Wu Q., Liu Q. Do hepatitis B virus and hepatitis C virus co-infections increase hepatocellular carcinoma occurrence through synergistically modulating lipogenic gene expression?. Hepatol Res 2012, 42:733-740.
65. Park E.J., Lee J.H., Yu G.Y., He G., Ali S.R., Holzer R.G. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell. 2010, 140:197-208.
66. Chen C.L., Yang H.I., Yang W.S., Liu C.J., Chen P.J., You S.L., et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in taiwan. Gastroenterology 2008, 135:111-121.
67. Wolf M.J., Adili A., Piotrowitz K., Abdullah Z., Boege Y., Stemmer K., et al. Metabolic activation of intrahepatic CD8+ T cells and NKT cells causes nonalcoholic steatohepatitis and liver cancer via cross-talk with hepatocytes. Cancer Cell 2014, 26:549-564.
68. Fox J.G., Feng Y., Theve E.J., Raczynski A.R., Fiala J.L., Doernte A.L., et al. Gut microbes define liver cancer risk in mice exposed to chemical and viral transgenic hepatocarcinogens. Gut 2010, 59:88-97.
69. Yoshimoto S., Loo T.M., Atarashi K., Kanda H., Sato S., Oyadomari S., et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 2013, 499:97-101.
70. Fattovich G., Stroffolini T., Zagni I., Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004, 127:50.
71. Lin M.V., King L.Y., Chung R.T. Hepatitis C virus-associated cancer. Annu Rev Pathol 2015, 10:345-370.
72. Matsuzaki K., Murata M., Yoshida K., Sekimoto G., Uemura Y., Sakaida N., et al. Chronic inflammation associated with hepatitis C virus infection perturbs hepatic transforming growth factor β signaling, promoting cirrhosis and hepatocellular carcinoma. Hepatology 2007, 46:48-57.
73. Piconese S., Timperi E., Pacella I., Schinzari V., Tripodo C., Rossi M., et al. Human OX40 tunes the function of regulatory T cells in tumor and nontumor areas of hepatitis C virus-infected liver tissue. Hepatology 2014, 60:1494-1507.