Liver-Specific Expressions of HBx and src in the p53 Mutant Trigger Hepatocarcinogenesis in Zebrafish

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Lu, Jeng Wei ^a,b   Yang, Wan Yu ^a   Tsai, Su Mei ^a   Lin, Yueh Min ^c,d   Chang, Pen Heng ^e   Chen, Jim Ray ^f,g   Wang, Horng Dar ^h   Wu, Jen Leih ⁱ   Jin, Shiow Lian Catherine ^b   Yuh, Chiou Hwa ^a,h,j  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^c CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^d JEN TEH JUNIOR COLLEGE OF MEDICINE   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^f CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^g CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^h NATIONAL TSING HUA UNIVERSITY   (Taiwan)

ⁱ INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

^j NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN; HEPATITIS B VIRUS X ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PROTEIN KINASE B; PROTEIN P53; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG; VASCULOTROPIN; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER STAGING; CONTROLLED STUDY; DRUG SCREENING; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENE FUNCTION; GENE MUTATION; GLYCOGEN METABOLISM; IN VIVO STUDY; LIPID METABOLISM; LIPOGENESIS; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER HYPERPLASIA; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TRANSGENIC ANIMAL; UPREGULATION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CARCINOGENESIS; CARCINOMA, HEPATOCELLULAR; CELL CYCLE; ENZYME ACTIVATION; FIBROSIS; GENE EXPRESSION; GLYCOGEN; HUMANS; HYPERPLASIA; LIPOGENESIS; LIVER; LIVER NEOPLASMS; MUTATION; NEOPLASM METASTASIS; ORGAN SPECIFICITY; PROLIFERATING CELL NUCLEAR ANTIGEN; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANS-ACTIVATORS; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH;

EID: 84885123381     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076951     Document Type: Article

References (72)

1. El-Serag HB, Rudolph KL, (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132: 2557-2576. doi:10.1053/j.gastro.2007.04.061. PubMed: 17570226.
2. Marrero CR, Marrero JA, (2007) Viral hepatitis and hepatocellular carcinoma. Arch Med Res 38: 612-620. doi:10.1016/j.arcmed.2006.09.004. PubMed: 17613352.
3. McGlynn KA, London WT, (2005) Epidemiology and natural history of hepatocellular carcinoma. Best Pract Res Clin Gastroenterol 19: 3-23. doi:10.1016/j.bpg.2004.10.004. PubMed: 15757802.
4. Seeff LB, Hoofnagle JH, (2006) Epidemiology of hepatocellular carcinoma in areas of low hepatitis B and hepatitis C endemicity. Oncogene 25: 3771-3777. doi:10.1038/sj.onc.1209560. PubMed: 16799618.
5. Hussain SP, Schwank J, Staib F, Wang XW, Harris CC, (2007) TP53 mutations and hepatocellular carcinoma: insights into the etiology and pathogenesis of liver cancer. Oncogene 26: 2166-2176. doi:10.1038/sj.onc.1210279. PubMed: 17401425.
6. Seifer M, Höhne M, Schaefer S, Gerlich WH, (1991) In vitro tumorigenicity of hepatitis B virus DNA and HBx protein. J Hepatol 13 (Suppl 4):: S61-S65. doi:10.1016/0168-8278(91)91234-8. PubMed: 1822516.
7. Wu BK, Li CC, Chen HJ, Chang JL, Jeng KS, et al. (2006) Blocking of G1/S transition and cell death in the regenerating liver of Hepatitis B virus X protein transgenic mice. Biochem Biophys Res Commun 340: 916-928. doi:10.1016/j.bbrc.2005.12.089. PubMed: 16403455.
8. Kim CM, Koike K, Saito I, Miyamura T, Jay G, (1991) HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 351: 317-320. doi:10.1038/351317a0. PubMed: 2034275.
9. Shieh YS, Chang YS, Hong JR, Chen LJ, Jou LK, et al. (2010) Increase of hepatic fat accumulation by liver specific expression of Hepatitis B virus X protein in zebrafish. Biochim Biophys Acta 1801: 721-730. doi:10.1016/j.bbalip.2010.04.008. PubMed: 20416398.
10. Liu W, Chen JR, Hsu CH, Li YH, Chen YM, et al. (2012) A zebrafish model of intrahepatic cholangiocarcinoma by dual expression of hepatitis B virus X and hepatitis C virus core protein in liver. Hepatology.
11. Lu JW, Yang WY, Lin YM, Jin SL, Yuh CH, (2013) Hepatitis B virus X antigen and aflatoxin B1 synergistically cause hepatitis, steatosis and liver hyperplasia in transgenic zebrafish. Acta Histochem, 115: 728-39. PubMed: 23499292.
12. Spitsbergen JM, Tsai HW, Reddy A, Miller T, Arbogast D, et al. (2000) Neoplasia in zebrafish (Danio rerio) treated with 7,12-dimethylbenz[a]anthracene by two exposure routes at different developmental stages. Toxicol Pathol 28: 705-715. doi:10.1177/019262330002800511. PubMed: 11026607.
13. Lam SH, Wu YL, Vega VB, Miller LD, Spitsbergen J, et al. (2006) Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat Biotechnol 24: 73-75. doi:10.1038/nbt1169. PubMed: 16327811.
14. Goessling W, North TE, Zon LI, (2007) Ultrasound biomicroscopy permits in vivo characterization of zebrafish liver tumors. Nat Methods 4: 551-553. doi:10.1038/nmeth1059. PubMed: 17572681.
15. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Parinov S, et al. (2012) An inducible kras(V12) transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis Model. J Mech 5: 63-72.
16. Lu JW, Hsia Y, Yang WY, Lin YI, Li CC, et al. (2012) Identification of the common regulators for hepatocellular carcinoma induced by hepatitis B virus X antigen in a mouse model. Carcinogenesis 33: 209-219. doi:10.1093/carcin/bgr224. PubMed: 22021908.
17. Summy JM, Gallick GE, (2003) Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev 22: 337-358. doi:10.1023/A:1023772912750. PubMed: 12884910.
18. Tseng WF, Jang TH, Huang CB, Yuh CH, (2011) An evolutionarily conserved kernel of gata5, gata6, otx2 and prdm1a operates in the formation of endoderm in zebrafish. Dev Biol 357: 541-557. doi:10.1016/j.ydbio.2011.06.040. PubMed: 21756893.
19. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236: 3088-3099. doi:10.1002/dvdy.21343. PubMed: 17937395.
20. Tsai SM, Liu DW, Wang WP, (2013) Fibroblast growth factor (Fgf) signaling pathway regulates liver homeostasis in zebrafish. Transgenic Res 22: 301-314. doi:10.1007/s11248-012-9636-9. PubMed: 22820869.
21. Zhu S, Lee JS, Guo F, Shin J, Perez-Atayde AR, et al. (2012) Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell 21: 362-373. doi:10.1016/j.ccr.2012.02.010. PubMed: 22439933.
22. Her GM, Yeh YH, Wu JL, (2003) 435-bp liver regulatory sequence in the liver fatty acid binding protein (L-FABP) gene is sufficient to modulate liver regional expression in transgenic zebrafish. Dev Dyn 227: 347-356. doi:10.1002/dvdy.10324. PubMed: 12815620.
23. Hsia CC, Kleiner DE Jr., Axiotis CA, Di Bisceglie A, Nomura AM, et al. (1992) Mutations of p53 gene in hepatocellular carcinoma: roles of hepatitis B virus and aflatoxin contamination in the diet. J Natl Cancer Inst 84: 1638-1641. doi:10.1093/jnci/84.21.1638. PubMed: 1279184.
24. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, et al. (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci U S A 102: 407-412. doi:10.1073/pnas.0406252102. PubMed: 15630097.
25. Soussi T, Béroud C, (2003) Significance of TP53 mutations in human cancer: a critical analysis of mutations at CpG dinucleotides. Hum Mutat 21: 192-200. doi:10.1002/humu.10189. PubMed: 12619105.
26. Boorman GA, Botts S, Bunton TE, Fournie JW, Harshbarger JC, et al. (1997) Diagnostic criteria for degenerative, inflammatory, proliferative nonneoplastic and neoplastic liver lesions in medaka (Oryzias latipes): consensus of a National Toxicology Program Pathology Working Group. Toxicol Pathol 25: 202-210. doi:10.1177/019262339702500210. PubMed: 9125779.
27. Hobbie KR, DeAngelo AB, George MH, Law JM, (2012) Neoplastic and nonneoplastic liver lesions induced by dimethylnitrosamine in Japanese medaka fish. Vet Pathol 49: 372-385. doi:10.1177/0300985811409443. PubMed: 21724976.
28. Lau GM, Yu GL, Gelman IH, Gutowski A, Hangauer D, et al. (2009) Expression of Src and FAK in hepatocellular carcinoma and the effect of Src inhibitors on hepatocellular carcinoma in vitro. Dig Dis Sci 54: 1465-1474. doi:10.1007/s10620-008-0519-0. PubMed: 18979199.
29. Li D, Yang P, Li H, Cheng P, Zhang L, et al. (2012) MicroRNA-1 inhibits proliferation of hepatocarcinoma cells by targeting endothelin-1. Life Sci 91: 440-447. doi:10.1016/j.lfs.2012.08.015. PubMed: 22963810.
30. Li Z, Huang X, Zhan H, Zeng Z, Li C, et al. (2012) Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J Hepatol 56: 419-425. doi:10.1016/j.jhep.2011.07.025. PubMed: 21888874.
31. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Lam SH, et al. (2011) A high level of liver-specific expression of oncogenic Kras(V12) drives robust liver tumorigenesis in transgenic zebrafish. Dis Model. J Mech 4: 801-813.
32. Chen CJ, Yu MW, Liaw YF, (1997) Epidemiological characteristics and risk factors of hepatocellular carcinoma. J Gastroenterol Hepatol 12: S294-S308. doi:10.1111/j.1440-1746.1997.tb00513.x. PubMed: 9407350.
33. Neuveut C, Wei Y, Buendia MA, (2010) Mechanisms of HBV-related hepatocarcinogenesis. J Hepatol 52: 594-604. doi:10.1016/j.jhep.2009.10.033. PubMed: 20185200.
34. Cougot D, Neuveut C, Buendia MA, (2005) HBV induced carcinogenesis. J Clin Virol 34 (Suppl 1):: S75-S78. doi:10.1016/S1386-6532(05)80014-9. PubMed: 16461228.
35. Lu JW, Hsia Y, Tu HC, Hsiao YC, Yang WY, et al. (2011) Liver development and cancer formation in zebrafish. Birth Defects Res C Embryo TODAY 93: 157-172. doi:10.1002/bdrc.20205. PubMed: 21671355.
36. Kim KH, Shin HJ, Kim K, Choi HM, Rhee SH, et al. (2007) Hepatitis B virus X protein induces hepatic steatosis via transcriptional activation of SREBP1 and PPARgamma. Gastroenterology 132: 1955-1967. doi:10.1053/j.gastro.2007.03.039. PubMed: 17484888.
37. Koo JS, Seong JK, Park C, Yu DY, Oh BK, et al. (2005) Large liver cell dysplasia in hepatitis B virus x transgenic mouse liver and human chronic hepatitis B virus-infected liver. Intervirology 48: 16-22. doi:10.1159/000082090. PubMed: 15785085.
38. Lakhtakia R, Kumar V, Reddi H, Mathur M, Dattagupta S, et al. (2003) Hepatocellular carcinoma in a hepatitis B 'x' transgenic mouse model: A sequential pathological evaluation. J Gastroenterol Hepatol 18: 80-91. doi:10.1046/j.1440-1746.2003.02902.x. PubMed: 12519229.
39. Ueda H, Ohkoshi S, Harris C, Jay G, (1995) Synergism between the hbx gene and aflatoxin B-1 in the development of murine liver-cancer. Int J Oncol 7: 735-740. PubMed: 21552896.
40. Yu DY, Moon HB, Son JK, Jeong S, Yu SL, et al. (1999) Incidence of hepatocellular carcinoma in transgenic mice expressing the hepatitis B virus X-protein. J Hepatol 31: 123-132. doi:10.1016/S0168-8278(99)80172-X. PubMed: 10424292.
41. Wang Y, Cui F, Lv Y, Li C, Xu X, et al. (2004) HBsAg and HBx knocked into the p21 locus causes hepatocellular carcinoma in mice. Hepatology 39: 318-324. doi:10.1002/hep.20076. PubMed: 14767984.
42. Liu W, Chen JR, Hsu CH, Li YH, Chen YM, et al. (2012) A zebrafish model of intrahepatic cholangiocarcinoma by dual expression of hepatitis B virus X and hepatitis C virus core protein in liver. Hepatology 56: 2268-2276. doi:10.1002/hep.25914. PubMed: 22729936.
43. Park SG, Min JY, Chung C, Hsieh A, Jung G, (2009) Tumor suppressor protein p53 induces degradation of the oncogenic protein HBx. Cancer Lett 282: 229-237. doi:10.1016/j.canlet.2009.03.019. PubMed: 19375220.
44. Xian L, Zhao J, Wang J, Fang Z, Peng B, et al. (2010) p53 Promotes proteasome-dependent degradation of oncogenic protein HBx by transcription of MDM2. Mol Biol Rep 37: 2935-2940. doi:10.1007/s11033-009-9855-1. PubMed: 19842060.
45. Gouas DA, Shi H, Hautefeuille AH, Ortiz-Cuaran SL, Legros PC, et al. (2010) Effects of the TP53 p.R249S mutant on proliferation and clonogenic properties in human hepatocellular carcinoma cell lines: interaction with hepatitis B virus X protein. Carcinogenesis 31: 1475-1482. doi:10.1093/carcin/bgq118. PubMed: 20538734.
46. Knoll S, Fürst K, Thomas S, Villanueva Baselga S, Stoll A, et al. (2011) Dissection of cell context-dependent interactions between HBx and p53 family members in regulation of apoptosis: a role for HBV-induced HCC. Cell Cycle 10: 3554-3565. doi:10.4161/cc.10.20.17856. PubMed: 22030623.
47. Chan C, Wang Y, Chow PK, Chung AY, Ooi LL, et al. (2013) Altered binding site selection of p53 transcription cassettes by hepatitis B virus X protein. Mol Cell Biol 33: 485-497. doi:10.1128/MCB.01189-12. PubMed: 23149944.
48. Gouas DA, Villar S, Ortiz-Cuaran S, Legros P, Ferro G, et al. (2012) TP53 R249S mutation, genetic variations in HBX and risk of hepatocellular carcinoma in The Gambia. Carcinogenesis 33: 1219-1224. doi:10.1093/carcin/bgs135. PubMed: 22759751.
49. Ortiz-Cuaran S, Villar S, Gouas D, Ferro G, Plymoth A, et al. (2013) Association between HBX status, aflatoxin-induced R249S TP53 mutation and risk of hepatocellular carcinoma in a case-control study from Thailand. Cancer Lett 331: 46-51. doi:10.1016/j.canlet.2012.11.012. PubMed: 23200676.
50. Guerrieri F, Belloni L, Pediconi N, Levrero M, (2013) Molecular mechanisms of HBV-associated hepatocarcinogenesis. Semin Liver Dis 33: 147-156. doi:10.1055/s-0033-1345721. PubMed: 23749671.
51. Lara-Pezzi E, Roche S, Andrisani OM, Sánchez-Madrid F, López-Cabrera M, (2001) The hepatitis B virus HBx protein induces adherens junction disruption in a src-dependent manner. Oncogene 20: 3323-3331. doi:10.1038/sj.onc.1204451. PubMed: 11423982.
52. Cha MY, Kim CM, Park YM, Ryu WS, (2004) Hepatitis B virus X protein is essential for the activation of Wnt/beta-catenin signaling in hepatoma cells. Hepatology 39: 1683-1693. doi:10.1002/hep.20245. PubMed: 15185310.
53. Chen J, Siddiqui A, (2007) Hepatitis B virus X protein stimulates the mitochondrial translocation of Raf-1 via oxidative stress. J Virol 81: 6757-6760. doi:10.1128/JVI.00172-07. PubMed: 17428866.
54. Chiu CM, Yeh SH, Chen PJ, Kuo TJ, Chang CJ, et al. (2007) Hepatitis B virus X protein enhances androgen receptor-responsive gene expression depending on androgen level. Proc Natl Acad Sci U S A 104: 2571-2578. doi:10.1073/pnas.0609498104. PubMed: 17259306.
55. Patton EE, Widlund HR, Kutok JL, Kopani KR, Amatruda JF, et al. (2005) BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr Biol 15: 249-254. doi:10.1016/j.cub.2005.01.031. PubMed: 15694309.
56. Zhuang D, Mannava S, Grachtchouk V, Tang WH, Patil S, et al. (2008) C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene 27: 6623-6634. doi:10.1038/onc.2008.258. PubMed: 18679422.
57. Puisieux A, Ozturk M, (1997) TP53 and hepatocellular carcinoma. Pathol Biol (Paris) 45: 864-870.
58. Schilling T, Kairat A, Melino G, Krammer PH, Stremmel W, et al. (2010) Interference with the p53 family network contributes to the gain of oncogenic function of mutant p53 in hepatocellular carcinoma. Biochem Biophys Res Commun 394: 817-823. doi:10.1016/j.bbrc.2010.03.082. PubMed: 20233581.
59. Woo HG, Wang XW, Budhu A, Kim YH, Kwon SM, et al. (2011) Association of TP53 mutations with stem cell-like gene expression and survival of patients with hepatocellular carcinoma. Gastroenterology 140: 1063-1070. doi:10.1053/j.gastro.2010.11.034. PubMed: 21094160.
60. Dovey M, White RM, Zon LI, (2009) Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 6: 397-404. doi:10.1089/zeb.2009.0606. PubMed: 19954345.
61. Sánchez-Bailón MP, Calcabrini A, Gómez-Domínguez D, Morte B, Martín-Forero E, et al. (2012) Src kinases catalytic activity regulates proliferation, migration and invasiveness of MDA-MB-231 breast cancer cells. Cell Signal 24: 1276-1286. doi:10.1016/j.cellsig.2012.02.011. PubMed: 22570868.
62. Ito Y, Kawakatsu H, Takeda T, Sakon M, Nagano H, et al. (2001) Activation of c-Src gene product in hepatocellular carcinoma is highly correlated with the indices of early stage phenotype. J Hepatol 35: 68-73. doi:10.1016/S0168-8278(01)00077-0. PubMed: 11495044.
63. Masaki T, Okada M, Shiratori Y, Rengifo W, Matsumoto K, et al. (1998) pp60c-src activation in hepatocellular carcinoma of humans and LEC rats. Hepatology 27: 1257-1264. doi:10.1002/hep.510270511. PubMed: 9581679.
64. Irby RB, Yeatman TJ, (2000) Role of Src expression and activation in human cancer. Oncogene 19: 5636-5642. doi:10.1038/sj.onc.1203912. PubMed: 11114744.
65. Shields DJ, Murphy EA, Desgrosellier JS, Mielgo A, Lau SK, et al. (2011) Oncogenic Ras/Src cooperativity in pancreatic neoplasia. Oncogene 30: 2123-2134. doi:10.1038/onc.2010.589. PubMed: 21242978.
66. Summy JM, Gallick GE, (2006) Treatment for advanced tumors: SRC reclaims center stage. Clin Cancer Res 12: 1398-1401. doi:10.1158/1078-0432.CCR-05-2692. PubMed: 16533761.
67. Klein NP, Schneider RJ, (1997) Activation of Src family kinases by hepatitis B virus HBx protein and coupled signaling to Ras. Mol Cell Biol 17: 6427-6436. PubMed: 9343405.
68. Park SS, Eom YW, Kim EH, Lee JH, Min DS, et al. (2004) Involvement of c-Src kinase in the regulation of TGF-beta1-induced apoptosis. Oncogene 23: 6272-6281. doi:10.1038/sj.onc.1207856. PubMed: 15208664.
69. Thompson KJ, Lau KN, Johnson S, Martinie JB, Iannitti DA, et al. (2011) Leptin inhibits hepatocellular carcinoma proliferation via p38-MAPK-dependent signalling. HPB (Oxf) 13: 225-233. doi:10.1111/j.1477-2574.2010.00259.x. PubMed: 21418127.
70. Ma J, Xie SL, Geng YJ, Jin S, Wang GY, et al. (2013) In vitro regulation of hepatocellular carcinoma cell viability, apoptosis, invasion, and AEG-1 expression by LY294002. Clin Res Hepatol. Gastroenterologist.
71. Wang C, Cigliano A, Delogu S, Armbruster J, Dombrowski F, et al. (2013) Functional crosstalk between AKT/mTOR and Ras/MAPK pathways in hepatocarcinogenesis: Implications for the treatment of human liver cancer. Cell Cycle 12: 1999-2010. doi:10.4161/cc.25099. PubMed: 23759595.
72. Muntané J, De la Rosa AJ, Docobo F, García-Carbonero R, Padillo FJ, (2013) Targeting tyrosine kinase receptors in hepatocellular carcinoma. Curr Cancer Drug Targets 13: 300-312. doi:10.2174/15680096113139990075. PubMed: 23016985.