Suppression of hepatocellular carcinoma proliferation and hepatitis B surface antigen secretion with interferon-λ1 or PEG-interferon-λ1

FASEB Journal

Volumn 28, Issue 8, 2014, Pages 3528-3539

  Tian, Shuo ^a   Hui, Xiwu ^a,b   Fan, Zhenzhen ^a   Li, Qinshan ^a   Zhang, Junwen ^a   Yang, Xia ^a   Ma, Xiaoli ^a   Huang, Bingren ^a   Chen, Deng ^a   Chen, Hong ^a  

^a PEKING UNION MEDICAL COLLEGE   (China)

^b CSPC ZhongQi Pharmaceutical Technology (Shijiazhuang) Co Ltd   (China)

Author keywords

Antitumor therapy; Tumor apoptosis

Indexed keywords

DOXORUBICIN; HEPATITIS B SURFACE ANTIGEN; INTERLEUKIN 29; JANUS KINASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEGINTERFERON LAMBDA; STAT1 PROTEIN; STAT2 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ANTIVIRAL ACTIVITY; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG HALF LIFE; DRUG MEGADOSE; DRUG TOLERABILITY; FEMALE; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL CARCINOMA; MAXIMUM PLASMA CONCENTRATION; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TIME TO MAXIMUM PLASMA CONCENTRATION; TUMOR XENOGRAFT;

ANTITUMOR THERAPY; TUMOR APOPTOSIS;

ADENOCARCINOMA; ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HEPATITIS B; HEPATITIS B SURFACE ANTIGENS; HUMANS; INTERLEUKIN-10 RECEPTOR BETA SUBUNIT; INTERLEUKINS; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; POLYETHYLENE GLYCOLS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84905251478     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-250704     Document Type: Article

References (46)

1. Michielsen, P., and Ho, E. (2011) Viral hepatitis B and hepatocellular carcinoma. Acta Gastroenterol. Belg. 74, 4-8
2. El-Serag, H. B. (2012) Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142, 1264-1273
3. Nguyen, V. T., Law, M. G., and Dore, G. J. (2009) Hepatitis B-related hepatocellular carcinoma: epidemiological characteristics and disease burden. J. Viral Hepat. 16, 453-463
4. Marcellin, P., Asselah, T., and Boyer, N. (2005) Treatment of chronic hepatitis B. J. Viral. Hepat. 12, 333-345 (Pubitemid 40961472)
5. Lok, A. S., and McMahon, B. J. (2007) Chronic hepatitis B. Hepatology 45, 507-539 (Pubitemid 46374607)
6. Lin, S. M., Sheen, I. S., Chien, R. N., Chu, C. M., and Liaw, Y. F. (1999) Long-term beneficial effect of interferon therapy in patients with chronic hepatitis B virus infection. Hepatology 29, 971-975
7. Lee, D., Chung, Y. H., Lee, S. H., Kim, S. E., Lee, Y. S., Kim, K. M., Lim, Y. S., Lee, H. C., Lee, Y. S., and Yu, E. (2012) Effect of response to interferon-alpha therapy on the occurrence of hepatocellular carcinoma in patients with chronic hepatitis B. Dig. Dis. 30, 568-573
8. Ikeda, K., Kobayashi, M., Saitoh, S., Someya, T., Hosaka, T., Akuta, N., Suzuki, Y., Suzuki, F., Tsubota, A., Arase, Y., and Kumada, H. (2005) Significance of hepatitis B virus DNA clearance and early prediction of hepatocellular carcinogenesis in patients with cirrhosis undergoing interferon therapy: long-term follow up of a pilot study. J. Gastroenterol. Hepatol. 20, 95-102 (Pubitemid 40143640)
9. Someya, T., Ikeda, K., Saitoh, S., Kobayashi, M., Hosaka, T., Sezaki, H., Akuta, N., Suzuki, F., Suzuki, Y., Arase, Y., and Kumada, H. (2006) Interferon lowers tumor recurrence rate after surgical resection or ablation of hepatocellular carcinoma: a pilot study of patients with hepatitis B virus-related cirrhosis. J. Gastroenterol. 41, 1206-1213 (Pubitemid 46487211)
10. Kotenko, S. V., Gallagher, G., Baurin, V. V., Lewis-Antes, A., Shen, M., Shah, N. K., Langer, J. A., Sheikh, F., Dickensheets, H., and Donnelly, R. P. (2003) IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4, 69-77 (Pubitemid 36109115)
11. Sheppard, P., Kindsvogel, W., Xu, W., Henderson, K., Schlutsmeyer, S., Whitmore, T. E., Kuestner, R., Garrigues, U., Birks, C., Roraback, J., Ostrander, C., Dong, D., Shin, J., Presnell, S., Fox, B., Haldeman, B., Cooper, E., Taft, D., Gilbert, T., Grant, F. J., Tackett, M., Krivan, W., McKnight, G., Clegg, C., Foster, D., and Klucher, K. M. (2003) IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4, 63-68 (Pubitemid 36104710)
12. Meager, A., Visvalingam, K., Dilger, P., Bryan, D., and Wadhwa, M. (2005) Biological activity of interleukins-28 and -29: comparison with type I interferons. Cytokine 31, 109-118 (Pubitemid 40910226)
13. Brand, S., Beigel, F., Olszak, T., Zitzmann, K., Eichhorst, S. T., Otte, J. M., Diebold, J., Diepolder, H., Adler, B., Auernhammer, C. J., Göke, B., and Dambacher, J. (2005) IL-28A and IL-29 mediate antiproliferative and antiviral signals in intestinal epithelial cells and murine CMV infection increases colonic IL-28A expression. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G960-G968 (Pubitemid 41532589)
14. Zhou, Z., Hamming, O. J., Ank, N., Paludan, S. R., Nielsen, A. L., and Hartmann, R. (2007) Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. J. Virol. 81, 7749-7758 (Pubitemid 47047861)
15. Doyle, S. E., Schreckhise, H., Khuu-Duong, K., Henderson, K., Rosler, R., Storey, H., Yao, L., Liu, H., Barahmand-pour, F., Sivakumar, P., Chan, C., Birks, C., Foster, D., Clegg, C. H., Wietzke-Braun, P., Mihm, S., Klucher, K. M. (2006) Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44, 896-906 (Pubitemid 46489554)
16. Sommereyns, C., Paul, S., Staeheli, P., and Michiels, T. (2008) IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 4, e1000017
17. Robek, M. D., Boyd, B. S., and Chisari, F. V. (2005) Lambda interferon inhibits hepatitis B and C virus replication. J. Virol. 79, 3851-3854 (Pubitemid 40327973)
18. Hong, S. H., Cho, O., Kim, K., Shin, H. J., Kotenko, S. V., and Park, S. (2007) Effect of interferon-lambda on replication of hepatitis B virus in human hepatoma cells. Virus Res. 126, 245-249 (Pubitemid 46726717)
19. Abushahba, W., Balan, M., Castaneda, I., Yuan, Y., Reuhl, K., Raveche, E., de la Torre, A., Lasfar, A., and Kotenko, S. V. (2010) Antitumor activity of type I and type III interferons in BNL hepatoma model. Cancer Immunol. Immunother. 59, 1059-1071
20. Miller, D. M., Klucher, K. M., Freeman, J. A., Hausman, D. F., Fontana, D., and Williams, D. E. (2009) Interferon lambda as a potential new therapeutic for hepatitis C. Ann. N. Y. Acad. Sci. 1182, 80-87
21. Muir, A. J., Shiffman, M. L., Zaman, A., Yoffe, B., de la Torre, A., Flamm, S., Gordon, S. C., Marotta, P., Vierling, J. M., Lopez-Talavera, J. C., Byrnes-Blake, K., Fontana, D., Freeman, J., Gray, T., Hausman, D., Hunder, N. N., and Lawitz, E. (2010) Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology 52, 822-832
22. Xie, Y. F., Chen, H., and Huang, B. R. (2007) Expression, purification and characterization of human IFN-lambda1 in Pichia pastoris. J. Biotechnol. 129, 472-480 (Pubitemid 46560157)
23. Hui, X., Chen, H., Zhang, S., Ma, X., Wang, X., and Huang, B. (2011) Antitumor activities of recombinant human interferon (IFN)-lambda1 in vitro and in xenograft models in vivo for colon cancer. Cancer Lett. 311, 141-151
24. Guenterberg, K. D., Grignol, V. P., Raig, E. T., Zimmerer, J. M., Chan, A. N., Blaskovits, F. M., Young, G. S., Nuovo, G. J., Mundy, B. L., Lesinski, G. B., and Carson, W. E. 3rd. (2010) Interleukin-29 binds to melanoma cells inducing Jak-STAT signal transduction and apoptosis. Mol. Cancer Ther. 9, 510-520
25. Duan, Z., Foster, R., Bell, D. A., Mahoney, J., Wolak, K., Vaidya, A., Hampel, C., Lee, H., and Seiden, M. V. (2006) Signal transducers and activators of transcription 3 pathway activation in drug-resistant ovarian cancer. Clin. Cancer Res. 12, 5055-5063 (Pubitemid 44453331)
26. Xie, T. X., Wei, D., Liu, M., Gao, A. C., Ali-Osman, F., Sawaya, R., and Huang, S. (2004) Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene 23, 3550-3560 (Pubitemid 38658421)
27. Bell, S. J., Fam, C. M., Chlipala, E. A., Carlson, S. J., Lee, J. I., Rosendahl, M. S., Doherty, D. H., and Cox, G. N. (2008) Enhanced circulating half-life and antitumor activity of a site-specific pegylated interferon-alpha protein therapeutic. Bioconjug. Chem. 19, 299-305 (Pubitemid 351213862)
28. Chae, S. Y., Kim, T. H., Park, K., Jin, C. H., Son, S., Lee, S., Youn, Y. S., Kim, K., Jo, D. G., Kwon, I. C., Chen, X., and Lee, K. C. (2010) Improved antitumor activity and tumor targeting of NH(2)-terminal-specific PEGylated tumor necrosis factor-related apoptosis-inducing ligand. Mol. Cancer Ther. 9, 1719-1729
29. Kim, T. H., Youn, Y. S., Jiang, H. H., Lee, S., Chen, X., and Lee, K. C. (2011) PEGylated TNF-related apoptosis-inducing ligand (TRAIL) analogues: pharmacokinetics and antitumor effects. Bioconjug. Chem. 22, 1631-1637
30. Wang, Y. J., Hao, S. J., Liu, Y. D., Hu, T., Zhang, G. F., Zhang, X., Qi, Q. S., Ma, G. H., and Su, Z. G. (2010) PEGylation markedly enhances the in vivo potency of recombinant human non-glycosylated erythropoietin: a comparison with glycosylated erythropoietin. J. Control Release 145, 306-313
31. Knowles, B. B., Howe, C. C., and Aden, D. P. (1980) Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science 209, 497-499
32. Chen, H. C., Chou, C. K., Sun, C. M., and Yeh, S. F. (1997) Suppressive effects of destruxin B on hepatitis B virus surface antigen gene expression in human hepatoma cells. Antiviral Res. 34, 137-144
33. Hsu, S. L., Lin, Y. F., and Chou, C. K. (1993) Retinoic acid biphasically regulates the gene expression of hepatitis B virus surface antigen in human hepatoma Hep3B cells. J. Biol. Chem. 268, 23093-23097
34. Li, Q., Kawamura, K., Ma, G., Iwata, F., Numasaki, M., Suzuki, N., Shimada, H., and Tagawa, M. (2010) Interferon-lambda induces G1 phase arrest or apoptosis in oesophageal carcinoma cells and produces anti-tumour effects in combination with anti-cancer agents. Eur. J. Cancer 46, 180-190
35. Li, W., Lewis-Antes, A., Huang, J., Balan, M., and Kotenko, S. V. (2008) Regulation of apoptosis by type III interferons. Cell. Prolif. 41, 960-979
36. Zitzmann, K., Brand, S., Baehs, S., Göke, B., Meinecke, J., Spöttl, G., Meyer, H., and Auernhammer, C. J. (2006) Novel interferon-lambdas induce antiproliferative effects in neuroendocrine tumor cells. Biochem. Biophys. Res. Commun. 344, 1334-1341
37. Parkin, D. M., Bray, F., Ferlay, J., and Pisani, P. (2005) Global cancer statistics, 2002. CA Cancer J. Clin. 55, 74-108 (Pubitemid 40372904)
38. Tanaka, M., Katayama, F., Kato, H., Tanaka, H., Wang, J., Qiao, Y. L., and Inoue, M. (2011) Hepatitis B and C virus infection and hepatocellular carcinoma in China: a review of epidemiology and control measures. J. Epidemiol. 21, 401-416
39. Jiang, D. K., Sun, J., Cao, G., Liu, Y., Lin, D., Gao, Y. Z., Ren, W. H., Long, X. D., Zhang, H., Ma, X. P., Wang, Z., Jiang, W., Chen, T. Y., Gao, Y., Sun, L. D., Long, J. R., Huang, H. X., Wang, D., Yu, H., Zhang, P., Tang, L. S., Peng, B., Cai, H., Liu, T. T., Zhou, P., Liu, F., Lin, X., Tao, S., Wan, B., Sai-Yin, H. X., Qin, L. X., Yin, J., Liu, L., Wu, C., Pei, Y., Zhou, Y. F., Zhai, Y., Lu, P. X., Tan, A., Zuo, X. B., Fan, J., Chang, J., Gu, X., Wang, N. J., Li, Y., Liu, Y. K., Zhai, K., Zhang, H., Hu, Z., Liu, J., Yi, Q., Xiang, Y., Shi, R., Ding, Q., Zheng, W., Shu, X. O., Mo, Z., Shugart, Y. Y., Zhang, X. J., Zhou, G., Shen, H., Zheng, S. L., Xu, J., and Yu, L. (2013) Genetic variants in STAT4 and HLA-DQ genes confer risk of hepatitis B virus-related hepatocellular carcinoma. Nat. Genet. 45, 72-75
40. Qu, L. S., Jin, F., Huang, X. W., and Shen, X. Z. (2010) Interferon-alpha therapy after curative resection prevents early recurrence and improves survival in patients with hepatitis B virus-related hepatocellular carcinoma. J. Surg. Oncol. 102, 796-801
41. Qu, L. S., Jin, F., Huang, X. W., and Shen, X. Z. (2010) High hepatitis B viral load predicts recurrence of small hepatocellular carcinoma after curative resection. J. Gastrointest. Surg. 14, 1111-1120
42. Pestka, S. (2007) The interferons: 50 years after their discovery, there is much more to learn. J. Biol. Chem. 282, 20047-20051
43. Wang, L., Tang, Z. Y., Qin, L. X., Wu, X. F., Sun, H. C., Xue, Q., and Ye, S. L. (2000) High-dose and long-term therapy with interferon-alfa inhibits tumor growth and recurrence in nude mice bearing human hepatocellular carcinoma xenografts with high metastatic potential. Hepatology 32, 43-48 (Pubitemid 30432364)
44. Zhuang, P. Y., Zhang, J. B., Zhang, W., Zhu, X. D., Liang, Y., Xu, H. X., Xiong, Y. Q., Kong, L. Q., Wang, L., Wu, W. Z., Tang, Z. Y., Qin, L. X., and Sun, H. C. (2010) Long-term interferonalpha treatment suppresses tumor growth but promotes metastasis capacity in hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 136, 1891-1900
45. Sato, A., Ohtsuki, M., Hata, M., Kobayashi, E., and Murakami, T. (2006) Antitumor activity of IFN-lambda in murine tumor models. J. Immunol. 176, 7686-7694 (Pubitemid 43849069)
46. Yan, Y., Zhang, J., Liu, Y., Zhu, T., Yuan, L., Ge, Y., Ding, H., and Bu, X. (2013) Inhibition of lung adenocarcinoma transfected with interleukin 28A recombinant adenovirus (Ad-mIFN-lambda2) in vivo. Cancer Biother. Radiopharm. 28, 124-130