Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Viral hepatitis and liver cancer: the case of hepatitis C

Oncogene volume 25, pages 3834–3847 (2006)Cite this article

Abstract

Chronic infection with the hepatitis C virus (HCV) is a major risk factor for the development of hepatocellular carcinoma (HCC) worldwide. The pathogenesis of HCC in HCV infection has extensively been analysed. Hepatitis C virus-induced chronic inflammation and the effects of cytokines in the development of fibrosis and liver cell proliferation are considered as one of the major pathogenic mechanisms. Increasing experimental evidence suggests that HCV contributes to HCC by directly modulating pathways that promote the malignant transformation of hepatocytes. Hepatitis C virus is an RNA virus that does not integrate into the host genome but HCV proteins interact with many host-cell factors well beyond their roles in the viral life cycle and are involved in a wide range of activities, including cell signaling, transcription, cell proliferation, apoptosis, membrane rearrangements, vesicular trafficking and translational regulation. At least four of the HCV gene products, namely HCV core, NS3, NS4B and NS5A, have been shown to exhibit transformation potential in tissue culture and several potentially oncogenic pathways have been shown to be altered by the expression of HCV proteins. Both HCV core and NS5A induce the accumulation of wild-type β-catenin and the Wnt–β-catenin pathway emerges as a common target for HCV (and HBV) in human HCCs, also independently from axin/β-catenin gene mutations. Induction of both endoplasmic reticulum stress and oxidative stress by HCV proteins might also contribute to HCV transformation. Most of the putative transforming functions of the HCV proteins have been defined in artificial cellular systems, which may not be applicable to HCV infection in vivo, and still need to be established in relevant infection and disease models.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Aguilar F, Hussain SP, Cerutti P . (1993). Proc Natl Acad Sci USA 90: 8586–8590.

  • Alam SS, Nakamura T, Naganuma A, Nozaki A, Nouso K, Shimomura H et al. (2002). Acta Med Okayama 56: 141–147.

  • Alisi A, Giambartolomei S, Cupelli F, Merlo P, Fontemaggi G, Spaziani A et al. (2003). Oncogene 22: 2573–2580.

  • Aoki H, Hayashi J, Moriyama M, Arakawa Y, Hino O . (2000). J Virol 74: 1736–1741.

  • Arima N, Kao CY, Licht T, Padmanabhan R, Sasaguri Y, Padmanabhan R . (2001). J Biol Chem 276: 12675–12684.

  • Balachandran S, Kim CN, Yeh WC, Mak TW, Bhalla K, Barber GN . (1998). EMBO J 17: 6888–6902.

  • Barba G, Harper F, Harada T, Kohara M, Goulinet S, Matsuura Y et al. (1997). Proc Natl Acad Sci USA 94: 1200–1205.

  • Bataller R, Paik YH, Lindquist JN, Lemasters JJ, Brenner DA . (2004). Gastroenterology 126: 529–540.

  • Blight KJ, Kolykhalov AA, Rice CM . (2000). Science 290: 1972–1974.

  • Blindenbacher A, Duong FH, Hunziker L, Stutvoet ST, Wang X, Terracciano L et al. (2003). Gastroenterology 124: 1465–1475.

  • Bluteau O, Jeannot E, Bioulac-Sage P, Marques JM, Blanc JF, Bui H et al. (2002). Nat Genet 32: 312–315.

  • Boige V, Laurent-Puig P, Fouchet P, Flejou JF, Monges G, Bedossa P et al. (1997). Cancer Res 57: 1986–1990.

  • Borowski P, Heiland M, Feucht H, Laufs R . (1999a). Arch Virol 144: 687–701.

  • Borowski P, Kuhl R, Laufs R, Schulze zur Wiesch J, Heiland M . (1999b). J Clin Virol 13: 61–69.

  • Borowski P, zur Wiesch JS, Resch K, Feucht H, Laufs R, Schmitz H . (1999c). J Biol Chem 274: 30722–30728.

  • Bosch FX, Ribes J, Borras J . (1999). Semin Liver Dis 19: 271–285.

  • Brass V, Bieck E, Montserret R, Wolk B, Hellings JA, Blum HE et al. (2002). J Biol Chem 277: 8130–8139.

  • Brechot C, Jaffredo F, Lagorce D, Gerken G, Meyer zum Buschenfelde K, Papakonstontinou A et al. (1998). J Hepatol 29: 173–183.

  • Bressac B, Kew M, Wands J, Ozturk M . (1991). Nature 350: 429–431.

  • Breuhahn K, Vreden S, Haddad R, Beckebaum S, Stippel D, Flemming P et al. (2004). Cancer Res 64: 6058–6064.

  • Brunt EM, Neuschwander-Tetri BA, Oliver D, Wehmeier KR, Bacon BR . (2004). Hum Pathol 35: 1070–1082.

  • Cacciola I, Pollicino T, Squadrito G, Cerenzia G, Orlando ME, Raimondo G . (1999). N Engl J Med 341: 22–26.

  • Chang SC, Yen JH, Kang HY, Jang MH, Chang MF . (1994). Biochem Biophys Res Commun 205: 1284–1290.

  • Chen CJ, Chen DS . (2002). Hepatology 36: 1046–1049.

  • Chen X, Cheung ST, So S, Fan ST, Barry C, Higgins J et al. (2002). Mol Biol Cell 13: 1929–1939.

  • Cho J, Baek W, Yang S, Chang J, Sung YC, Suh M . (2001). Biochim Biophys Acta 1538: 59–66.

  • Chung KM, Lee J, Kim JE, Song OK, Cho S, Lim J et al. (2000). J Virol 74: 5233–5241.

  • Crotta S, Stilla A, Wack A, D'Andrea A, Nuti S, D'Oro U et al. (2002). J Exp Med 195: 35–41.

  • Davila JA, Morgan RO, Shaib Y, McGlynn KA, El-Serag HB . (2005). Gut 54: 533–539.

  • de La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O et al. (1998). Proc Natl Acad Sci USA 95: 8847–8851.

  • Delpuech O, Trabut JB, Carnot F, Feuillard J, Brechot C, Kremsdorf D . (2002). Oncogene 21: 2926–2937.

  • Deuffic S, Poynard T, Buffat L, Valleron AJ . (1998). Lancet 351: 214–215.

  • Ding Q, Xia W, Liu JC, Yang JY, Lee DF, Xia J et al. (2005). Mol Cell 19: 159–170.

  • Disson O, Haouzi D, Desagher S, Loesch K, Hahne M, Kremer EJ et al. (2004). Gastroenterology 126: 859–872.

  • El-Serag HB, Davila JA, Petersen NJ, McGlynn KA . (2003). Ann Intern Med 139: 817–823.

  • El-Serag HB, Mason AC . (1999). N Engl J Med 340: 745–750.

  • Erhardt A, Hassan M, Heintges T, Haussinger D . (2002). Virology 292: 272–284.

  • Farazi PA, Glickman J, Jiang S, Yu A, Rudolph KL, DePinho RA . (2003). Cancer Res 63: 5021–5027.

  • Foy E, Li K, Wang C, Sumpter Jr R, Ikeda M, Lemon SM et al. (2003). Science 300: 1145–1148.

  • Fukuda K, Tsuchihara K, Hijikata M, Nishiguchi S, Kuroki T, Shimotohno K . (2001). Hepatology 33: 159–165.

  • Fukutomi T, Zhou Y, Kawai S, Eguchi H, Wands JR, Li J . (2005). Hepatology 41: 1096–1105.

  • Furuya K, Nakamura M, Yamamoto Y, Togei K, Otsuka H . (1988). Cancer 61: 99–105.

  • Gale Jr M, Kwieciszewski B, Dossett M, Nakao H, Katze MG . (1999). J Virol 73: 6506–6516.

  • Gale Jr MJ, Korth MJ, Tang NM, Tan SL, Hopkins DA, Dever TE et al. (1997). Virology 230: 217–227.

  • Ghosh AK, Majumder M, Steele R, Yaciuk P, Chrivia J, Ray R et al. (2000). J Biol Chem 275: 7184–7188.

  • Giambartolomei S, Covone F, Levrero M, Balsano C . (2001). Oncogene 20: 2606–2610.

  • Goh PY, Tan YJ, Lim SP, Lim SG, Tan YH, Hong WJ . (2001). Virology 290: 224–236.

  • Gong G, Waris G, Tanveer R, Siddiqui A . (2001). Proc Natl Acad Sci USA 98: 9599–9604.

  • Guo JT, Bichko VV, Seeger C . (2001). J Virol 75: 8516–8523.

  • Hayashi J, Aoki H, Kajino K, Moriyama M, Arakawa Y, Hino O . (2000). Hepatology 32: 958–961.

  • Henry SH, Bosch FX, Troxell TC, Bolger PM . (1999). Science 286: 2453–2454.

  • Higashitsuji H, Itoh K, Nagao T, Dawson S, Nonoguchi K, Kido T et al. (2000). Nat Med 6: 96–99.

  • Honda A, Arai Y, Hirota N, Sato T, Ikegaki J, Koizumi T et al. (1999). J Med Virol 59: 281–289.

  • Hope RG, Murphy DJ, McLauchlan J . (2002). J Biol Chem 277: 4261–4270.

  • Hsieh TY, Matsumoto M, Chou HC, Schneider R, Hwang SB, Lee AS et al. (1998). J Biol Chem 273: 17651–17659.

  • Hsu IC, Metcalf RA, Sun T, Welsh JA, Wang NJ, Harris CC . (1991). Nature 350: 427–428.

  • Ide Y, Zhang L, Chen M, Inchauspe G, Bahl C, Sasaguri Y et al. (1996). Gene 182: 203–211.

  • Iizuka N, Oka M, Yamada-Okabe H, Mori N, Tamesa T, Okada T et al. (2002). Cancer Res 62: 3939–3944.

  • Ikeda M, Yi M, Li K, Lemon SM . (2002). J Virol 76: 2997–3006.

  • Ishido S, Hotta H . (1998). FEBS Lett 438: 258–262.

  • Ishido S, Muramatsu S, Fujita T, Iwanaga Y, Tong WY, Katayama Y et al. (1997). Biochem Biophys Res Commun 230: 431–436.

  • Jin DY, Wang HL, Zhou Y, Chun AC, Kibler KV, Hou YD et al. (2000). EMBO J 19: 729–740.

  • Joo M, Hahn YS, Kwon M, Sadikot RT, Blackwell TS, Christman JW . (2005). J Virol 79: 7648–7657.

  • Jordan R, Wang L, Graczyk TM, Block TM, Romano PR . (2002). J Virol 76: 9588–9599.

  • Kaufman RJ . (1999). Genes Dev 13: 1211–1233.

  • Kawamura T, Furusaka A, Koziel MJ, Chung RT, Wang TC, Schmidt EV et al. (1997). Hepatology 25: 1014–1021.

  • Kinoshita T, Miyajima A . (2002). Biochim Biophys Acta 1592: 303–312.

  • Kittlesen DJ, Chianese-Bullock KA, Yao ZQ, Braciale TJ, Hahn YS . (2000). J Clin Invest 106: 1239–1249.

  • Koike K, Moriya K, Ishibashi K, Yotsuyanagi H, Shintani Y, Fujie H et al. (1997). Proc Natl Acad Sci USA 94: 233–236.

  • Kojiro M . (2005). Best Pract Res Clin Gastroenterol 19: 39–62.

  • Lan KH, Sheu ML, Hwang SJ, Yen SH, Chen SY, Wu JC et al. (2002). Oncogene 21: 4801–4811.

  • Laurent-Puig P, Legoix P, Bluteau O, Belghiti J, Franco D, Binot F et al. (2001). Gastroenterology 120: 1763–1773.

  • Lee JS, Chu IS, Heo J, Calvisi DF, Sun Z, Roskams T et al. (2004). Hepatology 40: 667–676.

  • Lee JS, Thorgeirsson SS . (2002). Hepatology 35: 1134–1143.

  • Legoix P, Bluteau O, Bayer J, Perret C, Balabaud C, Belghiti J et al. (1999). Oncogene 18: 4044–4046.

  • Lerat H, Honda M, Beard MR, Loesch K, Sun J, Yang Y et al. (2002). Gastroenterology 122: 352–365.

  • Lerat H, Rumin S, Habersetzer F, Berby F, Trabaud MA, Trepo C et al. (1998). Blood 91: 3841–3849.

  • Levrero M, De Laurenzi V, Costanzo A, Gong J, Wang JY, Melino G . (2000). J Cell Sci 113 (Part 10): 1661–1670.

  • Liew CT, Li HM, Lo KW, Leow CK, Chan JY, Hin LY et al. (1999). Oncogene 18: 789–795.

  • Llovet JM, Burroughs A, Bruix J . (2003). Lancet 362: 1907–1917.

  • Lohmann V, Korner F, Dobierzewska A, Bartenschlager R . (2001). J Virol 75: 1437–1449.

  • Lohmann V, Korner F, Koch J, Herian U, Theilmann L, Bartenschlager R . (1999). Science 285: 110–113.

  • Lu W, Lo SY, Chen M, Wu K, Fung YK, Ou JH . (1999). Virology 264: 134–141.

  • Ma Y, Hendershot LM . (2001). Cell 107: 827–830.

  • Macdonald GA, Greenson JK, Saito K, Cherian SP, Appelman HD, Boland CR . (1998). Hepatology 28: 90–97.

  • Machida K, Tsukiyama-Kohara K, Seike E, Tone S, Shibasaki F, Shimizu M et al. (2001). J Biol Chem 276: 12140–12146.

  • Majumder M, Ghosh AK, Steele R, Ray R, Ray RB . (2001). J Virol 75: 1401–1407.

  • Majumder M, Ghosh AK, Steele R, Zhou XY, Phillips NJ, Ray R et al. (2002). Virology 294: 94–105.

  • Majumder M, Steele R, Ghosh AK, Zhou XY, Thornburg L, Ray R et al. (2003). FEBS Lett 555: 528–532.

  • Mamiya N, Worman HJ . (1999). J Biol Chem 274: 15751–15756.

  • Marcellin P, Asselah T, Boyer N . (2002). Hepatology 36: S47–S56.

  • Marchio A, Meddeb M, Pineau P, Danglot G, Tiollais P, Bernheim A et al. (1997). Genes Chromosomes Cancer 18: 59–65.

  • Marusawa H, Hijikata M, Chiba T, Shimotohno K . (1999). J Virol 73: 4713–4720.

  • Matsumoto M, Hsieh TY, Zhu N, VanArsdale T, Hwang SB, Jeng KS et al. (1997). J Virol 71: 1301–1309.

  • Merle P, de la Monte S, Kim M, Herrmann M, Tanaka S, Von Dem Bussche A et al. (2004). Gastroenterology 127: 1110–1122.

  • Ming L, Thorgeirsson SS, Gail MH, Lu P, Harris CC, Wang N et al. (2002). Hepatology 36: 1214–1220.

  • Mise M, Arii S, Higashituji H, Furutani M, Niwano M, Harada T et al. (1996). Hepatology 23: 455–464.

  • Mitsuhashi N, Shimizu H, Ohtsuka M, Wakabayashi Y, Ito H, Kimura F et al. (2003). Hepatology 37: 1105–1113.

  • Miyoshi Y, Iwao K, Nagasawa Y, Aihara T, Sasaki Y, Imaoka S et al. (1998). Cancer Res 58: 2524–2527.

  • Moradpour D, Blum HE . (2005). Eur J Gastroenterol Hepatol 17: 477–483.

  • Moradpour D, Wands JR . (2002). Molecular Pathogenesis of Hepatocellular Carcinoma. WB Saunders: Philadelphia.

    Google Scholar 

  • Moriya K, Fujie H, Shintani Y, Yotsuyanagi H, Tsutsumi T, Ishibashi K et al. (1998). Nat Med 4: 1065–1067.

  • Moriya K, Nakagawa K, Santa T, Shintani Y, Fujie H, Miyoshi H et al. (2001). Cancer Res 61: 4365–4370.

  • Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y et al. (1997). J Gen Virol 78 (Part 7): 1527–1531.

  • Muller M, Schilling T, Sayan AE, Kairat A, Lorenz K, Schulze-Bergkamen H et al. (2005). Cell Death Differ 12: 1564–1577.

  • Nagai H, Pineau P, Tiollais P, Buendia MA, Dejean A . (1997). Oncogene 14: 2927–2933.

  • Nam SW, Park JY, Ramasamy A, Shevade S, Islam A, Long PM et al. (2005). Hepatology 42: 809–818.

  • Nelson DR, Gonzalez-Peralta RP, Qian K, Xu Y, Marousis CG, Davis GL et al. (1997). J Viral Hepat 4: 29–35.

  • Neo SY, Leow CK, Vega VB, Long PM, Islam AF, Lai PB et al. (2004). Hepatology 39: 944–953.

  • Neuman MG, Benhamou JP, Bourliere M, Ibrahim A, Malkiewicz I, Asselah T et al. (2002). Cytokine 17: 108–117.

  • NIH Conference (2002). NIH Consens State Sci Statements 19: 1–46.

  • Nishida N, Fukuda Y, Komeda T, Kita R, Sando T, Furukawa M et al. (1994). Cancer Res 54: 3107–3110.

  • Ohata K, Hamasaki K, Toriyama K, Matsumoto K, Saeki A, Yanagi K et al. (2003). Cancer 97: 3036–3043.

  • Okabe H, Satoh S, Kato T, Kitahara O, Yanagawa R, Yamaoka Y et al. (2001). Cancer Res 61: 2129–2137.

  • Okuda M, Li K, Beard MR, Showalter LA, Scholle F, Lemon SM et al. (2002). Gastroenterology 122: 366–375.

  • Otsuka M, Kato N, Lan K, Yoshida H, Kato J, Goto T et al. (2000). J Biol Chem 275: 34122–34130.

  • Owsianka AM, Patel AH . (1999). Virology 257: 330–340.

  • Ozturk M . (1999). Semin Liver Dis 19: 235–242.

  • Palescandolo E, Schinzari E, Vossio S, Rossini A, Cariani E, Levrero M . (2006) (submitted).

  • Park JS, Yang JM, Min MK . (2000). Biochem Biophys Res Commun 267: 581–587.

  • Pasquinelli C, Shoenberger JM, Chung J, Chang KM, Guidotti LG, Selby M et al. (1997). Hepatology 25: 719–727.

  • Patil MA, Chua MS, Pan KH, Lin R, Lih CJ, Cheung ST et al. (2005). Oncogene 24: 3737–3747.

  • Pavio N, Battaglia S, Boucreux D, Arnulf B, Sobesky R, Hermine O et al. (2005). Oncogene 24: 6119–6132.

  • Perlemuter G, Sabile A, Letteron P, Vona G, Topilco A, Chretien Y et al. (2002). FASEB J 16: 185–194.

  • Pflugheber J, Fredericksen B, Sumpter Jr R, Wang C, Ware F, Sodora DL et al. (2002). Proc Natl Acad Sci USA 99: 4650–4655.

  • Piao Z, Kim H, Malkhosyan S, Park C . (2000). Int J Oncol 17: 507–512.

  • Pietschmann T, Lohmann V, Kaul A, Krieger N, Rinck G, Rutter G et al. (2002). J Virol 76: 4008–4021.

  • Pollicino T, Squadrito G, Cerenzia G, Cacciola I, Raffa G, Crax A et al. (2004). Gastroenterology 126: 102–110.

  • Polyak SJ, Khabar KS, Paschal DM, Ezelle HJ, Duverlie G, Barber GN et al. (2001). J Virol 75: 6095–6106.

  • Polyak SJ, McArdle S, Liu SL, Sullivan DG, Chung M, Hofgartner WT et al. (1998). J Virol 72: 4288–4296.

  • Putzer BM, Tuve S, Tannapfel A, Stiewe T . (2003). Cell Death Differ 10: 612–614.

  • Qadri I, Iwahashi M, Simon F . (2002). Biochim Biophys Acta 1592: 193–204.

  • Ravaggi A, Natoli G, Primi D, Albertini A, Levrero M, Cariani E . (1994). J Hepatol 20: 833–836.

  • Ray RB, Lagging LM, Meyer K, Ray R . (1996). J Virol 70: 4438–4443.

  • Ray RB, Meyer K, Steele R, Shrivastava A, Aggarwal BB, Ray R . (1998). J Biol Chem 273: 2256–2259.

  • Ray RB, Steele R, Basu A, Meyer K, Majumder M, Ghosh AK et al. (2002). Virus Res 87: 21–29.

  • Ray RB, Steele R, Meyer K, Ray R . (1997). J Biol Chem 272: 10983–10986.

  • Ruggieri A, Harada T, Matsuura Y, Miyamura T . (1997). Virology 229: 68–76.

  • Ruster B, Zeuzem S, Krump-Konvalinkova V, Berg T, Jonas S, Severin K et al. (2001). J Med Virol 63: 128–134.

  • Sabile A, Perlemuter G, Bono F, Kohara K, Demaugre F, Kohara M et al. (1999). Hepatology 30: 1064–1076.

  • Sakamuro D, Furukawa T, Takegami T . (1995). J Virol 69: 3893–3896.

  • Santoni-Rugiu E, Preisegger KH, Kiss A, Audolfsson T, Shiota G, Schmidt EV et al. (1996). Proc Natl Acad Sci USA 93: 9577–9582.

  • Satoh S, Daigo Y, Furukawa Y, Kato T, Miwa N, Nishiwaki T et al. (2000a). Nat Genet 24: 245–250.

  • Satoh S, Hirota M, Noguchi T, Hijikata M, Handa H, Shimotohno K . (2000b). Virology 270: 476–487.

  • Shi ST, Polyak SJ, Tu H, Taylor DR, Gretch DR, Lai MM . (2002). Virology 292: 198–210.

  • Shimoda R, Nagashima M, Sakamoto M, Yamaguchi N, Hirohashi S, Yokota J et al. (1994). Cancer Res 54: 3171–3172.

  • Shintani Y, Fujie H, Miyoshi H, Tsutsumi T, Tsukamoto K, Kimura S et al. (2004). Gastroenterology 126: 840–848.

  • Shirota Y, Kaneko S, Honda M, Kawai HF, Kobayashi K . (2001). Hepatology 33: 832–840.

  • Smith MW, Yue ZN, Geiss GK, Sadovnikova NY, Carter VS, Boix L et al. (2003). Cancer Res 63: 859–864.

  • Soo HM, Garzino-Demo A, Hong W, Tan YH, Tan YJ, Goh PY et al. (2002). Virology 303: 253–277.

  • Squadrito G, Pollicino T, Cacciola I, Caccamo G, Villari D, La Masa T et al. (2006). Cancer 106: 1326–1330.

  • Street A, Macdonald A, Crowder K, Harris M . (2004). J Biol Chem 279: 12232–12241.

  • Street A, Macdonald A, McCormick C, Harris M . (2005). J Virol 79: 5006–5016.

  • Sumida Y, Nakashima T, Yoh T, Nakajima Y, Ishikawa H, Mitsuyoshi H et al. (2000). J Hepatol 33: 616–622.

  • Sun Z, Lu P, Gail MH, Pee D, Zhang Q, Ming L et al. (1999). Hepatology 30: 379–383.

  • Suzuki R, Matsuura Y, Suzuki T, Ando A, Chiba J, Harada S et al. (1995). J Gen Virol 76 (Part 1): 53–61.

  • Tai DI, Tsai SL, Chang YH, Huang SN, Chen TC, Chang KS et al. (2000a). Cancer 89: 2274–2281.

  • Tai DI, Tsai SL, Chen YM, Chuang YL, Peng CY, Sheen IS et al. (2000b). Hepatology 31: 656–664.

  • Tan SL, Nakao H, He Y, Vijaysri S, Neddermann P, Jacobs BL et al. (1999). Proc Natl Acad Sci USA 96: 5533–5538.

  • Tanaka S, Mori M, Sakamoto Y, Makuuchi M, Sugimachi K, Wands JR . (1999). J Clin Invest 103: 341–345.

  • Taniguchi H, Kato N, Otsuka M, Goto T, Yoshida H, Shiratori Y et al. (2004). J Med Virol 72: 52–59.

  • Tanimoto A, Ide Y, Arima N, Sasaguri Y, Padmanabhan R . (1997). Biochem Biophys Res Commun 236: 360–364.

  • Tardif KD, Mori K, Siddiqui A . (2002). J Virol 76: 7453–7459.

  • Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM . (1999). Science 285: 107–110.

  • Taylor-Robinson SD, Foster GR, Arora S, Hargreaves S, Thomas HC . (1997). Lancet 350: 1142–1143.

  • Tellinghuisen TL, Rice CM . (2002). Curr Opin Microbiol 5: 419–427.

  • Terada T, Ueda K, Nakanuma Y . (1993). Virchows Arch A 422: 381–388.

  • Thimme R, Bukh J, Spangenberg HC, Wieland S, Pemberton J, Steiger C et al. (2002). Proc Natl Acad Sci USA 99: 15661–15668.

  • Thorgeirsson SS, Grisham JW . (2002). Nat Genet 31: 339–346.

  • Thorgeirsson SS, Lee JS, Grisham JW . (2006). Hepatology 43: S145–S150.

  • Torbenson M, Thomas DL . (2002). Lancet Infect Dis 2: 479–486.

  • Tseng CT, Klimpel GR . (2002). J Exp Med 195: 43–49.

  • Tsuchihara K, Ueno K, Yamanaka A, Isono K, Endo K, Nishida R et al. (2000). FEBS Lett 478: 299–303.

  • Tu H, Gao L, Shi ST, Taylor DR, Yang T, Mircheff AK et al. (1999). Virology 263: 30–41.

  • Varaklioti A, Vassilaki N, Georgopoulou U, Mavromara P . (2002). J Biol Chem 277: 17713–17721.

  • Vossio S, Palescandolo E, Pediconi N, Moretti F, Balsano C, Levrero M et al. (2002). Oncogene 21: 3796–3803.

  • Wakita T, Katsume A, Kato J, Taya C, Yonekawa H, Kanegae Y et al. (2000). J Med Virol 62: 308–317.

  • Wakita T, Taya C, Katsume A, Kato J, Yonekawa H, Kanegae Y et al. (1998). J Biol Chem 273: 9001–9006.

  • Waleswski JL, Keller TR, Stump DD, Branch AD . (2001). RNA 7: 710–721.

  • Wang F, Yoshida I, Takamatsu M, Ishido S, Fujita T, Oka K et al. (2000). Biochem Biophys Res Commun 273: 479–484.

  • Waris G, Tardif KD, Siddiqui A . (2002). Biochem Pharmacol 64: 1425–1430.

  • Xu Z, Choi J, Yen TS, Lu W, Strohecker A, Govindarajan S et al. (2001). Embo J 20: 3840–3848.

  • Yamaguchi R, Yano H, Iemura A, Ogasawara S, Haramaki M, Kojiro M . (1998). Hepatology 28: 68–77.

  • Yamanaka T, Uchida M, Doi T . (2002). Biochem Biophys Res Commun 294: 521–527.

  • Ye QH, Qin LX, Forgues M, He P, Kim JW, Peng AC et al. (2003). Nat Med 9: 416–423.

  • Yoshida T, Hanada T, Tokuhisa T, Kosai K, Sata M, Kohara M et al. (2002). J Exp Med 196: 641–653.

  • You LR, Chen CM, Yeh TS, Tsai TY, Mai RT, Lin CH et al. (1999). J Virol 73: 2841–2853.

  • Zhao LJ, Wang L, Ren H, Cao J, Li L, Ke JS et al. (2005). Exp Cell Res 305: 23–32.

  • Zhou T, Evans AA, London WT, Xia X, Zou H, Shen F et al. (1997). Cancer Res 57: 2749–2753.

  • Zhu N, Khoshnan A, Schneider R, Matsumoto M, Dennert G, Ware C et al. (1998). J Virol 72: 3691–3697.

  • Zhu N, Ware CF, Lai MM . (2001). Virology 283: 178–187.

Download references

Acknowledgements

This work was supported by grants from Associazione Italiana per la Ricerca sul Cancro (AIRC), from the ‘Ministero dell'Istruzione dell'Università e della Ricerca Scientifica’ (PRIN, FIRB) and from the European Community (LSHC-CT-2004-503576).

Author information

Authors and Affiliations

  1. Department of Internal Medicine, University of Rome ‘La Sapienza’, Rome, Italy

    M Levrero

  2. Laboratory of Gene Expression, Fondazione Andrea Cesalpino, Rome, Italy

    M Levrero

  3. Department of Experimental Oncology and AIRC Center for Molecular Oncogenomics (ROC), Regina Elena Cancer Center, Rome, Italy

    M Levrero

Authors
  1. M Levrero
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M Levrero.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Levrero, M. Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene 25, 3834–3847 (2006). https://doi.org/10.1038/sj.onc.1209562

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1209562

Keywords

This article is cited by

Search

Advanced search

Quick links