A review of molecular mechanisms in the development of hepatocellular carcinoma by afatoxin and hepatitis B and C viruses

Journal of Environmental Pathology, Toxicology and Oncology

Volumn 32, Issue 2, 2013, Pages 165-175

  Moudgil, Vandana ^a   Redhu, Davender ^a   Dhanda, Suman ^a   Singh, Jasbir ^a  

^a KURUKSHETRA UNIVERSITY   (India)

Author keywords

Afatoxins; Biological biomarkers; Carcinoma; DNA adducts; Hepacivirus; Hepatitis B virus; Hepato toxicity; Signal recognition particle

Indexed keywords

AFLATOXIN; BIOLOGICAL MARKER; PROTEIN P53; TELOMERASE REVERSE TRANSCRIPTASE; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CARCINOGENESIS; CELL CYCLE PROGRESSION; CODON; DISEASE ASSOCIATION; EXPOSURE; GROWTH REGULATION; HEPATITIS B; HEPATITIS C; HUMAN; LIPID PEROXIDATION; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MASS IMMUNIZATION; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUESTIONNAIRE; RISK ASSESSMENT; RISK FACTOR; VIRUS GENE; VIRUS MUTATION;

AFLATOXIN B1; ANIMALS; CARCINOMA, HEPATOCELLULAR; DNA ADDUCTS; HEPACIVIRUS; HEPATITIS B VIRUS; HUMANS; LIPID PEROXIDATION; LIVER NEOPLASMS; MUTATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84884166945     PISSN: 07318898     EISSN: None     Source Type: Journal    
DOI: 10.1615/JEnvironPatholToxicolOncol.2013007166     Document Type: Article

References (90)

1. Yu J, Chang PK, Ehrlich KC, Cary JW, Bhat-nagar D, Cleveland TE, Payne GA, Linz JE, Wo-loshuk CP, Bennett JW. Clustered pathway genes in afatoxin biosynthesis. Appl Environ Microbiol. 2004;70:1253-62.
2. Ueno Y, Ueno I. Toxicology and biochemistry of mycotoxins In: Uraguchi K, Yamazaki M, editors. Toxicology, biochemistry and pathology of myco-toxins. New York: Halstead Press; 1978. p. 107-188.
3. Wild CP, Gong YY. Mycotoxins and human disease: a largely ignored global health issue. Carci-nogenesis. 2010;31:71-82.
4. Dutton MF, Heathcote JG. The structure, biochemical properties and origin of the afatoxins B2a and G2a. Chem Ind. 1968;13:418-421.
5. Holzapfel CW, Steyn PS, Purchase IFH. Isolation and structure of afatoxins M1 and M2. Tetrahedron Lett. 1966;25:2799-2803.
6. Hsieh DP, Lin MT, Yao RC, Singh R. Biogenesis of afatoxins: conversion of norsolorinsic acid and other hypothetical intermediates into afatoxin B1 by Aspergillus parasiticus. J Agric Food Chem. 1976;24:1170-1174.
7. Lin MT, Hsieh DP, Yao RC, Donkersloot JA. Conversion of averufn into afatoxins by Aspergillus parasiticus. Biochemistry. 1973;12:5167-5171.
8. Lee LS, Bennet JW, Cucullu AF, Ory RL. Biogenesis of afatoxin B1: conversion of versicolorin A to afatoxin B1 by Aspergillus parasiticus. J Agric Food Chem. 1976;24:1167-1170.
9. Bennet JW, Lee LS, Shoss SM, Boudreaux GH. Identifcation of averatin as an AFB1 precursor; placement in the biosynthetic pathway. Appl Environ Microbiol. 1980;39:835-839.
10. Wong JJ, Hsieh DP. Mutagenicity of afatoxins related to their metabolism and carcinogenic potential. Proc Natl Acad Sci U S A. 1976;73:2241-2244.
11. Patterson DS. Metabolism as a factor in determining toxic action of afatoxins in different animal species. Food Cosmet Toxicol. 1973;11:287-294.
12. Dalezios J, Wogan GN, Weinbeb SM. Afatoxin P1: a new afatoxin metabolite in monkeys. Science. 1971;171:584-585.
13. Verma RJ. Afatoxins cause DNA damage. Int J Hum Genet. 2004;4:231-236.
14. Muench KF, Misra RP, Humayun MZ. Sequence specifcity in afatoxin B1-DNA interactions. Proc Natl Acad Sci U S A. 1983;80:6-10.
15. Basu AK, Essigmann JM. Site-specifcally modi-fed oligodeoxynucleotides as probes for the structural and biological effects of DNA-damaging agents. Chem Res Toxicol. 1988;1:1-18.
16. Swenson DH, Miller EC, Miller JA. Afatoxin B1-2, 3-oxide: evidence for its formation in rat liver in vivo and by human liver microsomes in vitro. Bio-chem Biophys Res Commun. 1974;60:1036-1043.
17. Wogan GN, Newberne PM. Dose-response characteristics of AFB1 carcinogenesis in the rat. Cancer Res. 1967;27:2370-2376.
18. Kirk GD, Camus-Randon AM, Mendy M, Goedert JJ, Merle P, Trepo C, Brechot C, Hainaut P, Mon-tesano R. Ser-249 p53 mutations in plasma DNA of patients with hepatocellular carcinoma from The Gambia. J Natl Cancer Inst. 2000;92:148-153.
19. Smela ME, Currier SS, Bailey EA, Essigmann JM. The chemistry and biology of afatoxin B1: from mutational spectrometry to carcinogenesis. Carci-nogenesis. 2001;22:535-545.
20. Katiyar S, Dash BC, Thakur V, Guptan RC, Sarin SK, Das BC. p53 Tumor suppressor gene mutations in hepatocellular carcinoma patients in India. Cancer. 2000;88:1565-1573.
21. Chen SY, Chen CJ, Chou SR. Association of af-latoxin B1-albumin adducts levels with hepatitis B surface antigen status among adolescents in Taiwan. Cancer Epidemiol Biomarkers Prev. 2001;10:1223-1226.
22. Wang JS, Qian GS, Zarba A, He X, Zhu YR, Zhang BC, Jacobson L, Gange SJ, Munoz A, Kensler TW, Groopman JD. Temporal patterns of afatoxin-albu-min adducts in hepatitis B surface antigen-positive and antigen-negative residents of Daxin, Qidong County, People's Republic of China. Cancer Epidemiol Biomarkers Prev. 1996;5:253-261.
23. Groopman JD, Wang JS, Scholl P. Molecular bio-markers for afatoxins: from adducts to gene mutations to human liver cancer. Can J Physiol Pharmacol. 1996;74:203-209.
24. Sarasin A, Moule Y. Translational step inhibited in vivo by afatoxin B1 in rat-liver polysomes. Eur J Biochem. 1975;54:329-340.
25. Singh J, Dani HM, Singh S, Sharma R, Steinberg P. Interactions of afatoxin B1 with SRP components can disrupt protein targeting. Cell Biochem Funct. 2005;23:9-13.
26. Singh J, Dani HM, Sharma R, Steinberg P. Inhibition of the biosynthesis of SRP polypeptides and secretory proteins by afatoxin B1 can disrupt protein targeting. Cell Biochem Funct. 2006;24:507-10.
27. Toskulkao C, Glinsukon T. Hepatic lipid peroxi-dation and intracellular calcium accumulation in ethanol potentiated afatoxin B1 toxicity. J Pharma-cobiodyn. 1988;11:191-197.
28. Raval PJ, Verma RJ. Afatoxin-induced cytotoxici-ties in rabbit's hepatocytes. J Anim Morphol Physi-ol. 1997;44:1-4.
29. Roebuck BD. Hyperplasia, partial hepatectomy and the carcinogenicity of afatoxin B1. J Cell Biochem. 2004;91:243-249.
30. Degen GH, Neumann HG. The major metabolite of afatoxin B1 in the rat is a glutathione conjugate. Chem Biol Interact. 1978;22:239-255.
31. Bodreddigari S, Jones LK, Egner PA, Groop-man JD, Sutter CH, Roebuck BD, Guengerich FP, Kensler TW, Sutter TR. Protection against af-latoxin B1-induced cytotoxicity by expression of the cloned afatoxin B1-aldehyde reductases rat AKR7A1 and human AKR7A3. Chem Res Toxi-col. 2008;21:1134-1142.
32. Hayes JD, Judah DJ, Neal GE. Resistance to afa-toxin-B1 is associated with the expression of a novel aldo-ketoreductase which has catalytic activity towards a cytotoxic aldehyde-containing metabolite of the toxin. Cancer Res. 1993;53:3887-3894.
33. Ellis EM. Protection against afatoxin B1 in rat-a new look at the link between toxicity, carcinoge-nicity, and metabolism. Toxicol Sci. 2009;109:1-3.
34. Liao SF, Yang HI, Lee MH, Chen CJ, Lee WC. Fifteen-year population attributable fractions and causal pies of risk factors for newly developed he-patocellular carcinomas in 11,801 men in Taiwan. PLoS One. 2012;7:e34779.
35. Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D. Human afatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr. 2004;80:1106-1122.
36. Liu Y, Wu F. Global burden of afatoxin-induced hepatocellular carcinoma: a risk assessment. Environ Health Perspect. 2010;118:818-824.
37. Hsu A, Lai CL, Yuen MF. Update on the risk of he-patocellular carcinoma in chronic hepatitis B virus infection. Curr Hepatitis Rep. 2011;10:106-111.
38. Raisuddin S, Singh KP, Zaidi SIA, Paul BN, Ray PK. Immunosuppressive effects of afatoxin in growing rats. Mycopathologia. 1993;124:189-194.
39. Plymoth A, Viviani S, Hainaut P. Control of hepato-cellular carcinoma through hepatitis B vaccination in areas of high endemicity: perspectives for global liver cancer prevention. Cancer Lett. 2009;286:15-21.
40. Kuniholm MH, Lesi OA, Mendy M, Akano AO, Sam O, Hall AJ, Whittle H, Bah E, Goedert JJ, Hainaut P, Kirk GD. Afatoxin exposure and viral hepatitis in the etiology of liver cirrhosis in the Gambia, West Africa. Environ Health Perspect. 2008;116:1553-1557.
41. Amundson SA, Myers TG, Fornace AJ. Roles for p53 in growth arrest and apoptosis: putting on the brakes after genotoxic stress. Oncogene. 1998;17:3287-3299.
42. Zhang YJ. Interactions of chemical carcinogens and genetic variation in hepatocellular carcinoma. World J Hepatol. 2010;2:94-102.
43. Hussain SP, Aquilar F, Amstad P, Cerutti P. Oxy-radical induced mutagenesis of hotspot codons 248 and 249 of the human p53 gene. Oncogene. 1994;9:2277-2281.
44. Ohshima H, Bartsch H. Chronic infection and in-fammatory processes as cancer risk factors: possible role for nitric oxide in carcinogenesis. Mutat Res. 1994;305:253-264.
45. Sell S, Hunt J, Dunsford H, Chisar F. Synergy between hepatitis B virus expression and chemical hepatocarcinogens in transgenic mice. Cancer Res. 1991;51:1278-1285.
46. Kew MC. Synergistic interaction between afatoxin B1 and hepatitis B virus in hepatocarcinogenesis. Liver Int. 2003;23:405-409.
47. Liu ZM, Li LQ, Peng MH, Liu TW, Qin Z, Guo Y, Xiao KY, Ye XP, Mo XS, Qin X, Li S, Yan LN, Shen HM, Wang LW, Wang Q, Wang Kai-bo, Liang Ren-Xiang, Wei Zong-Liang, Ong CN, Santella RM, Peng T. Hepatitis B virus infection contributes to oxidative stress in a population exposed to afatoxin B1 and high-risk for hepatocellular carcinoma. Cancer Lett. 2008;263:212-22.
48. Qian GS, Ross RK, Yu MC. A follow-up study of urinary markers of afatoxin exposure and liver cancer risk in Shanghai, People's Republic of China. Cancer Epidemiol Biomarkers Prev. 1994;3:3-10.
49. Mizrak D, Engin B, Onder FO, Yener B, Bektaş M, Biyikli Z, Idilman R, Cinar K, Karayalçin K, Ersöz S, Karayalçin S, Ozden A, Yurdaydin C, Yazihan N, Ataoǧlu H, Bozkaya H, Uzunalimoǧlu O. Afatoxin exposure in viral hepatitis patients in Turkey. Turk J Gastroenterol. 2009;20:192-197.
50. Turner PC, Mendy M, Whittle H, Fortuin M, Hall AJ, Wild CP. Hepatitis B infection and afatoxin biomarker levels in Gambian children. Trop Med Int Health. 2000;5:837-841.
51. Murugavel KG, Naranatt PP, Shankar EM, Mathews S, Raghuram K, Rajasambandam P, Jayanthi V, Surendran R, Murali A, Srinivas U, Palaniswamy KR, Srikumari D, Thyagarajan SP. Prevalence of afatoxin B1 in liver biopsies of proven hepato-cellular carcinoma in India determined by an in-house immunoperoxidase test. J Med Microbiol. 2007;56(Pt 11):1455-1459.
52. Park US, Su JJ, Ban KC, Qin L, Lee EH, Lee YI. Mutations in the p53 tumour suppressor gene in tree shrew hepatocellular carcinoma associated with hepatitis B virus infection and intake of afa-toxin B1. Gene. 2000;251:73-80.
53. Feitelson MA. Hepatitis B virus in hepatocarcino-genesis. J Cell Physiol. 1999;181:188-202.
54. Kew MC. Hepatitis B virus X protein in the patho-genesis of hepatitis B virus-induced hepatocellular carcinoma. J Gastroenterol Hepatol. 2011;26(Suppl 1):144-152.
55. Chang MH. Decreasing incidence of hepatocellu-lar carcinoma among children following universal hepatitis B immunization. Liver Int. 2003;23:309-14.
56. Kew MC. Prevention of hepatocellular carcinoma. HPB (Oxford). 2005;7:16-25.
57. Turner PC, Sylla A, Diallo MS, Castegnaro JJ, Hall AJ, Wild CP. The role of afatoxins and hepatitis viruses in the etiopathogenesis of hepatocellular carcinoma: a basis for primary prevention in Guinea-Conakry, West Africa. J Gastroenterol Hepatol. 2002;17(Suppl S4):S441-S448.
58. Chen DS. Hepatitis C virus in chronic liver disease and hepatocellular carcinoma in Taiwan. Princess Takamatsu Symp. 1995;25:27-32.
59. But DYK, Lai CL, Yuen MF. Natural history of hepatitis-related hepatocellular carcinoma. World J Gastroenterol. 2008;14:1652-1656.
60. Sheikh MY, Choi J, Qadri I. Hepatitis C virus infection: molecular pathways to metabolic syndrome. Hepatology. 2008;47:2127-2133.
61. Seeff LB, Hoofnagle JH. Epidemiology of hepato-cellular carcinoma in areas of low hepatitis B and hepatitis C endemicity. Oncogene. 2006;25:3771-3777.
62. Lopez JB. Recent developments in the frst detection of hepatocellular carcinoma. Clin Biochem Rev. 2005;26:65-79.
63. Poynard T, Yuen MF, Ratziu V, Lai CL. Viral hepatitis C. Lancet. 2003;362:2095-2100.
64. Brechot C. Molecular mechanisms of hepatitis B and C viruses related to liver carcinogenesis. Hepa-togastroenterology. 1998;45(Suppl 3):1189-1196.
65. Raptis I, Koskinas J, Emmanouil T, Hadziyannis S. Changing relative roles of hepatitis B and C viruses in the aetiology of hepatocellular carcinoma in Greece: epidemiological and clinical observations. J Viral Hepat. 2003;10:450-454.
66. Di Bisceglie AM, Lyra AC, Schwartz M, Reddy RK, Martin P, Gores G, Lok AS, Hussain KB, Gish R, Van Thiel DH, Younossi Z, Tong M, Hassanein T, Balart L, Fleckenstein J, Flamm S, Blei A, Be-feler AS; Liver Cancer Network. Hepatitis C-relat-ed hepatocellular carcinoma in the United States: infuence of ethnic status. Am J Gastroenterol. 2003;98:2060-2063.
67. Zhao H, Wang J, Han Y, Huang Z, Ying J, Bi X, Zhao J, Fang Y, Zhou H, Zhou J, Li Z, Zhang Y, Yang X, Yan T, Wang L, Torbenson MS, Cai J. ARID2: a new tumour suppressor gene in hepato-cellular carcinoma. Oncotarget. 2011;2:886-891.
68. Kew MC. Hepatitis C virus and hepatocellular carcinoma in developing and developed countries. Vir Hepatit Rev. 1998;4:259-269.
69. Liaw YF. Role of hepatitis C virus in dual and triple hepatitis virus infection. Hepatology. 1995;22(4 Pt 1):1101-1108.
70. Fujita N, Sugimoto R, Ma N, Tanaka H, Iwasa M, Kobayashi Y, Kawanishi S, Watanabe S, Kaito M, Takei Y. Comparison of hepatic oxidative DNA damage in patients with chronic hepatitis B and C. J Viral Hepat. 2008;15:498-507.
71. Sato S, Fujiyama S, Tanaka M, Yamasaki K, Kuramoto I, Kawano S, Sato T, Mizuno K, Non-aka S. Coinfection of hepatitis C virus in patients with chronic hepatitis B infection. J Hepatol. 1994;21:159-166.
72. Abdel-Hafz HA. Role of hepatitis B virus x protein in DNA repair during hepatocellular carcinoma development. J Carcinogene Mutagene. 2011;S3:001.
73. Oyagbemi AA, Azeez OI, Saba AB. Hepatocellu-lar carcinoma and the underlying mechanisms. Afr Health Sci. 2010;10:93-98.
74. Wild CP, Montesano R. A model of interaction: af-latoxins and hepatitis viruses in liver cancer aetiology and prevention. Cancer Lett. 2009;286:22-28.
75. Wu F, Khlangwiset P. Health economic impacts and cost-effectiveness of afatoxin reduction strategies in Africa: case studies in biocontrol and post-harvest interventions. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2010;27:496-509.
76. Wild CP, Hall AJ. Primary prevention of hepato-cellular carcinoma in developing countries. Mutat Res. 2000;462:381-393.
77. Wong ZA, Wei CI, Rice DW, Hsieh DP. Effects of phenobarbital pretreatment on the metabolism and toxicokinetics of afatoxin B1 in the rhesus monkey. Toxicol Appl Pharmacol. 1981;60:387-397.
78. Yang CF, Liu J, Wasser S, Shen HM, Tan CE, Ong CN. Inhibition of ebselen on afatoxinB1-induced hepatocarcinogenesis in Fischer 344 rats. Carcino-genesis. 2000;12:2237-2243.
79. Wattenberg LW. Chemoprevention of cancer. Cancer Res. 1985;45:1-8.
80. Liu YL, Roebuck BD, Yager JD, Groopman JD, Kensler TW. Protection by 5-(2- pyrazinyl)-4-methyl-1, 2-dithiol-3-thione (oltipraz) against the hepatotoxicity of afatoxin B1 in the rat. Toxicol Appl Pharmacol. 1988;93:442-451.
81. Lee JS, Surh YJ. Nrf2 as a novel molecular target for chemoprevention. Cancer Lett. 2005;224:171-84.
82. Langouet S, Furge LL, Kerriguy N, Nakamura K, Guillouzo A, Guengerich FP. Inhibition of human cytochrome P450 enzymes by 1,2-dithiole-3-thione, oltipraz and its derivatives, and sulforaphane. Chem Res Toxicol. 2000;13:245-252.
83. Langouet S, Coles B, Morel F, Becquemont L, Beaune P, Guengerich FP, Ketterer B, Guillouzo A. Inhibition of CYP1A2 and CYP3A4 by oltipraz results in reduction of afatoxin B1 metabolism in human hepatocytes in primary culture. Cancer Res. 1995;55:5574-5549.
84. Farombi EO, Hansen M, Ravn-Haren G, Moller P, Dragsted LO. Commonly consumed and naturally occurring dietary substances affect biomarkers of oxidative stress and DNA damage in healthy rats. Food Chem Toxicol. 2004;42:1315-1322.
85. Farombi EO, Akanni OO, Emerole GO. Antioxida-tive and scavenging activities of kolaviron in vitro. Pharm Biol. 2002;40:107-116.
86. Farombi EO, Tahnteng JG, Agboola AO, Nwank-wo JO, Emerole GO. Chemoprevention of 2-acet-ylaminofuorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron--a Garcinia kola seed extract. Food Chem Toxicol. 2000;38:535-541.
87. Farombi EO. Mechanisms for the hepatoprotec-tive action of kolaviron: studies on hepatic enzymes, microsomal lipids and lipid peroxidation in carbon tetrachloride-treated rats. Pharmacol Res. 2000;42:75-80.
88. Farombi EO, Moller P, Dragsted LO. Ex vivo and in vitro protective effects of kolaviron against oxygen-derived radical-induced DNA damage and oxi-dative stress in human lymphocytes and rat-liver cells. Cell Biol Toxicol. 2004;20:71-82.
89. Abbas HK, editor. Afatoxin and food safety. Boca Raton, FL: CRC Press; 2005.
90. Obuseh FA, Jolly PE, Kulczycki A, Ehiri J, Water-bor J, Desmond RA, Preko PO, Jiang Y, Piyathilake CJ. Afatoxin levels, plasma vitamins A and E concentrations, and their association with HIV and hepatitis B virus infections in Ghanaians: a cross-sectional study. J Int AIDS Soc. 2011;14:53.