Sorafenib inhibits hypoxia-inducible factor-1α synthesis: Implications for antiangiogenic activity in hepatocellular carcinoma

Clinical Cancer Research

Volumn 18, Issue 20, 2012, Pages 5662-5671

  Liu, Li Ping ^a   Ho, Rocky L K ^a   Chen, George G ^a   Lai, Paul B S ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN P70S6K; PROTEIN S6; SORAFENIB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG MEGADOSE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS INHIBITION; TUMOR VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; MICE; NEOVASCULARIZATION, PATHOLOGIC; NIACINAMIDE; PHENYLUREA COMPOUNDS; PHOSPHORYLATION; TRANSPLANTATION, HETEROLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84867531311     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-0552     Document Type: Article

References (43)

1. Ueda H, Tanaka H, Kida Y, Fukuchi H, Ichinose M. Adjuvant chemotherapy with tegafur/uracil administration after transcatheter arterial chemoembolization for advanced hepatocellular carcinoma. Oncol Rep 2008;19:1355-61.
2. Brahimi-Horn MC, Chiche J, Pouyssegur J. Hypoxia and cancer. J Mol Med (Berl) 2007;85:1301-7. (Pubitemid 50004093)
3. Semenza GL. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics Oncogene 2010;29:625-34.
4. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32. (Pubitemid 37328811)
5. Tsuzuki Y, Fukumura D, Oosthuyse B, Koike C, Carmeliet P, Jain RK. Vascular endothelial growth factor (VEGF) modulation by targeting hypoxia-inducible factor-1alpha-> hypoxia response element-> VEGF cascade differentially regulates vascular response and growth rate in tumors. Cancer Res 2000;60:6248-52.
6. Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 1995;270:1230-7.
7. 2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
8. 2-regulated prolyl hydroxylation. Science 2001;292:468-72.
9. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 2000;60:1541-5. (Pubitemid 30183422)
10. Reiling JH, Sabatini DM. Stress and mTORture signaling. Oncogene 2006;25:6373-83. (Pubitemid 44582282)
11. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, et al. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 2005;19:2199-211. (Pubitemid 41330321)
12. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008;359:378-90.
13. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009;10:25-34.
14. Liu L, Cao Y, Chen C, Zhang X, McNabola A, Wilkie D, et al. Sorafenib blocks the RAF/MEK/ERK pathway, inhibits tumor angiogenesis, and induces tumor cell apoptosis in hepatocellular carcinoma model PLC/PRF/5. Cancer Res 2006;66:11851-8. (Pubitemid 46094197)
15. Wilhelm SM, Carter C, Tang L, Wilkie D, McNabola A, Rong H, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004;64:7099-109. (Pubitemid 39331023)
16. Shin HW, Cho CH, Kim TY, Park JW. Sunitinib deregulates tumor adaptation to hypoxia by inhibiting HIF-1alpha synthesis in HT-29 colon cancer cells. Biochem Biophys Res Commun 2010;398:205-11.
17. Nilsson MB, Zage PE, Zeng L, Xu L, Cascone T, Wu HK, et al. Multiple receptor tyrosine kinases regulate HIF-1alpha and HIF-2alpha in normoxia and hypoxia in neuroblastoma: implications for antiangiogenic mechanisms of multikinase inhibitors. Oncogene 2010;29:2938-49.
18. Liu LP, Liang HF, Chen XP, Zhang WG, Yang SL, Xu T, et al. The role of NF-kappaB in Hepatitis b virus X protein-mediated upregulation of VEGF and MMPs. Cancer Invest 2010;28:443-51.
19. Post DE, Van Meir EG. Generation of bidirectional hypoxia/HIF-responsive expression vectors to target gene expression to hypoxic cells. Gene Ther 2001;8:1801-7. (Pubitemid 34100581)
20. Dieterich DC, Lee JJ, Link AJ, Graumann J, Tirrell DA, Schuman EM. Labeling, detection and identification of newly synthesized proteomes with bioorthogonal non-canonical amino-acid tagging. Nat Protoc 2007;2:532-40. (Pubitemid 47040017)
21. Sun SY, Rosenberg LM, Wang X, Zhou Z, Yue P, Fu H, et al. Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res 2005;65:7052-8. (Pubitemid 41161231)
22. Miettinen M, Lindenmayer AE, Chaubal A. Endothelial cell markers CD31, CD34, and BNH9 antibody to H- and Y-antigens-evaluation of their specificity and sensitivity in the diagnosis of vascular tumors and comparison with von Willebrand factor. Mod Pathol 1994;7:82-90.
23. Kobayashi H, Tsuruchi N, Sugihara K, Kaku T, Saito T, Kamura T, et al. Expression of alpha-smooth muscle actin in benign or malignant ovarian tumors. Gynecol Oncol 1993;48:308-13. (Pubitemid 23090797)
24. Wilhelm SM, Adnane L, Newell P, Villanueva A, Llovet JM, Lynch M. Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Mol Cancer Ther 2008;7:3129-40.
25. Obermair A, Bancher-Todesca D, Bilgi S, Kaider A, Kohlberger P, Mullauer-Ertl S, et al. Correlation of vascular endothelial growth factor expression and microvessel density in cervical intraepithelial neoplasia. J Natl Cancer Inst 1997;89:1212-7. (Pubitemid 27350031)
26. Xiang Z, Zeng Z, Tang Z, Fan J, Sun H, Wu W, et al. Increased expression of vascular endothelial growth factor-C and nuclear CXCR4 in hepatocellular carcinoma is correlated with lymph node metastasis and poor outcome. Cancer J 2009;15:519-25.
27. Tseng PL, Tai MH, Huang CC, Wang CC, Lin JW, Hung CH, et al. Overexpression of VEGF is associated with positive p53 immunostaining in hepatocellular carcinoma (HCC) and adverse outcome of HCC patients. J Surg Oncol 2008;98:349-57.
28. Feng YX, Wang T, Deng YZ, Yang P, Li JJ, Guan DX, et al. Sorafenib suppresses postsurgical recurrence and metastasis of hepatocellular carcinoma in an orthotopic mouse model. Hepatology 2011;53:483-92.
29. Iijima Y, Laser M, Shiraishi H, Willey CD, Sundaravadivel B, Xu L, et al. c-Raf/MEK/ERK pathway controls protein kinase C-mediated p70S6K activation in adult cardiac muscle cells. J Biol Chem 2002;277:23065-75. (Pubitemid 34967293)
30. Ueda T, Sasaki M, Elia AJ, Chio II, Hamada K, Fukunaga R, et al. Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. Proc Natl Acad Sci U S A 2010;107:13984-90.
31. Xia Z, Guo M, Ma H. Functional analysis of novel phosphorylation sites of CREB-binding protein using mass spectrometry and mammalian two-hybrid assays. Proteomics 2011;11:3444-51.
32. Jun JH, Yoon WJ, Seo SB, Woo KM, Kim GS, Ryoo HM, et al. BMP2-activated Erk/MAP kinase stabilizes Runx2 by increasing p300 levels and histone acetyltransferase activity. J Biol Chem 2010;285:36410-9.
33. Garcia-Maceira P, Mateo J. Silibinin inhibits hypoxia-inducible factor-1alpha and mTOR/p70S6K/4E-BP1 signalling pathway in human cervical and hepatoma cancer cells: implications for anticancer therapy. Oncogene 2009;28:313-24.
34. Jin F, Liu X, Zhou Z, Yue P, Lotan R, Khuri FR, et al. Activation of nuclear factor-kappaB contributes to induction of death receptors and apoptosis by the synthetic retinoid CD437 in DU145 human prostate cancer cells. Cancer Res 2005;65:6354-63. (Pubitemid 40994422)
35. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 2007;12:9-22. (Pubitemid 47001784)
36. Jin X, Jin HR, Lee D, Lee JH, Kim SK, Lee JJ. A quassinoid 6alpha-tigloyloxychaparrinone inhibits hypoxia-inducible factor-1 pathway by inhibition of eukaryotic translation initiation factor 4E phosphorylation. Eur J Pharmacol 2008;592:41-7.
37. Yang H, Li LW, Shi M, Wang JH, Xiao F, Zhou B, et al. In vivo study of breast carcinoma radiosensitization by targeting eIF4E. Biochem Biophys Res Commun 2012;423:878-83.
38. Manning BD. Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol 2004;167:399-403. (Pubitemid 39489047)
39. Ruffolo SC, Forsell PK, Yuan X, Desmarais S, Himms-Hagen J, Cromlish W, et al. Basal activation of p70S6K results in adipose-specific insulin resistance in protein-tyrosine phosphatase 1B-/- mice. J Biol Chem 2007;282:30423-33. (Pubitemid 350035220)
40. Kim A, Balis FM, Widemann BC. Sorafenib and sunitinib. Oncologist 2009;14:800-5.
41. Blivet-Van Eggelpoel MJ, Chettouh H, Fartoux L, Aoudjehane L, Barbu V, Rey C, et al. Epidermal growth factor receptor and HER-3 restrict cell response to sorafenib in hepatocellular carcinoma cells. J Hepatol 2012;57:108-15.
42. Liu H, Zhang T, Chen R, McConkey DJ, Ward JF, Curley SA. Multiple kinase pathways involved in the different de novo sensitivity of pancreatic cancer cell lines to 17-AAG. J Surg Res 2011;176:141-53.
43. Li QL, Gu FM, Wang Z, Jiang JH, Yao LQ, Tan CJ, et al. Activation of PI3K/AKT and MAPK pathway through a PDGFRbeta-dependent feedback loop is involved in rapamycin resistance in hepatocellular carcinoma. PLoS One 2012;7:e33379.