Molecular Pathogenesis of Hepatocellular Carcinoma

Journal of Surgical Research

Volumn 136, Issue 1, 2006, Pages 125-135

  McKillop, Iain H ^a   Moran, Diarmuid M ^a   Jin, Xiaoling ^b   Koniaris, Leonidas G ^b  

^a UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

chronic active hepatits; cirrhosis; hepatitis; hepatocelluar; nodule

Indexed keywords

ALPHA INTERFERON; CISPLATIN; DOXORUBICIN; EPIRUBICIN; ERLOTINIB; FLOXURIDINE; FLUOROURACIL; HEPATITIS VACCINE; INTERFERON; IODINATED POPPYSEED OIL; LAMIVUDINE; PACLITAXEL; RIBAVIRIN;

ALCOHOL ABUSE; ASPERGILLUS FLAVUS; ASPERGILLUS PARASITICUS; CANCER STAGING; CANCER SURGERY; HEPATITIS C; HUMAN; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER TRANSPLANTATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; REVIEW; TUMOR RECURRENCE; VIRUS HEPATITIS;

ANIMALS; CARCINOMA, HEPATOCELLULAR; HUMANS; LIVER NEOPLASMS;

EID: 33750296975     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2006.04.013     Document Type: Review

References (112)

1. Kew M.C. Epidemiology of hepatocellular carcinoma. Toxicology 35 (2002) 181-182
2. Okuda K. Hepatocellular carcinoma. J Hepatol 32 (2000) 225
3. Parkin D.M., Bray F., Ferlay J., and Pisani P. Estimating the world cancer burden: Globocan 2000. Int J Cancer 94 (2001) 153
4. Llovet J.M., Burroughs A., and Bruix J. Hepatocellular carcinoma. Lancet 362 (2003) 1907
5. Bosch F.X., Ribes J., Cleries R., and Diaz M. Epidemiology of hepatocellular carcinoma. Clin Liver Dis 9 (2005) 191
6. Bosch F.X., Ribes J., and Borras J. Epidemiology of primary liver cancer. Semin Liver Dis 19 (1999) 271
7. Bergsland E.K., and Venook A.P. Hepatocellular carcinoma. Curr Opin Oncol 12 (2000) 357
8. Davis G.L., Albright J.E., Cook S.F., and Rosenberg D.M. Projecting future complications of chronic hepatitis C in the United States. Liver Transpl 9 (2003) 331
9. Smart R.G., Mann R.E., and Suurvali H. Changes in liver cirrhosis death rates in different countries in relation to per capita alcohol consumption and Alcoholics Anonymous membership. J Stud Alcohol 59 (1998) 245
10. Koniaris L.G., McKillop I.H., Schwartz S.I., and Zimmers T.A. Liver regeneration. J Am Coll Surg 197 (2003) 634
11. Zhu A.X. Hepatocellular carcinoma: are we making progress?. Cancer Invest 21 (2003) 418
12. el-Serag H.B. Epidemiology of hepatocellular carcinoma. Clin Liver Disease 5 (2001) 87
13. Kew M.C. Interaction between hepatitis B and C viruses in hepatocellular carcinogenesis. J Viral Hepat 13 (2006) 145
14. Ray Kim W. Global epidemiology and burden of hepatitis C. Microbes Infect 4 (2002) 1219
15. Ali A., and Zein N.N. Hepatitis C infection: a systemic disease with extrahepatic manifestations. Cleve Clin J Med 72 (2005) 1005-1008, 1010-1004, 1016 passim.
16. Gordon S.C., Bayati N., and Silverman A.L. Clinical outcome of hepatitis C as a function of mode of transmission. Hepatology 28 (1998) 562
17. Degos F., Christidis C., Ganne-Carrie N., et al. Hepatitis C virus related cirrhosis: time to occurrence of hepatocellular carcinoma and death. Gut 47 (2000) 131
18. Romeo R., and Colombo M. The natural history of hepatocellular carcinoma. Toxicology 39 (2002) 181-182
19. Ikeda K., Saitoh S., Koida I., et al. A multivariate analysis of risk factors for hepatocellular carcinogenesis: a prospective observation of 795 patients with viral and alcoholic cirrhosis. Hepatology 18 (1993) 47
20. Ray R.B., Lagging L.M., Meyer K., Steele R., and Ray R. Transcriptional regulation of cellular and viral promoters by the hepatitis C virus core protein. Virus Res 37 (1995) 209
21. Moriya K., Fujie H., Shintani Y., et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med 4 (1998) 1065
22. Marusawa H., Hijikata M., Chiba T., and Shimotohno K. Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alpha-mediated apoptosis via NF-kappaB activation. J Virol 73 (1999) 4713
23. Jin X., Zimmers T.A., Perez E.A., Pierce R.H., Zhang Z., and Koniaris L.G. Paradoxical effects of short- and long-term interleukin-6 exposure on liver injury and repair. Hepatology 43 (2006) 474
24. Hayashi J., Aoki H., Kajino K., Moriyama M., Arakawa Y., and Hino O. Hepatitis C virus core protein activates the MAPK/ERK cascade synergistically with tumor promoter TPA, but not with epidermal growth factor or transforming growth factor alpha. Hepatology 32 (2000) 958
25. Sakamuro D., Furukawa T., and Takegami T. Hepatitis C virus nonstructural protein NS3 transforms NIH 3T3 cells. J Virol 69 (1995) 3893
26. Ghosh A.K., Steele R., Meyer K., Ray R., and Ray R.B. Hepatitis C virus NS5A protein modulates cell cycle regulatory genes and promotes cell growth. J General Virol 80 (1999) 1179
27. Maddrey W.C. Hepatitis B-an important public health issue. Clin Laboratory 47 (2001) 51
28. Beasley R.P., Hwang L.Y., Lin C.C., and Chien C.S. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22 707 men in Taiwan. Lancet 2 (1981) 1129
29. Lok A.S. Hepatitis B infection: pathogenesis and management. J Hepatology 32 (2000) 89
30. Huo T.I., Wang X.W., Forgues M., et al. Hepatitis B virus X mutants derived from human hepatocellular carcinoma retain the ability to abrogate p53-induced apoptosis. Oncogene 20 (2001) 3620
31. Brau N. Treatment of chronic hepatitis C in human immunodeficiency virus/hepatitis C virus-coinfected patients in the era of pegylated interferon and ribavirin. Semin Liver Dis 25 (2005) 33
32. Henry S.H., Bosch F.X., and Bowers J.C. Aflatoxin, hepatitis and worldwide liver cancer risks. Adv Exp Med Biol 504 (2002) 229
33. Smela M.E., Currier S.S., Bailey E.A., and Essigmann J.M. The chemistry and biology of aflatoxin B(1): from mutational spectrometry to carcinogenesis. Carcinogenesis 22 (2001) 535
34. Miller E.C. Some current perspectives on chemical carcinogenesis in humans and experimental animals: Presidential Address. Cancer Res 38 (1978) 1479
35. Essigmann J.M., Green C.L., Croy R.G., Fowler K.W., Buchi G.H., and Wogan G.N. Interactions of aflatoxin B1 and alkylating agents with DNA: structural and functional studies. Cold Spring Harb Symp Quant Biol 1 (1983) 327
36. Hsu I.C., Metcalf R.A., Sun T., Welsh J.A., Wang N.J., and Harris C.C. Mutational hotspot in the p53 gene in human hepatocellular carcinomas. Nature 350 (1991) 427
37. Shen H.M., and Ong C.N. Mutations of the p53 tumor suppressor gene and ras oncogenes in aflatoxin hepatocarcinogenesis. Mutat Res 366 (1996) 23
38. Puisieux A., Lim S., Groopman J., and Ozturk M. Selective targeting of p53 gene mutational hotspots in human cancers by etiologically defined carcinogens. Cancer Res 51 (1991) 6185
39. Albano E., French S.W., and Ingelman-Sundberg M. Hydroxyethyl radicals in ethanol hepatotoxicity. Front Biosci 4 (1999) D533
40. Longnecker M.P. Alcohol consumption and risk of cancer in humans: an overview. Alcohol 12 (1995) 87
41. McKillop I.H., and Schrum L.W. Alcohol and liver cancer. Alcohol 35 (2005) 195
42. Hoek J.B., and Pastorino J.G. Cellular signaling mechanisms in alcohol-induced liver damage. Semin Liver Dis 24 (2004) 257
43. Donato F., Tagger A., Gelatti U., et al. Alcohol and hepatocellular carcinoma: the effect of lifetime intake and hepatitis virus infections in men and women. Am J Epidemiol 155 (2002) 323
44. Voigt M.D. Alcohol in hepatocellular cancer. Clin Liver Dis 9 (2005) 151
45. Yu H., Harris R.E., Kabat G.C., and Wynder E.L. Cigarette smoking, alcohol consumption and primary liver cancer: a case-control study in the USA. Int J Cancer 42 (1988) 325
46. Holmes-McNary M. Impact factors on development of cirrhosis and subsequent hepatocellular carcinoma. Compend Contin Educ Dent 22 (2001) 19
47. Yamada Y., Weller R.O., Kleihues P., and Ludeke B.I. Effects of ethanol and various alcoholic beverages on the formation of O6-methyldeoxyguanosine from concurrently administered N-nitrosomethylbenzylamine in rats: a dose-response study. Carcinogenesis 13 (1992) 1171
48. Crabb D.W., Bosron W.F., and Li T.K. Ethanol metabolism. Pharmacol Ther 34 (1987) 59
49. Ekstrom G., and Ingelman-Sundberg M. Rat liver microsomal NADPH-supported oxidase activity and lipid peroxidation dependent on ethanol-inducible cytochrome P-450 (P-450IIE1). Biochem Pharmacol 38 (1989) 1313
50. Wu D., and Cederbaum A.I. Alcohol, oxidative stress, and free radical damage. Alcohol Res Health 27 (2003) 277
51. Lieber C.S., and Leo M.A. Metabolism of ethanol and some associated adverse effects on the liver and the stomach. Recent Dev Alcohol 14 (1998) 7
52. Morimoto M., Hagbjork A.L., Nanji A.A., et al. Role of cytochrome P4502E1 in alcoholic liver disease pathogenesis. Alcohol 10 (1993) 459
53. Dupont I., Lucas D., Clot P., Menez C., and Albano E. Cytochrome P4502E1 inducibility and hydroxyethyl radical formation among alcoholics. J Hepatol 28 (1998) 564
54. Guengerich F.P., Shimada T., Yun C.H., et al. Interactions of ingested food, beverage, and tobacco components involving human cytochrome P4501A2, 2A6, 2E1, and 3A4 enzymes. Environ Health Perspect 102 Suppl 9 (1994) 49
55. Djordjevic D., Nikolic J., and Stefanovic V. Ethanol interactions with other cytochrome P450 substrates including drugs, xenobiotics, and carcinogens. Pathol Biol (Paris) 46 (1998) 760
56. Lu S.C. Regulation of glutathione synthesis. Curr Top Cell Regul 36 (2000) 95
57. Fernandez-Checa J.C., Kaplowitz N., Garcia-Ruiz C., and Colell A. Mitochondrial glutathione: importance and transport. Semin Liver Dis 18 (1998) 389
58. Bode C., and Bode J.C. Effect of alcohol consumption on the gut. Best Pract Res Clin Gastroenterol 17 (2003) 575
59. Sato M., Suzuki S., and Senoo H. Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 28 (2003) 105
60. Stickel F., Schuppan D., Hahn E.G., and Seitz H.K. Cocarcinogenic effects of alcohol in hepatocarcinogenesis. Gut 51 (2002) 132
61. Smedile A., and Bugianesi E. Steatosis and hepatocellular carcinoma risk. Eur Rev Med Pharmacol Sci 9 (2005) 291
62. Bugianesi E. Review article: steatosis, the metabolic syndrome and cancer. Aliment Pharmacol Ther 22 Suppl 2 (2005) 40
63. Caldwell S.H., Crespo D.M., Kang H.S., and Al-Osaimi A.M. Obesity and hepatocellular carcinoma. Gastroenterology 127 (2004) S97
64. She Q.B., Solit D.B., Ye Q., et al. The BAD protein integrates survival signaling by EGFR/MAPK and PI3K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell 8 (2005) 287
65. Bianco R., Shin I., Ritter C.A., et al. Loss of PTEN/MMAC1/TEP in EGF receptor-expressing tumor cells counteracts the antitumor action of EGFR tyrosine kinase inhibitors. Oncogene 22 (2003) 2812
66. Feitelson M.A., Sun B., Satiroglu Tufan N.L., Liu J., Pan J., and Lian Z. Genetic mechanisms of hepatocarcinogenesis. Oncogene 21 (2002) 2593
67. Lencioni R., Cioni D., Crocetti L., and Bartolozzi C. Percutaneous ablation of hepatocellular carcinoma: state-of-the-art. Liver Transpl 10 (2004) S91
68. Lim I.K. Spectrum of molecular changes during hepatocarcinogenesis induced by DEN and other chemicals in Fischer 344 male rats. [republished in Mech Ageing Dev 2003;124:697; PMID: 12825548]. Mechanisms Ageing Dev 123 (2002) 1665
69. Arakawa M., Kage M., Sugihara S., Nakashima T., Suenaga M., and Okuda K. Emergence of malignant lesions within an adenomatous hyperplastic nodule in a cirrhotic liver. Observations in five cases. Gastroenterology 91 (1986) 198
70. Takayama T., Makuuchi M., Hirohashi S., et al. Malignant transformation of adenomatous hyperplasia to hepatocellular carcinoma. Lancet 336 (1990) 1150
71. Nakashima Y., Nakashima O., Hsia C.C., Kojiro M., and Tabor E. Vascularization of small hepatocellular carcinomas: correlation with differentiation. Liver 19 (1999) 12
72. Okazaki I., Wada N., Nakano M., et al. Difference in gene expression for matrix metalloproteinase-1 between early and advanced hepatocellular carcinomas. Hepatology 25 (1997) 580
73. Edamoto Y., Hara A., Biernat W., et al. Alterations of RB1, p53 and Wnt pathways in hepatocellular carcinomas associated with hepatitis C, hepatitis B and alcoholic liver cirrhosis. Int J Cancer 106 (2003) 334
74. Okabe H., Satoh S., Kato T., et al. Genome-wide analysis of gene expression in human hepatocellular carcinomas using cDNA microarray: identification of genes involved in viral carcinogenesis and tumor progression. Cancer Res 61 (2001) 2129
75. Schmidt C.M., McKillop I.H., Cahill P.A., and Sitzmann J.V. Increased MAPK expression and activity in primary human hepatocellular carcinoma. Biochem Biophys Res Commun 236 (1997) 54
76. Schmidt C.M., McKillop I.H., Cahill P.A., and Sitzmann J.V. Alterations in guanine nucleotide regulatory protein expression and activity in human hepatocellular carcinoma. Hepatology 26 (1997) 1189
77. Kimura H., Kagawa K., Deguchi T., et al. Cytogenetic analyses of hepatocellular carcinoma by in situ hybridization with a chromosome-specific DNA probe. Cancer 77 (1996) 271
78. Chaubert P., Gayer R., Zimmermann A., et al. Germ-line mutations of the p16INK4(MTS1) gene occur in a subset of patients with hepatocellular carcinoma. Hepatology 25 (1997) 1376
79. Calvisi D.F., Factor V.M., Loi R., and Thorgeirsson S.S. Activation of beta-catenin during hepatocarcinogenesis in transgenic mouse models: relationship to phenotype and tumor grade. Cancer Res 61 (2001) 2085
80. Zimmers T.A., Pierce R.H., McKillop I.H., and Koniaris L.G. Resolving the role of IL-6 in liver regeneration. author reply 1591. Hepatology 38 (2003) 1590-1591
81. Zimmers T.A., McKillop I.H., Pierce R.H., Yoo J.Y., and Koniaris L.G. Massive liver growth in mice induced by systemic interleukin 6 administration. Hepatology 38 (2003) 326-334
82. Cadoret A., Ovejero C., Saadi-Kheddouci S., et al. Hepatomegaly in transgenic mice expressing an oncogenic form of beta-catenin. Cancer Res 61 (2001) 3245
83. Buetow K.H., Sheffield V.C., Zhu M., et al. Low frequency of p53 mutations observed in a diverse collection of primary hepatocellular carcinomas. Proc Natl Acad Sci USA 89 (1992) 9622
84. Teramoto T., Satonaka K., Kitazawa S., Fujimori T., Hayashi K., and Maeda S. p53 gene abnormalities are closely related to hepatoviral infections and occur at a late stage of hepatocarcinogenesis. Cancer Res 54 (1994) 231
85. Ozturk M. p53 mutation in hepatocellular carcinoma after aflatoxin exposure. Lancet 338 (1991) 1356
86. Thorgeirsson S.S., Lee J.S., and Grisham J.W. Molecular prognostication of liver cancer: end of the beginning. J Hepatol 44 (2006) 798
87. Johnson P.J. Malignant tumors of the liver. In: O'Grady J., Lake J., and Howdle P. (Eds). Comprehensive clinical hepatology (2000), Mosby, London 18-25-21-25
88. Chang M.H., Chen C.J., Lai M.S., et al. Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. [see comment]. N Engl J Med 336 (1997) 1855
89. Forns X., Bukh J., and Purcell R.H. The challenge of developing a vaccine against hepatitis C virus. J Hepatol 37 (2002) 684
90. Ikeda K., Saitoh S., Kobayashi M., et al. Long-term interferon therapy for 1 year or longer reduces the hepatocellular carcinogenesis rate in patients with liver cirrhosis caused by hepatitis C virus: a pilot study. J Gastroenterol Hepatol 16 (2001) 406
91. Breborowicz J., Mackiewicz A., and Breborowicz D. Microheterogeneity of alpha-fetoprotein in patient serum as demonstrated by lectin affino-electrophoresis. Scand J Immunol 14 (1981) 15
92. Kuromatsu R., Tanaka M., Shimauchi Y., Shimada M., Tanikawa K., Watanabe K., and Yokoo T. Usefulness of ED036 kit for measuring serum PIVKA-II levels in small hepatocellular carcinoma. J Gastroenterol 32 (1997) 507
93. Bruix J., Sherman M., Llovet J.M., et al., European Association for the Study of the Liver. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. [see comment]. J Hepatol 35 (2001) 421
94. Liu J.H., Chen P.W., Asch S.M., Busuttil R.W., and Ko C.Y. Surgery for hepatocellular carcinoma: does it improve survival?. Ann Surg Oncol 11 (2004) 298
95. Shabahang M., Franceschi D., Yamashiki N., et al. Comparison of hepatic resection and hepatic transplantation in the treatment of hepatocellular carcinoma among cirrhotic patients. Ann Surg Oncol 9 (2002) 881
96. Jansen M.C., van Hillegersberg R., Chamuleau R.A., van Delden O.M., Gouma D.J., and van Gulik T.M. Outcome of regional and local ablative therapies for hepatocellular carcinoma: a collective review. Eur J Surg Oncol 31 (2005) 331
97. Bruix J., and Llovet J.M. Prognostic prediction and treatment strategy in hepatocellular carcinoma. Hepatology 35 (2002) 519
98. Kokudo N., and Makuuchi M. Current role of portal vein embolization/hepatic artery chemoembolization. Surg Clin North Am 84 (2004) 643
99. Koniaris L.G., Chan D.Y., Magee C., et al. Focal hepatic ablation using interstitial photon radiation energy. J Am Coll Surg 191 (2000) 164
100. Garcea G., Lloyd T.D., Aylott C., Maddern G., and Berry D.P. The emergent role of focal liver ablation techniques in the treatment of primary and secondary liver tumours. Eur J Cancer 39 (2003) 2150
101. Rust C., and aGores G.J. Locoregional management of hepatocellular carcinoma. Surgical and ablation therapies. Clin Liver Disease 5 (2001) 161
102. Aguayo A., and Patt Y.Z. Nonsurgical treatment of hepatocellular carcinoma. Clin Liver Disease 5 (2001) 175
103. Suehiro T., Terashi T., Shiotani S., Soejima Y., and Sugimachi K. Liver transplantation for hepatocellular carcinoma. Surgery 131 (2002) S190
104. El-Meteini M., Fayez A., Fathy M., et al. Living related liver transplantation for hepatocellular carcinoma in Egypt. Transplant Proc 37 (2005) 3141
105. Dumortier J., Chapuis F., Borson O., et al. Unresectable hepatocellular carcinoma: Survival and prognostic factors after lipiodol chemoembolisation in 89 patients. Dig Liver Dis 38 (2006) 125
106. Di Maio M., De Maio E., Perrone F., Pignata S., and Daniele B. Hepatocellular carcinoma: systemic treatments. J Clin Gastroenterol 35 (2002) S109
107. Muto Y., Moriwaki H., Ninomiya M., et al. Prevention of second primary tumors by an acyclic retinoid, polyprenoic acid, in patients with hepatocellular carcinoma. Hepatoma Prevention Study Group. N Engl J Med 334 (1996) 1561
108. Ben-Josef E., Normolle D., Ensminger W.D., et al. Phase II trial of high-dose conformal radiation therapy with concurrent hepatic artery floxuridine for unresectable intrahepatic malignancies. J Clin Oncol 23 (2005) 8739
109. Philip P.A., Mahoney M.R., Allmer C., et al. Phase II study of Erlotinib (OSI-774) in patients with advanced hepatocellular cancer. J Clin Oncol 23 (2005) 6657
110. Lee J.S., Chu I.S., Heo J., et al. Classification and prediction of survival in hepatocellular carcinoma by gene expression profiling. Hepatology 40 (2004) 667
111. Smith M.W., Yue Z.N., Geiss G.K., et al. Identification of novel tumor markers in hepatitis C virus-associated hepatocellular carcinoma. Cancer Res 63 (2003) 859
112. Iizuka N., Oka M., Yamada-Okabe H., et al. Oligonucleotide microarray for prediction of early intrahepatic recurrence of hepatocellular carcinoma after curative resection. Lancet 361 (2003) 923