Apigenin inhibits tumor angiogenesis through decreasing HIF-1α and VEGF expression

Carcinogenesis

Volumn 28, Issue 4, 2007, Pages 858-864

  Fang, Jing ^a   Zhou, Qiong ^a   Liu, Ling Zhi ^a   Xia, Chang ^b   Hu, Xiaowen ^a   Shi, Xianglin ^a   Jiang, Bing Hua ^a,b  

^a Chinese Academy of Sciences   (China)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APIGENIN; FLAVONOID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MATRIGEL; OXYGEN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CHICKEN; CHORIOALLANTOIS; COLON CANCER; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INHIBITION KINETICS; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR VASCULARIZATION;

ANIMALS; ANOXIA; APIGENIN; APOPTOSIS; BINDING SITES; CELL DIVISION; CELL LINE, TUMOR; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; COLLAGEN; DRUG COMBINATIONS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LAMININ; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; PROMOTER REGIONS (GENETICS); PROTEOGLYCANS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34047132303     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgl205     Document Type: Article

References (46)

1. Folkman,J. (2002) Role of angiogenesis in tumor growth and metastasis. Semin. Oncol., 29, 15-18.
2. Plate,K.H., Breier,G., Weich,H.A. and Risau,W. (1992) Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature, 359, 845-848.
3. Ferrara,N. and Davis-Smyth,T. (1997) The biology of vascular endothelial growth factor. Endocr. Rev., 18, 4-25.
4. Carmeliet,P. and Jain,R.K. (2000) Angiogenesis in cancer and other diseases. Nature, 407, 249-257.
5. Brekken,R.A., Overholser,J.P., Stastny,V.A., Waltenberger,J., Minna,J.D. and Thorpe,P.E. (2000) Selective inhibition of vascular endothelial growth factor (VEGF) receptor 2 (KDR/Flk-1) activity by a monoclonal anti-VEGF antibody blocks tumor growth in mice. Cancer Res., 60, 5117-5124.
6. Borgstrom,P., Bourdon,M.A., Hillan,K.J., Sriramarao,P. and Ferrara,N. (1998) Neutralizing anti-vascular endothelial growth factor antibody completely inhibits angiogenesis and growth of human prostate carcinoma micro tumors in vivo. Prostate, 35, 1-10.
7. Angelov,L., Salhia,B., Roncari,L., McMahon,G. and Guha,A. (1999) Inhibition of angiogenesis by blocking activation of the vascular endothelial growth factor receptor 2 leads to decreased growth of neurogenic sarcomas. Cancer Res., 59, 5536-5541.
8. Cheng,S.Y., Huang,H.J., Nagane,M., Ji,X.D., Wang,D., Shih,C.C., Arap,W., Huang,C.M. and Cavenee,W.K. (1996) Suppression of glioblastoma angiogenicity and tumorigenicity by inhibition of endogenous expression of vascular endothelial growth factor. Proc. Natl Acad. Sci. USA, 93, 8502-8507.
9. Masood,R., Cai,J., Zheng,T., Smith,D.L., Hinton,D.R. and Gill,P.S. (2001) Vascular endothelial growth factor (VEGF) is an autocrine growth factor for VEGF receptor-positive human tumors. Blood, 98, 1904-1913.
10. Jackson,M.W., Roberts,J.S., Heckford,S.E., Ricciardelli,C., Stahl,J., Choong,C., Horsfall,D.J. and Tilley,W.D. (2002) A potential autocrine role for vascular endothelial growth factor in prostate cancer. Cancer Res., 62, 854-859.
11. Soker,S., Kaefer,M., Johnson,M., Klagsbrun,M., Atala,A. and Freeman,M.R. (2001) Vascular endothelial growth factor-mediated autocrine stimulation of prostate tumor cells coincides with progression to a malignant phenotype. Am. J. Pathol., 159, 651-659.
12. Semenza,G.L. (2000) Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit. Rev. Biochem. Mol. Biol., 35, 71-103.
13. Forsythe,J.A., Jiang,B.H., Iyer,N.V., Agani,F., Leung,S.W., Koos,R.D. and Semenza,G.L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol., 16, 4604-4613.
14. Zhong,H., De Marzo,A.M., Laughner,E., Lim,M., Hilton,D.A., Zagzag,D., Buechler,P., Isaacs,W.B., Semenza,G.L. and Simons,J.W. (1999) Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res., 59, 5830-5835.
15. Maxwell,P.H., Dachs,G.U., Gleadle,J.M., Nicholls,L.G., Harris,A.L., Stratford,I.J., Hankinson,O., Pugh,C.W. and Ratcliffe,P.J. (1997) Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc. Natl Acad. Sci. USA, 94, 8104-8109.
16. Jiang,B.H., Rue,E., Wang,G.L., Roe,R. and Semenza,G.L. (1996) Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem., 271, 17771-17778.
17. Wang,G.L., Jiang,B.H., Rue,E.A. and Semenza,G.L. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. USA, 92, 5510-5514.
18. Kallio,P.J., Wilson,W.J., O'Brien,S., Makino,Y. and Poellinger,L. (1999) Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J. Biol. Chem., 274, 6519-6525.
19. Salceda,S. and Caro,J. (1997) Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem., 272, 22642-22647.
20. Maxwell,P.H., Wiesener,M.S., Chang,G.W., Clifford,S.C., Vaux,E.C., Cockman,M.E., Wykoff,C.C., Pugh,C.W., Maher,E.R. and Ratcliffe,P.J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature, 399, 271-275.
21. Jaakkola,P., Mole,D.R., Tian,Y.M. et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science, 292, 468-472.
22. Ivan,M., Kondo,K., Yang,H., Kim,W., Valiando,J., Ohh,M., Salic,A., Asara,J.M., Lane,W.S. and Kaelin,W.G. Jr (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: Implications for O2 sensing. Science, 292, 464-468.
23. Duthie,G. and Crozier,A. (2000) Plant-derived phenolic antioxidants. Curr. Opin. Clin. Nutr. Metab. Care, 3, 447-451.
24. Fotsis,T., Pepper,M.S., Aktas,E., Breit,S., Rasku,S., Adlercreutz,H., Wahala,K., Montesano,R. and Schweigerer,L. (1997) Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res., 57, 2916-2921.
25. Morrissey,C., O'Neill,A., Spengler,B., Christoffel,V., Fitzpatrick,J.M. and Watson,R.W. (2005) Apigenin drives the production of reactive oxygen species and initiates a mitochondrial mediated cell death pathway in prostate epithelial cells. Prostate, 63, 131-142.
26. Yin,F., Giuliano,A.E., Law,R.E. and Van Herle,A.J. (2001) Apigenin inhibits growth and induces G2/M arrest by modulating cyclin-CDK regulators and ERK MAP kinase activation in breast carcinoma cells. Anticancer Res., 21, 413-420.
27. Gupta,S., Afaq,F. and Mukhtar,H. (2001) Selective growth-inhibitory, cell-cycle deregulatory and apoptotic response of apigenin in normal versus human prostate carcinoma cells. Biochem. Biophys. Res. Commun., 287, 914-920.
28. Wang,W., Heideman,L., Chung,C.S., Pelling,J.C., Koehler,K.J. and Birt,D.F. (2000) Cell-cycle arrest at G2/M and growth inhibition by apigenin in human colon carcinoma cell lines. Mol. Carcinog., 28, 102-110.
29. Fang,J., Xia,C., Cao,Z., Zheng,J.Z., Reed,E. and Jiang,B.H. (2005) Apigenin inhibits VEGF and HIF-1 expression via PI3K/AKT/p70S6K1 and HDM2/p53 pathways. FASEB J., 19, 342-353.
30. Fang,J., Cao,Z., Chen,Y.C., Reed,E. and Jiang,B.H. (2004) 9-beta-D-arabinofuranosyl-2-fluoroadenine inhibits expression of vascular endothelial growth factor through hypoxia-inducible factor-1 in human ovarian cancer cells. Mol. Pharmacol., 66, 178-186.
31. Passaniti,A., Taylor,R.M., Pili,R., Guo,Y., Long,P.V., Haney,J.A., Pauly,R.R., Grant,D.S. and Martin,G.R. (1992) A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest, 67, 519-528.
32. Zhong,H., De Marzo,A.M., Laughner,E., Lim,M., Hilton,D.A., Zagzag,D., Buechler,P., Isaacs,W.B., Semenza,G.L. and Simons,J.W. (1999) Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res., 59, 5830-5835.
33. Semenza,G.L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer, 3, 721-732.
34. Katschinski,D.M., Le,L., Heinrich,D., Wagner,K.F., Hofer,T., Schindler,S.G. and Wenger,R.H. (2002) Heat induction of the unphosphorylated form of hypoxia-inducible factor-1alpha is dependent on heat shock protein-90 activity. J. Biol. Chem., 277, 9262-9267.
35. Minet,E., Mottet,D., Michel,G., Roland,I., Raes,M., Remacle,J. and Michiels,C. (1999) Hypoxia-induced activation of HIF-1: Role of HIF-1alpha-Hsp90 interaction. FEBS Lett., 460, 251-256.
36. Isaacs,J.S., Jung,Y.J., Mimnaugh,E.G., Martinez,A., Cuttitta,F. and Neckers,L.M. (2002) Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J. Biol. Chem., 277, 29936-29944.
37. Balbay,M.D., Pettaway,C.A., Kuniyasu,H., Inoue,K., Ramirez,E., Li,E., Fidler,I.J. and Dinney,C.P. (1999) Highly metastatic human prostate cancer growing within the prostate of athymic mice overexpresses vascular endothelial growth factor. Clin. Cancer Res., 5, 783-789.
38. Connolly,J.M. and Rose,D.P. (1998) Angiogenesis in two human prostate cancer cell lines with differing metastatic potential when growing as solid tumors in nude mice. J. Urol., 160, 932-936.
39. Melnyk,O., Zimmerman,M., Kim,K.J. and Shuman,M. (1999) Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a pre-clinical model. J. Urol., 161, 960-963.
40. Harper,M.E., Glynne-Jones,E., Goddard,L., Mathews,P. and Nicholson,R.I. (1998) Expression of androgen receptor and growth factors in premalignant lesions of the prostate. J. Pathol., 186, 169-177.
41. Zhong,H., Chiles,K., Feldser,D., Laughner,E., Hanrahan,C., Georgescu,M.M., Simons,J.W. and Semenza,G.L. (2000) 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., 60, 1541-1545.
42. Jiang,B.H., Jiang,G., Zheng,J.Z., Lu,Z., Hunter,T. and Vogt,P.K. (2001) Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ., 12, 363-369.
43. Laughner,E., Taghavi,P., Chiles,K., Mahon,P.C. and Semenza,G.L. (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: Novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol., 21, 3995-4004.
44. Stiehl,D.P., Jelkmann,W., Wenger,R.H. and Hellwig-Burgel,T. (2002) Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett., 512, 157-162.
45. Zundel,W., Schindler,C., Haas-Kogan,D. et al. (2000) Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev., 14, 391-396.
46. Ravi,R., Mookerjee,B., Bhujwalla,Z.M., Sutter,C.H., Artemov,D., Zeng,Q., Dillehay,L.E., Madan,A., Semenza,G.L. and Bedi,A. (2000) Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1alpha. Genes Dev., 14, 34-44.10).