Increased expression of CYP4Z1 promotes tumor angiogenesis and growth in human breast cancer

Toxicology and Applied Pharmacology

Volumn 264, Issue 1, 2012, Pages 73-83

  Yu, Wei ^a   Chai, Hongyan ^b   Li, Ying ^a   Zhao, Haixia ^a   Xie, Xianfei ^a   Zheng, Hao ^a   Wang, Chenlong ^a   Wang, Xue ^a   Yang, Guifang ^b   Cai, Xiaojun ^b   Falck, John R ^c   Yang, Jing ^a,b  

^a WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Angiogenesis; Breast cancer; Cytochrome P450; TIMP 2; VEGF A

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 20 HYDROXYICOSATETRAENOIC ACID; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CYTOCHROME P450; CYTOCHROME P450 4Z1; CYTOCHROME P450 INHIBITOR; HET 0016; LAURIC ACID; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MYRISTIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN KINASE B; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 2; UNCLASSIFIED DRUG; VASCULOTROPIN A; WORTMANNIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CARCINOGENESIS; CELL DENSITY; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHICK; CHORIOALLANTOIS; CONTROLLED STUDY; CULTURE MEDIUM; DRUG POTENCY; EMBRYO; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR MEMBRANE; MEDIATOR; MICROVASCULATURE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; TUMOR GROWTH; TUMOR VOLUME; TUMOR XENOGRAFT; UMBILICAL VEIN ENDOTHELIAL CELL; ZEBRA FISH;

AMIDINES; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASE-2; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZEBRAFISH;

DANIO RERIO;

EID: 84865955844     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.07.019     Document Type: Article

References (53)

1. Alexanian A., Rufanova V.A., Miller B., Flasch A., Roman R.J., Sorokin A. Down-regulation of 20-HETE synthesis and signaling inhibits renal adenocarcinoma cell proliferation and tumor growth. Anticancer. Res. 2009, 29:3819-3824.
2. Bhat T.A., Singh R.P. Tumor angiogenesis-a potential target in cancer chemoprevention. Food Chem. Toxicol. 2008, 46:1334-1345.
3. Bourboulia D., Stetler-Stevenson W.G. Matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs): positive and negative regulators in tumor cell adhesion. Semin. Cancer Biol. 2010, 20:161-168.
4. Chandrashekar N., Selvamani A., Subramanian R., Pandi A., Thiruvengadam D. Baicalein inhibits pulmonary carcinogenesis-associated inflammation and interferes with COX-2, MMP-2 and MMP-9 expressions in-vivo. Toxicol. Appl. Pharmacol. 2012, 261:10-21.
5. Chen P., Guo M., Wygle D., Edwards P.A., Falck J.R., Roman R.J., Scicli A.G. Inhibitors of cytochrome P450 4A suppress angiogenic responses. Am. J. Pathol. 2005, 166:615-624.
6. Chen L., Ackerman R., Guo A.M. 20-HETE in neovascularization. Prostaglandins Other Lipid Mediat. 2012, 98:63-68.
7. 2 regulates the angiogenic phenotype via PTEN oxidation. J. Biol. Chem. 2005, 280:16916-16924.
8. Cook K.M., Figg W.D. Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J. Clin. 2010, 60:222-243.
9. Destouches D., El K.D., Hamma-Kourbali Y., Krust B., Albanese P., Katsoris P., Guichard G., Briand J.P., Courty J., Hovanessian A.G. Suppression of tumor growth and angiogenesis by a specific antagonist of the cell-surface expressed nucleolin. PLoS One 2008, 3:e2518.
10. Dhanasekaran A., Bodiga S., Gruenloh S., Gao Y., Dunn L., Falck J.R., Buonaccorsi J.N., Medhora M., Jacobs E.R. 20-HETE increases survival and decreases apoptosis in pulmonary arteries and pulmonary artery endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 2009, 296:H777-H786.
11. Downie D., McFadyen M.C., Rooney P.H., Cruickshank M.E., Parkin D.E., Miller I.D., Telfer C., Melvin W.T., Murray G.I. Profiling cytochrome P450 expression in ovarian cancer: identification of prognostic markers. Clin. Cancer Res. 2005, 11:7369-7375.
12. Folch J., Lees M., Sloane S.G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226:497-509.
13. Ghayad S.E., Cohen P.A. Inhibitors of the PI3K/Akt/mTOR pathway: new hope for breast cancer patients. Recent Pat. Anticancer Drug Discov. 2010, 5:29-57.
14. Guo M., Roman R.J., Falck J.R., Edwards P.A., Scicli A.G. Human U251 glioma cell proliferation is suppressed by HET0016 [N-hydroxy-N'-(4-butyl-2-methylphenyl)formamidine], a selective inhibitor of CYP4A. J. Pharmacol. Exp. Ther. 2005, 315:526-533.
15. Guo M., Roman R.J., Fenstermacher J.D., Brown S.L., Falck J.R., Arbab A.S., Edwards P.A., Scicli A.G. 9L gliosarcoma cell proliferation and tumor growth in rats are suppressed by N-hydroxy-N'-(4-butyl-2-methylphenol) formamidine (HET0016), a selective inhibitor of CYP4A. J. Pharmacol. Exp. Ther. 2006, 317:97-108.
16. Guo A.M., Arbab A.S., Falck J.R., Chen P., Edwards P.A., Roman R.J., Scicli A.G. Activation of vascular endothelial growth factor through reactive oxygen species mediates 20-hydroxyeicosatetraenoic acid-induced endothelial cell proliferation. J. Pharmacol. Exp. Ther. 2007, 321:18-27.
17. Guo A.M., Sheng J., Scicli G.M., Arbab A.S., Lehman N.L., Edwards P.A., Falck J.R., Roman R.J., Scicli A.G. Expression of CYP4A1 in U251 human glioma cell induces hyperproliferative phenotype in vitro and rapidly growing tumors in vivo. J. Pharmacol. Exp. Ther. 2008, 327:10-19.
18. Hsieh M.C., Hu W.P., Yu H.S., Wu W.C., Chang L.S., Kao Y.H., Wang J.J. A DC-81-indole conjugate agent suppresses melanoma A375 cell migration partially via interrupting VEGF production and stromal cell-derived factor-1alpha-mediated signaling. Toxicol. Appl. Pharmacol. 2011, 255:150-159.
19. Hsu M.H., Savas U., Griffin K.J., Johnson E.F. Human cytochrome P450 family 4 enzymes: function, genetic variation and regulation. Drug Metab. Rev. 2007, 39:515-538.
20. Kawakami M., Furuhata T., Kimura Y., Yamaguchi K., Hata F., Sasaki K., Hirata K. Expression analysis of vascular endothelial growth factors and their relationships to lymph node metastasis in human colorectal cancer. J. Exp. Clin. Cancer Res. 2003, 22:229-237.
21. Kessenbrock K., Plaks V., Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010, 141:52-67.
22. Lawson N.D., Weinstein B.M. Arteries and veins: making a difference with zebrafish. Nat. Rev. Genet. 2002, 3:674-682.
23. Lee S., Jilani S.M., Nikolova G.V., Carpizo D., Iruela-Arispe M.L. Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J. Cell Biol. 2005, 169:681-691.
24. Lee S.K., Kim J.M., Lee M.Y., Son K.H., Yeom Y.I., Kim C.H., Shin Y., Koh J.S., Han D.C., Kwon B.M. Confirmation of a linkage between H-Ras and MMP-13 expression as well as MMP-9 by chemical genomic approach. Int. J. Cancer 2006, 118:2172-2181.
25. Lei J., Ingbar D.H. Src kinase integrates PI3K/Akt and MAPK/ERK1/2 pathways in T3-induced Na-K-ATPase activity in adult rat alveolar cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2011, 301:L765-L771.
26. Liang Y., Besch-Williford C., Brekken R.A., Hyder S.M. Progestin-dependent progression of human breast tumor xenografts: a novel model for evaluating antitumor therapeutics. Cancer Res. 2007, 67:9929-9936.
27. Lieu C., Kopetz S. The SRC family of protein tyrosine kinases: a new and promising target for colorectal cancer therapy. Clin. Colorectal Cancer 2010, 9:89-94.
28. McAuliffe P.F., Meric-Bernstam F., Mills G.B., Gonzalez-Angulo A.M. Deciphering the role of PI3K/Akt/mTOR pathway in breast cancer biology and pathogenesis. Clin. Breast Cancer 2010, 10(Suppl. 3):S59-S65.
29. Medhora M., Dhanasekaran A., Gruenloh S.K., Dunn L.K., Gabrilovich M., Falck J.R., Harder D.R., Jacobs E.R., Pratt P.F. Emerging mechanisms for growth and protection of the vasculature by cytochrome P450-derived products of arachidonic acid and other eicosanoids. Prostaglandins Other Lipid Mediat. 2007, 82:19-29.
30. Meng F., Henson R., Wehbe-Janek H., Ghoshal K., Jacob S.T., Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 2007, 133:647-658.
31. Murray G.I., Patimalla S., Stewart K.N., Miller I.D., Heys S.D. Profiling the expression of cytochrome P450 in breast cancer. Histopathology 2010, 57:202-211.
32. Nithipatikom K., DiCamelli R.F., Kohler S., Gumina R.J., Falck J.R., Campbell W.B., Gross G.J. Determination of cytochrome P450 metabolites of arachidonic acid in coronary venous plasma during ischemia and reperfusion in dogs. Anal. Biochem. 2001, 292:115-124.
33. Oh S.H., Kim W.Y., Kim J.H., Younes M.N., El-Naggar A.K., Myers J.N., Kies M., Cohen P., Khuri F., Hong W.K., Lee H.Y. Identification of insulin-like growth factor binding protein-3 as a farnesyl transferase inhibitor SCH66336-induced negative regulator of angiogenesis in head and neck squamous cell carcinoma. Clin. Cancer Res. 2006, 12:653-661.
34. Pesta M., Holubec L., Topolcan O., Cerna M., Rupert K., Holubec L.S., Treska V., Kormunda S., Elgrova L., Finek J., Cerny R. Quantitative estimation of matrix metalloproteinases 2 and 7 (MMP-2, MMP-7) and tissue inhibitors of matrix metalloproteinases 1 and 2 (TIMP-1, TIMP-2) in colorectal carcinoma tissue samples. Anticancer. Res. 2005, 25:3387-3391.
35. Reimer C.L., Agata N., Tammam J.G., Bamberg M., Dickerson W.M., Kamphaus G.D., Rook S.L., Milhollen M., Fram R., Kalluri R., Kufe D., Kharbanda S. Antineoplastic effects of chemotherapeutic agents are potentiated by NM-3, an inhibitor of angiogenesis. Cancer Res. 2002, 62:789-795.
36. Reuben S.C., Gopalan A., Petit D.M., Bishayee A. Modulation of angiogenesis by dietary phytoconstituents in the prevention and intervention of breast cancer. Mol. Nutr. Food Res. 2012, 56:14-29.
37. Rieger M.A., Ebner R., Bell D.R., Kiessling A., Rohayem J., Schmitz M., Temme A., Rieber E.P., Weigle B. Identification of a novel mammary-restricted cytochrome P450, CYP4Z1, with overexpression in breast carcinoma. Cancer Res. 2004, 64:2357-2364.
38. Rivera J., Ward N., Hodgson J., Puddey I.B., Falck J.R., Croft K.D. Measurement of 20-hydroxyeicosatetraenoic acid in human urine by gas chromatography-mass spectrometry. Clin. Chem. 2004, 50:224-226.
39. Savas U., Hsu M.H., Johnson E.F. Differential regulation of human CYP4A genes by peroxisome proliferators and dexamethasone. Arch. Biochem. Biophys. 2003, 409:212-220.
40. Savas U., Hsu M.H., Griffin K.J., Bell D.R., Johnson E.F. Conditional regulation of the human CYP4X1 and CYP4Z1 genes. Arch. Biochem. Biophys. 2005, 436:377-385.
41. Schneider B.P., Miller K.D. Angiogenesis of breast cancer. J. Clin. Oncol. 2005, 23:1782-1790.
42. Seki T., Wang M.H., Miyata N., Laniado-Schwartzman M. Cytochrome P450 4A isoform inhibitory profile of N-hydroxy-N'-(4-butyl-2-methylphenyl)-formamidine (HET0016), a selective inhibitor of 20-HETE synthesis. Biol. Pharm. Bull. 2005, 28:1651-1654.
43. Selvakumar P., Lakshmikuttyamma A., Shrivastav A., Das S.B., Dimmock J.R., Sharma R.K. Potential role of N-myristoyltransferase in cancer. Prog. Lipid Res. 2007, 46:1-36.
44. Seta F., Patil K., Bellner L., Mezentsev A., Kemp R., Dunn M.W., Schwartzman M.L. Inhibition of VEGF expression and corneal neovascularization by siRNA targeting cytochrome P450 4B1. Prostaglandins Other Lipid Mediat. 2007, 84:116-127.
45. Sudhakar A., Nyberg P., Keshamouni V.G., Mannam A.P., Li J., Sugimoto H., Cosgrove D., Kalluri R. Human alpha1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by alpha1beta1 integrin. J. Clin. Invest. 2005, 115:2801-2810.
46. Summy J.M., Gallick G.E. Src family kinases in tumor progression and metastasis. Cancer Metastasis Rev. 2003, 22:337-358.
47. Syed D.N., Afaq F., Sarfaraz S., Khan N., Kedlaya R., Setaluri V., Mukhtar H. Delphinidin inhibits cell proliferation and invasion via modulation of Met receptor phosphorylation. Toxicol. Appl. Pharmacol. 2008, 231:52-60.
48. Tobia C., De Sena G., Presta M. Zebrafish embryo, a tool to study tumor angiogenesis. Int. J. Dev. Biol. 2011, 55:505-509.
49. Vona-Davis L., Rose D.P. Angiogenesis, adipokines and breast cancer. Cytokine Growth Factor Rev. 2009, 20:193-201.
50. Waleh N.S., Murphy B.J., Zaveri N.T. Increase in tissue inhibitor of metalloproteinase-2 (TIMP-2) levels and inhibition of MMP-2 activity in a metastatic breast cancer cell line by an anti-invasive small molecule SR13179. Cancer Lett. 2010, 289:111-118.
51. Wang D.S., Miller R., Shaw R., Shaw G. The pleckstrin homology domain of human beta I sigma II spectrin is targeted to the plasma membrane in vivo. Biochem. Biophys. Res. Commun. 1996, 225:420-426.
52. Yu W., Chen L., Yang Y.Q., Falck J.R., Guo A.M., Li Y., Yang J. Cytochrome P450 omega-hydroxylase promotes angiogenesis and metastasis by upregulation of VEGF and MMP-9 in non-small cell lung cancer. Cancer Chemother. Pharmacol. 2011, 68:619-629.
53. Zollner A., Dragan C.A., Pistorius D., Muller R., Bode H.B., Peters F.T., Maurer H.H., Bureik M. Human CYP4Z1 catalyzes the in-chain hydroxylation of lauric acid and myristic acid. Biol. Chem. 2009, 390:313-317.