Long-term interferon-α treatment suppresses tumor growth but promotes metastasis capacity in hepatocellular carcinoma

Journal of Cancer Research and Clinical Oncology

Volumn 136, Issue 12, 2010, Pages 1891-1900

  Zhuang, Peng Yuan ^a,b   Zhang, Ju Bo ^b   Zhang, Wei ^b   Zhu, Xiao Dong ^b   Liang, Ying ^b,c   Xu, Hua Xiang ^b   Xiong, Yu Quan ^b   Kong, Ling Qun ^b   Wang, Lu ^b   Wu, Wei Zhong ^b   Tang, Zhao You ^b   Qin, Lun Xiu ^b   Sun, Hui Chuan ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c Jiangbin Hospital Guangxi Zhuang Autonomous Region   (China)

Author keywords

Hepatocellular carcinoma (HCC); Interferon (IFN ); Tumor hypoxia; Tumor metastasis

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 8; PLATELET DERIVED GROWTH FACTOR A; RECOMBINANT ALPHA INTERFERON; SCATTER FACTOR RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CANCER INVASION; CELL MIGRATION; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG EFFECT; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER CELL CARCINOMA; MALE; METASTASIS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR PROMOTION; TUMOR VASCULARIZATION; UPREGULATION;

ANIMALS; ANOXIA; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOLOGIC FACTORS; INTERFERON-ALPHA; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM METASTASIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SURVIVAL ANALYSIS; TIME FACTORS; TUMOR BURDEN; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 78649325862     PISSN: 01715216     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00432-010-0848-1     Document Type: Article

References (45)

1. G Bix R Castello M Burrows, et al. 2006 Endorepellin in vivo: targeting the tumor vasculature and retarding cancer growth and metabolism J Natl Cancer Inst 98 1634 1646 1:CAS:528:DC%2BD28XhtlSms7vO 10.1093/jnci/djj441 17105986 (Pubitemid 44811646)
2. RG Bristow RP Hill 2008 Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability Nat Rev Cancer 8 180 192 1:CAS:528:DC%2BD1cXitlOisrw%3D 10.1038/nrc2344 18273037 (Pubitemid 351301853)
3. DA Chan AJ Giaccia 2007 Hypoxia, gene expression, and metastasis Cancer Metastasis Rev 26 333 339 1:CAS:528:DC%2BD2sXotFWrtbw%3D 10.1007/s10555-007- 9063-1 17458506 (Pubitemid 47101666)
4. YS Chang J Adnane PA Trail, et al. 2007 Sorafenib (BAY 43-9006) inhibits tumor growth and vascularization and induces tumor apoptosis and hypoxia in RCC xenograft models Cancer Chemother Pharmacol 59 561 574 1:CAS:528: DC%2BD2sXhvVeiuro%3D 10.1007/s00280-006-0393-4 17160391 (Pubitemid 46295136)
5. BM Fenton SF Paoni 2007 The addition of AG-013736 to fractionated radiation improves tumor response without functionally normalizing the tumor vasculature Cancer Res 67 9921 9928 1:CAS:528:DC%2BD2sXhtFOnsbjE 10.1158/0008-5472.CAN-07-1066 17942924 (Pubitemid 47621241)
6. BM Fenton SF Paoni I Ding 2004 Effect of VEGF receptor-2 antibody on vascular function and oxygenation in spontaneous and transplanted tumors Radiother Oncol 72 221 230 1:CAS:528:DC%2BD2cXmsVGisLc%3D 10.1016/j.radonc.2004. 05.005 15297140 (Pubitemid 39024597)
7. M Franco S Man L Chen, et al. 2006 Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia Cancer Res 66 3639 3648 1:CAS:528:DC%2BD28XjtVOrsbs%3D 10.1158/0008-5472.CAN-05-3295 16585189
8. RA Gatenby RJ Gillies 2008 A microenvironmental model of carcinogenesis Nat Rev Cancer 8 56 61 1:CAS:528:DC%2BD2sXhsVKku73J 10.1038/nrc2255 18059462
9. RJ Gillies RA Gatenby 2007 Hypoxia and adaptive landscapes in the evolution of carcinogenesis Cancer Metastasis Rev 26 311 317 1:CAS:528:DC%2BD2sXotFWrtLk%3D 10.1007/s10555-007-9065-z 17404691 (Pubitemid 47101668)
10. AL Harris 2002 Hypoxia-a key regulatory factor in tumour growth Nat Rev Cancer 2 38 47 1:CAS:528:DC%2BD38XhvF2jtL4%3D 10.1038/nrc704 11902584
11. YK Hong DS Chung YA Joe, et al. 2000 Efficient inhibition of in vivo human malignant glioma growth and angiogenesis by interferon-beta treatment at early stage of tumor development Clin Cancer Res 6 3354 3360 1:CAS:528:DC%2BD3cXmsVOmtLY%3D 10955823
12. K Ikeda Y Arase S Saitoh, et al. 2000 Interferon beta prevents recurrence of hepatocellular carcinoma after complete resection or ablation of the primary tumor-A prospective randomized study of hepatitis C virus-related liver cancer Hepatology 32 228 232 1:CAS:528:DC%2BD3cXlvVyjtrk%3D 10.1053/jhep.2000.9409 10915728
13. JI Izawa P Sweeney P Perrotte, et al. 2002 Inhibition of tumorigenicity and metastasis of human bladder cancer growing in athymic mice by interferon-beta gene therapy results partially from various antiangiogenic effects including endothelial cell apoptosis Clin Cancer Res 8 1258 1270 1:CAS:528:DC%2BD38XjsF2ltLk%3D 11948141
14. E Jonasch FG Haluska 2001 Interferon in oncological practice: review of interferon biology, clinical applications, and toxicities Oncologist 6 34 55 1:CAS:528:DC%2BD3MXhtlKjsbc%3D 10.1634/theoncologist.6-1-34 11161227 (Pubitemid 32155814)
15. S Katyal JH Oliver 3rd MS Peterson JV Ferris BS Carr RL Baron 2000 Extrahepatic metastases of hepatocellular carcinoma Radiology 216 698 703 1:STN:280:DC%2BD3cvktVantA%3D%3D 10966697
16. S Kubo S Nishiguchi K Hirohashi, et al. 2001 Effects of long-term postoperative interferon-alpha therapy on intrahepatic recurrence after resection of hepatitis C virus-related hepatocellular carcinoma. A randomized, controlled trial Ann Intern Med 134 963 967 1:CAS:528:DC%2BD3MXktF2gs70%3D 11352697
17. Y Li Y Tang L Ye, et al. 2003 Establishment of a hepatocellular carcinoma cell line with unique metastatic characteristics through in vivo selection and screening for metastasis-related genes through cDNA microarray J Cancer Res Clin Oncol 129 43 51 1:CAS:528:DC%2BD3sXjsl2nsrs%3D 10.1007/s00432-003-0493-z 12618900 (Pubitemid 38002301)
18. Y Li B Tian J Yang, et al. 2004 Stepwise metastatic human hepatocellular carcinoma cell model system with multiple metastatic potentials established through consecutive in vivo selection and studies on metastatic characteristics J Cancer Res Clin Oncol 130 460 468 1:CAS:528:DC%2BD2cXls1CjsLk%3D 10.1007/s00432-004-0564-9 15146329
19. D Liao RS Johnson 2007 Hypoxia: a key regulator of angiogenesis in cancer Cancer Metastasis Rev 26 281 290 1:CAS:528:DC%2BD2sXotFWrtLw%3D 10.1007/s10555-007-9066-y 17603752 (Pubitemid 47101669)
20. SM Lin CJ Lin CW Hsu, et al. 2004 Prospective randomized controlled study of interferon-alpha in preventing hepatocellular carcinoma recurrence after medical ablation therapy for primary tumors Cancer 100 376 382 1:CAS:528:DC%2BD2cXhtVOgsrs%3D 10.1002/cncr.20004 14716774 (Pubitemid 38063648)
21. JM Llovet A Burroughs J Bruix 2003 Hepatocellular carcinoma Lancet 362 1907 1917 10.1016/S0140-6736(03)14964-1 14667750 (Pubitemid 37518510)
22. CM Lo CL Liu SC Chan, et al. 2007 A randomized, controlled trial of postoperative adjuvant interferon therapy after resection of hepatocellular carcinoma Ann Surg 245 831 842 10.1097/01.sla.0000245829.00977.45 17522506 (Pubitemid 46809282)
23. V Mazzaferro R Romito M Schiavo, et al. 2006 Prevention of hepatocellular carcinoma recurrence with alpha-interferon after liver resection in HCV cirrhosis Hepatology 44 1543 1554 1:CAS:528:DC%2BD2sXislKktQ%3D%3D 10.1002/hep.21415 17133492 (Pubitemid 44970357)
24. Y Mizukami WS Jo EM Duerr, et al. 2005 Induction of interleukin-8 preserves the angiogenic response in HIF-1alpha-deficient colon cancer cells Nat Med 11 992 997 1:CAS:528:DC%2BD2MXpslelurY%3D 16127434
25. DA Murphy S Makonnen W Lassoued MD Feldman C Carter WM Lee 2006 Inhibition of tumor endothelial ERK activation, angiogenesis, and tumor growth by sorafenib (BAY43-9006) Am J Pathol 169 1875 1885 1:CAS:528:DC%2BD28Xht12isr3F 10.2353/ajpath.2006.050711 17071608 (Pubitemid 351182016)
26. H Nagano A Miyamoto H Wada, et al. 2007 Interferon-alpha and 5-fluorouracil combination therapy after palliative hepatic resection in patients with advanced hepatocellular carcinoma, portal venous tumor thrombus in the major trunk, and multiple nodules Cancer 110 2493 2501 1:CAS:528: DC%2BD2sXhsVyisr7L 10.1002/cncr.23033 17941012 (Pubitemid 350174935)
27. M Nakamura H Nagano S Marubashi, et al. 2008 Pilot study of combination chemotherapy of S-1, a novel oral DPD inhibitor, and interferon-alpha for advanced hepatocellular carcinoma with extrahepatic metastasis Cancer 112 1765 1771 1:CAS:528:DC%2BD1cXls1GktL0%3D 10.1002/cncr.23356 18327806 (Pubitemid 351536836)
28. DM Parkin F Bray J Ferlay P Pisani 2005 Global cancer statistics, 2002 CA Cancer J Clin 55 74 108 10.3322/canjclin.55.2.74 15761078
29. S Pennacchietti P Michieli M Galluzzo M Mazzone S Giordano PM Comoglio 2003 Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene Cancer Cell 3 347 361 10.1016/S1535-6108(03)00085-0 12726861 (Pubitemid 38340304)
30. WG Roberts PM Whalen E Soderstrom, et al. 2005 Antiangiogenic and antitumor activity of a selective PDGFR tyrosine kinase inhibitor, CP-673, 451 Cancer Res 65 957 966 1:CAS:528:DC%2BD2MXhtVWntb8%3D 15705896
31. Y Shiratori S Shiina T Teratani, et al. 2003 Interferon therapy after tumor ablation improves prognosis in patients with hepatocellular carcinoma associated with hepatitis C virus Ann Intern Med 138 299 306 12585827
32. HC Sun ZY Tang L Wang, et al. 2006 Postoperative interferon alpha treatment postponed recurrence and improved overall survival in patients after curative resection of HBV-related hepatocellular carcinoma: a randomized clinical trial J Cancer Res Clin Oncol 132 458 465 1:CAS:528: DC%2BD28Xks1emtbo%3D 10.1007/s00432-006-0091-y 16557381
33. ZY Tang SL Ye YK Liu, et al. 2004 A decade's studies on metastasis of hepatocellular carcinoma J Cancer Res Clin Oncol 130 187 196 10.1007/s00432-003-0511-1 14685850 (Pubitemid 38553626)
34. Y Tomimaru Y Sasaki T Yamada, et al. 2006 The significance of surgical resection for pulmonary metastasis from hepatocellular carcinoma Am J Surg 192 46 51 10.1016/j.amjsurg.2005.12.006 16769274 (Pubitemid 43849603)
35. K Uka H Aikata N Mori, et al. 2008 Combination therapy of oral fluoropyrimidine anticancer drug S-1 and interferon alpha for HCC patients with extrahepatic metastases Oncology 75 8 16 1:CAS:528:DC%2BD1cXhtFKgsrjK 10.1159/000151614 18719349
36. P Vaupel A Mayer 2007 Hypoxia in cancer: significance and impact on clinical outcome Cancer Metastasis Rev 26 225 239 1:CAS:528:DC%2BD2sXotFWrtLo%3D 10.1007/s10555-007-9055-1 17440684 (Pubitemid 47101660)
37. Z von Marschall A Scholz T Cramer, et al. 2003 Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis J Natl Cancer Inst 95 437 448 10.1093/jnci/95.6.437
38. H Wada H Nagano H Yamamoto, et al. 2007 Combination therapy of interferon-alpha and 5-fluorouracil inhibits tumor angiogenesis in human hepatocellular carcinoma cells by regulating vascular endothelial growth factor and angiopoietins Oncol Rep 18 801 809 1:CAS:528:DC%2BD2sXhtFygu7jN 17786339
39. L Wang ZY Tang LX Qin, et al. 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 1:CAS:528:DC%2BD3cXltFWgs74%3D 10.1053/jhep.2000.8525 10869287
40. L Wang WZ Wu HC Sun, et al. 2003 Mechanism of interferon alpha on inhibition of metastasis and angiogenesis of hepatocellular carcinoma after curative resection in nude mice J Gastrointest Surg 7 587 594 10.1016/S1091-255X(03)00072-6 12850669 (Pubitemid 36875750)
41. BW Yang Y Liang JL Xia HC Sun L Wang JB Zhang ZY Tang KD Liu J Chen Q Xue J Chen DM Gao WZ Wu 2008 Biological characteristics of fluorescent protein-expressing human hepatocellular carcinoma xenograft model in nude mice Eur J Gastroenterol Hepatol 20 1077 1084 10.1097/MEG.0b013e3283050a67 19047839
42. BW Yang Y Liang JL Xia, et al. 2008 Biological characteristics of fluorescent protein-expressing human hepatocellular carcinoma xenograft model in nude mice Eur J Gastroenterol Hepatol 20 1077 1084 10.1097/MEG.0b013e3283050a67 19047839
43. SY Yoon YJ Lee JH Seo, et al. 2006 uPAR expression under hypoxic conditions depends on iNOS modulated ERK phosphorylation in the MDA-MB-231 breast carcinoma cell line Cell Res 16 75 81 1:CAS:528:DC%2BD28XlvFShsQ%3D%3D 10.1038/sj.cr.7310010 16467878 (Pubitemid 43129311)
44. Zhang T, Sun HC, Zhou HY, et al. (2009) Interferon alpha inhibits hepatocellular carcinoma growth through inducing apoptosis and interfering with adhesion of tumor endothelial cells. Cancer Lett [Epub ahead of print]
45. XD Zhu JB Zhang PY Zhuang, et al. 2008 High expression of macrophage colony-stimulating factor in peritumoral liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma J Clin Oncol 26 2707 2716 10.1200/JCO.2007.15.6521 18509183