Combination therapy of interferon-α and 5-fluorouracil inhibits tumor angiogenesis in human hepatocellular carcinoma cells by regulating vascular endothelial growth factor and angiopoietins

Oncology Reports

Volumn 18, Issue 4, 2007, Pages 801-809

  Wada, Hiroshi ^a   Nagano, Hiroaki ^a   Yamamoto, Hirofumi ^a   Arai, Isao ^a   Ota, Hideo ^a   Nakamura, Masato ^a   Damdinsuren, Bazarragchaa ^a   Noda, Takehiro ^a   Marubashi, Shigeru ^a   Miyamoto, Atsushi ^a   Takeda, Yutaka ^a   Umeshita, Koji ^a   Doki, Yuichiro ^a   Dono, Keizo ^a   Nakamori, Shoji ^a   Sakon, Masato ^a   Monden, Morito ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Angiopoietin; Chemotherapy; Hepatocellular carcinoma; Interferon

Indexed keywords

ALPHA INTERFERON; ANGIOPOIETIN; ANTINEOPLASTIC AGENT; FLUOROURACIL; MESSENGER RNA; RNA; UNCLASSIFIED DRUG; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL; APOPTOSIS; ARTICLE; BAGG ALBINO MOUSE; DRUG EFFECT; DRUG POTENTIATION; ENZYME IMMUNOASSAY; FEMALE; GENETICS; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULARIZATION;

ANGIOPOIETINS; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; DRUG SYNERGISM; FEMALE; FLUOROURACIL; HUMANS; IMMUNOENZYME TECHNIQUES; INTERFERON-ALPHA; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, NEOPLASM; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 38449120032     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.18.4.801     Document Type: Article

References (51)

1. Farmer DG, Rosove MH, Shaked A and Busuttil RW: Current treatment modalities for hepatocellular carcinoma. Ann Surg 219: 236-247, 1994. (Pubitemid 24085118)
2. Bruix J and Llovet JM: Prognostic prediction and treatment strategy in hepatocellular carcinoma. Hepatology 35: 519-524, 2002. (Pubitemid 34183954)
3. Shen DW, Lu YG, Chin KV, Pastan I and Gottesman MM: Human hepatocellular carcinoma cell lines exhibit multidrug resistance unrelated to MRD1 gene expression. J Cell Sci 98: 317-322, 1991. (Pubitemid 21924980)
4. Baron S and Dianzani F: The interferons: a biological system with therapeutic potential in viral infections. Antiviral Res 24: 97-110, 1994. (Pubitemid 24228865)
5. Gutterman JU: Cytokine therapeutics: lessons from interferon alpha. Proc Natl Acad Sci USA 91: 1198-1205, 1994.
6. Hertzog PJ, Hwang SY and Kola I: Role of interferons in the regulation of cell proliferation, differentiation, and development. Mol Reprod Dev 39: 226-232, 1994. (Pubitemid 24312166)
7. Von Marschall Z, Scholz A, Cramer T, et al: Effects of interferon alpha on vascular endothelial growth factor gene transcription and tumor angiogenesis. J Natl Cancer Inst 95: 437-448, 2003. (Pubitemid 36432418)
8. Gohji K, Fidler IJ, Tsan R, et al: Human recombinant interferons-beta and -gamma decrease gelatinase production and invasion by human KG-2 renal-carcinoma cells. Int J Cancer 58: 380-384, 1994. (Pubitemid 24254648)
9. Huang SF, Kim SJ, Lee AT, et al: Inhibition of growth and metastasis of orthotopic human prostate cancer in athymic mice by combination therapy with pegylated interferon-alpha-2b and docetaxel. Cancer Res 62: 5720-5726, 2002. (Pubitemid 35204727)
10. Oliveira IC, Sciavolino PJ, Lee TH and Vilcek J: Downregulation of interleukin 8 gene expression in human fibroblasts: unique mechanism of transcriptional inhibition by interferon. Proc Natl Acad Sci USA 89: 9049-9053, 1992.
11. Singh RK, Gutman M, Bucana CD, Sanchez R, Llansa N and Fidler IJ: Interferons alpha and beta down-regulate the expression of basic fibroblast growth factor in human carcinomas. Proc Natl Acad Sci USA 92: 4562-4566, 1995.
12. Solorzano CC, Hwang R, Baker CH, et al: Administration of optimal biological dose and schedule of interferon alpha combined with gemcitabine induces apoptosis in tumor-associated endothelial cells and reduces growth of human pancreatic carcinoma implanted orthotopically in nude mice. Clin Cancer Res 9: 1858-1867, 2003. (Pubitemid 36554614)
13. Castello MA, Ragni G, Antimi A, et al: Successful management with interferon alpha-2a after prednisone therapy failure in an infant with a giant cavernous hemangioma. Med Pediatr Oncol 28: 213-215, 1997. (Pubitemid 27078426)
14. Jonasch E and Haluska FG: Interferon in oncological practice: review of interferon biology, clinical applications and toxicities. Oncologist 6: 34-55, 2001. (Pubitemid 32155814)
15. Shepherd FA, Beaulieu R, Gelmon K, et al: Prospective randomized trial of two dose levels of interferon alfa with zidovudine for the treatment of Kaposi's sarcoma associated with human immunodeficiency virus infection: a Canadian HIV Clinical Trials Network study. J Clin Oncol 16: 1736-1742, 1998.
16. Llovet JM, Sala M, Castells L, et al: Randomized controlled trial of interferon treatment for advanced hepatocellular carcinoma. Hepatology 31: 54-58, 2000. (Pubitemid 30033689)
17. Leung TW, Patt YZ, Lau WY, et al: Complete pathological remission is possible with systemic combination chemotherapy for inoperable hepatocellular carcinoma. Clin Cancer Res 5: 1676-1681, 1999. (Pubitemid 29334445)
18. Urabe T, Kaneko S, Matsushita E, Unoura M and Kobayashi K: Clinical pilot study of intrahepatic arterial chemotherapy with methotrexate, 5-fluorouracil, cisplatin and subcutaneous interferon-alpha-2b for patients with locally advanced hepatocellular carcinoma. Oncology 55: 39-47, 1998. (Pubitemid 128707622)
19. Patt YZ, Hassan MM, Lozano RD, et al: Phase II trial of systemic continuous fluorouracil and subcutaneous recombinant interferon Alfa-2b for treatment of hepatocellular carcinoma. J Clin Oncol 21: 421-427, 2003. (Pubitemid 46606469)
20. Obi S, Yoshida H, Toune R, et al: Combination therapy of intraarterial 5-fluorouracil and systemic interferon-alpha for advanced hepatocellular carcinoma with portal venous invasion. Cancer 106: 1990-1997, 2006. (Pubitemid 43673215)
21. Miyamoto A, Umeshita K, Sakon M, et al: Advanced hepatocellular carcinoma with distant metastases, successfully treated by a combination therapy of alpha-interferon and oral tegafur/uracil. J Gastroenterol Hepatol 15: 1447-1451, 2000. (Pubitemid 32052922)
22. Sakon M, Nagano H, Dono K, et al: Combined intraarterial 5-fluorouracil and subcutaneous interferon-alpha therapy for advanced hepatocellular carcinoma with tumor thrombi in the major portal branches. Cancer 94: 435-442, 2002. (Pubitemid 34081374)
23. Ota H, Nagano H, Sakon M, et al: Treatment of hepatocellular carcinoma with major portal vein thrombosis by combined therapy with subcutaneous interferon-alpha and intra-arterial 5-fluorouracil; role of type 1 interferon receptor expression. Br J Cancer 93: 557-564, 2005. (Pubitemid 43079999)
24. Nagano H, Sakon M, Eguchi H, et al: Hepatic resection followed by IFN-alpha and 5-FU for advanced hepatocellular carcinoma with tumor thrombus in the major portal branch. Hepatogastroenterology (In press).
25. Schwartz EL, Hoffman M, O'Connor CJ and Wadler S: Stimulation of 5-fluorouracil metabolic activation by interferon-alpha in human colon carcinoma cells. Biochem Biophys Res Commun 182: 1232-1239, 1992.
26. Damdinsuren B, Nagano H, Sakon M, et al: Interferon-beta is more potent than interferon-alpha in inhibition of human hepatocellular carcinoma cell growth when used alone and in combination with anticancer drugs. Ann Surg Oncol 10: 1184-1190, 2003. (Pubitemid 40486814)
27. Eguchi H, Nagano H, Yamamoto H, et al: Augmentation of antitumor activity of 5-fluorouracil by interferon alpha is associated with up-regulation of p27Kip1 in human hepatocellular carcinoma cells. Clin Cancer Res 6: 2881-2890, 2000. (Pubitemid 30482131)
28. Kondo M, Nagano H, Wada H, et al: Combination of IFN-alpha and 5-fluorouracil induces apoptosis through IFN-alpha/beta receptor in human hepatocellular carcinoma cells. Clin Cancer Res 11: 1277-1286, 2005. (Pubitemid 40175781)
29. Yamamoto T, Nagano H, Sakon M, et al: Partial contribution of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)/TRAIL receptor pathway to antitumor effects of interferon-alpha/5-fluorouracil against hepatocellular carcinoma. Clin Cancer Res 10: 7884-7895, 2004. (Pubitemid 39587527)
30. Slaton JW, Perrotte P, Inoue K, Dinney CP and Fidler IJ: Interferon-alpha-mediated down-regulation of angiogenesis-related genes and therapy of bladder cancer are dependent on optimization of biological dose and schedule. Clin Cancer Res 5: 2726-2734, 1999. (Pubitemid 29493945)
31. Teicher BA, Chen V, Shih C, et al: Treatment regimens including the multitargeted antifolate LY231514 in human tumor xenografts. Clin Cancer Res 6: 1016-1023, 2000. (Pubitemid 30159362)
32. Ishikawa Y, Kubota T, Otani Y, et al: Dihydropyrimidine dehydrogenase activity and messenger RNA level may be related to the antitumor effect of 5-fluorouracil on human tumor xenografts in nude mice. Clin Cancer Res 5: 883-889, 1999.
33. Britten CD, Hilsenbeck SG, Eckhardt SG, et al: Enhanced antitumor activity of 6-hydroxymethylacylfulvene in combination with irinotecan and 5-fluorouracil in the HT29 human colon tumor xenograft model. Cancer Res 59: 1049-1053, 1999. (Pubitemid 29135965)
34. Wada H, Nagano H, Yamamoto H, et al: Expression pattern of angiogenic factors and prognosis after hepatic resection in hepatocellular carcinoma: importance of angiopoietin-2 and hypoxia-induced factor-1 alpha. Liver Int 26: 414-423, 2006.
35. Ogawa M, Yamamoto H, Nagano H, et al: Hepatic expression of ANG2 RNA in metastatic colorectal cancer. Hepatology 39: 528-539, 2004. (Pubitemid 38222195)
36. Hisaka T, Yano H, Ogasawara S, et al: Interferon-alphaCon1 suppresses proliferation of liver cancer cell lines in vitro and in vivo. J Hepatol 41: 782-789, 2004. (Pubitemid 39434308)
37. Kojiro S, Yano H, Ogasawara S, et al: Antiproliferative effects of 5-fluorouracil and interferon-alpha in combination on a hepatocellular carcinoma cell line in vitro and in vivo . J Gastroenterol Hepatol 21: 129-137, 2006.
38. Folkman J: Tumor angiogenesis: therapeutic implications. N Engl J Med 285: 1182-1186, 1971.
39. Tanaka S, Mori M, Sakamoto Y, Makuuchi M, Sugimachi K and Wands JR: Biologic significance of angiopoietin-2 expression in human hepatocellular carcinoma. J Clin Invest 103: 341-345, 1999. (Pubitemid 29069983)
40. Torimura T, Ueno T, Kin M, et al: Overexpression of angiopoietin-1 and angiopoietin-2 in hepatocellular carcinoma. J Hepatol 40: 799-807, 2004.
41. Mitsuhashi N, Shimizu H, Ohtsuka M, et al: Angiopoietins and Tie-2 expression in angiogenesis and proliferation of human hepatocellular carcinoma. Hepatology 37: 1105-1113, 2003.
42. Maisonpierre PC, Suri C, Jones PF, et al: Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60, 1997.
43. Davis S, Aldrich TH, Jones PF, et al: Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87: 1161-1169, 1996.
44. Suri C, Jones PF, Patan S, et al: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87: 1171-1180, 1996.
45. Papapetropoulos A, Garcia-Cardena G, Dengler TJ, Maisonpierre PC, Yancopoulos GD and Sessa WC: Direct actions of angiopoietin-1 on human endothelium: evidence for network stabilization, cell survival and interaction with other angiogenic growth factors. Lab Invest 79: 213-223, 1999.
46. Asahara T, Chen D, Takahashi T, et al: Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ Res 83: 233-240, 1998.
47. Harada H, Kitagawa M, Tanaka N, et al: Anti-oncogenic and oncogenic potentials of interferon regulatory factors-1 and -2. Science 259: 971-974, 1993.
48. Zhang L, Yang N, Park JW, et al: Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 63: 3403-3412, 2003.
49. Potente M, Urbich C, Sasaki K, et al: Involvement of Foxo transcription factors in angiogenesis and postnatal neovascularization. J Clin Invest 115: 2382-2392, 2005.
50. Tran H, Brunet A, Grenier JM, et al: DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 296: 530-534, 2002.
51. Kops GJ, Dansen TB, Polderman PE, et al: Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419: 316-321, 2002.