Benzo[a]pyrene-3,6-dione inhibited VEGF expression through inducing HIF-1α degradation

Biochemical and Biophysical Research Communications

Volumn 357, Issue 2, 2007, Pages 517-523

  Li, Zhao Dong ^a   Liu, Ling Zhi ^b   Shi, Xianglin ^a   Fang, Jing ^a   Jiang, Bing Hua ^a,b  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

BPQ; HIF 1; Hsp90; VEGF

Indexed keywords

7,8 DIHYDROXYBENZO[A]PYRENE 9,10 OXIDE; BENZO[A]PYRENE; BENZO[A]PYRENE 3,6 DIONE; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; POLYCYCLIC AROMATIC HYDROCARBON; PROTEASOME; UNCLASSIFIED DRUG; VASCULOTROPIN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ADENOCARCINOMA; BENZOPYRENES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KIDNEY; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34247144232     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2007.03.178     Document Type: Article

References (39)

1. Hecht S.S. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat. Rev. Cancer 3 (2003) 733-744
2. Hoffmann D., Djordjevic M.V., and Hoffmann I. The changing cigarette. Prev. Med. 26 (1997) 427-434
3. Nesnow S., Mass M.J., Ross J.A., Galati A.J., Lambert G.R., Gennings C., Carter Jr. W.H., and Stoner G.D. Lung tumorigenic interactions in strain A/J mice of five environmental polycyclic aromatic hydrocarbons. Environ. Health Perspect. 106 Suppl. 6 (1998) 1337-1346
4. Conney A.H., Chang R.L., Jerina D.M., and Wei S.J. Studies on the metabolism of benzo[a]pyrene and dose-dependent differences in the mutagenic profile of its ultimate carcinogenic metabolite. Drug Metab. Rev. 26 (1994) 125-163
5. Cosman M., de los S.C., Fiala R., Hingerty B.E., Singh S.B., Ibanez V., Margulis L.A., Live D., Geacintov N.E., and Broyde S. Solution conformation of the major adduct between the carcinogen (+)-anti-benzo[a]pyrene diol epoxide and DNA. Proc. Natl. Acad. Sci. USA 89 (1992) 1914-1918
6. MacLeod M.C., Mansfield B.K., and Selkirk J.K. Time course of metabolism of benzo[e]pyrene by hamster embryo cells and the effect of chemical modifiers. Chem. Biol. Interact. 40 (1982) 275-285
7. Nebert D.W., Puga A., and Vasiliou V. Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction. Ann. N Y Acad. Sci. 685 (1993) 624-640
8. Honey S., O'Keefe P., Drahushuk A.T., Olson J.R., Kumar S., and Sikka H.C. Metabolism of benzo(a)pyrene by duck liver microsomes. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 126 (2000) 285-292
9. Levin W., Wood A.W., Wislocki P.G., Kapitulnik J., Yagi H., Jerina D.M., and Conney A.H. Carcinogenicity of benzo-ring derivatives of benzo(a)pyrene on mouse skin. Cancer Res. 37 (1977) 3356-3361
10. Merimsky O., and Inbar M. Cigarette smoking and skin cancer. Clin. Dermatol. 16 (1998) 585-588
11. Smith L.E., Denissenko M.F., Bennett W.P., Li H., Amin S., Tang M., and Pfeifer G.P. Targeting of lung cancer mutational hotspots by polycyclic aromatic hydrocarbons. J. Natl. Cancer Inst. 92 (2000) 803-811
12. Blagosklonny M.V. Antiangiogenic therapy and tumor progression. Cancer Cell 5 (2004) 13-17
13. Tanaka S., Sugimachi K., Yamashita Y., Shirabe K., Shimada M., Wands J.R., and Sugimachi K. Angiogenic switch as a molecular target of malignant tumors. J. Gastroenterol. 38 Suppl. 15 (2003) 93-97
14. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1 (1995) 27-31
15. Folkman J. Seminars in medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N. Engl. J. Med. 333 (1995) 1757-1763
16. Brognard J., Clark A.S., Ni Y., and Dennis P.A. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res. 61 (2001) 3986-3997
17. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., and Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16 (1996) 4604-4613
18. Semenza G.L. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 71-103
19. Jiang B.H., Semenza G.L., Bauer C., and Marti H.H. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am. J. Physiol. 271 (1996) C1172-C1180
20. 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. Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc. Natl. Acad. Sci. USA 94 (1997) 8104-8109
21. 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. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 59 (1999) 5830-5835
22. Jiang B.H., Rue E., Wang G.L., Roe R., and Semenza G.L. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271 (1996) 17771-17778
23. Wang G.L., Jiang B.H., Rue E.A., and Semenza G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92 (1995) 5510-5514
24. Huang L.E., Gu J., Schau M., and Bunn H.F. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95 (1998) 7987-7992
25. Kallio P.J., Wilson W.J., O'Brien S., Makino Y., and Poellinger L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 274 (1999) 6519-6525
26. Salceda S., and Caro J. 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 (1997) 22642-22647
27. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., and Kaelin Jr. W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292 (2001) 464-468
28. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., Maxwell P.H., Pugh C.W., and Ratcliffe P.J. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292 (2001) 468-472
29. 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. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399 (1999) 271-275
30. Gradin K., McGuire J., Wenger R.H., Kvietikova I., fhitelaw M.L., Toftgard R., Tora L., Gassmann M., and Poellinger L. Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor. Mol. Cell. Biol. 16 (1996) 5221-5231
31. Neckers L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol. Med. 8 (2002) S55-S61
32. Isaacs J.S., Jung Y.J., Mimnaugh E.G., Martinez A., Cuttitta F., and Neckers L.M. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J. Biol. Chem. 277 (2002) 29936-29944
33. Mabjeesh N.J., Post D.E., Willard M.T., Kaur B., Van Meir E.G., Simons J.W., and Zhong H. Geldanamycin induces degradation of hypoxia-inducible factor 1alpha protein via the proteosome pathway in prostate cancer cells. Cancer Res. 62 (2002) 2478-2482
34. Jiang B.H., Jiang G., Zheng J.Z., Lu Z., Hunter T., and Vogt P.K. Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ. 12 (2001) 363-369
35. Antonsson C., Whitelaw M.L., McGuire J., Gustafsson J.A., and Poellinger L. Distinct roles of the molecular chaperone hsp90 in modulating dioxin receptor function via the basic helix-loop-helix and PAS domains. Mol. Cell. Biol. 15 (1995) 756-765
36. Bresnick E.H., Dalman F.C., Sanchez E.R., and Pratt W.B. Evidence that the 90-kDa heat shock protein is necessary for the steroid binding conformation of the L cell glucocorticoid receptor. J. Biol. Chem. 264 (1989) 4992-4997
37. Xu Y., and Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc. Natl. Acad. Sci. USA 90 (1993) 7074-7078
38. Mimnaugh E.G., Chavany C., and Neckers L. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J. Biol. Chem. 271 (1996) 22796-22801
39. Whitesell L., Sutphin P., An W.G., Schulte T., Blagosklonny M.V., and Neckers L. Geldanamycin-stimulated destabilization of mutated p53 is mediated by the proteasome in vivo. Oncogene 14 (1997) 2809-2816