Epoxy metabolites of docosahexaenoic acid (DHA) inhibit angiogenesis, tumor growth, and metastasis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 16, 2013, Pages 6530-6535

  Zhang, Guodong ^a   Panigrahy, Dipak ^b,c   Mahakian, Lisa M ^d   Yang, Jun ^a   Liu, Jun Yan ^a   Lee, Kin Sing Stephen ^a   Wettersten, Hiromi I ^e   Ulu, Arzu ^a   Hu, Xiaowen ^d   Tam, Sarah ^d   Hwang, Sung Hee ^a   Ingham, Elizabeth S ^d   Kieran, Mark W ^b,c   Weiss, Robert H ^a,e,f   Ferrara, Katherine W ^d   Hammock, Bruce D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d US Department of Veteran's Affairs Medical Center ^*  (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f The Department of Veteran's Affairs Northern California VA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

10,11 EPOXYDOCOSAPENTAENOIC ACID; 13,14 EPOXYDOCOSAPENTAENOIC ACID; 16,17 EPOXYDOCOSAPENTAENOIC ACID; 19,20 EPOXYDOCOSAPENTAENOIC ACID; 4 [4 [3 (1 ADAMANTYL)UREIDO]CYCLOHEXYLOXY]BENZOIC ACID; 7,8 EPOXYDOCOSAPENTAENOIC ACID; ANGIOGENESIS INHIBITOR; ANTIMETASTATIC AGENT; ANTINEOPLASTIC AGENT; DOCOSAHEXAENOIC ACID; EPOXYICOSATRIENOIC ACID; FIBROBLAST GROWTH FACTOR 2; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROTEINASE; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CELL MIGRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG MECHANISM; DRUG METABOLISM; DRUG POTENTIATION; DRUG STABILITY; ENDOTHELIUM CELL; ENZYME SYNTHESIS; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LOW DRUG DOSE; LUNG METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRIPLE NEGATIVE BREAST CANCER;

ANIMALS; CARCINOMA, LEWIS LUNG; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; EPOXIDE HYDROLASES; EPOXY COMPOUNDS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROSCOPY; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC;

EID: 84876218926     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304321110     Document Type: Article

References (51)

1. Cho E, et al. (2001) Prospective study of dietary fat and the risk of age-related macular degeneration. Am J Clin Nutr 73(2):209-218.
2. Seddon JM, George S, Rosner B (2006) Cigarette smoking, fish consumption, omega-3 fatty acid intake, and associations with age-related macular degeneration: The US Twin Study of Age-Related Macular Degeneration. Arch Ophthalmol 124(7):995-1001.
3. SanGiovanni JP, et al.; Age-Related Eye Disease Study Research Group (2007) The relationship of dietary lipid intake and age-related macular degeneration in a case-control study: AREDS Report No. 20. Arch Ophthalmol 125(5):671-679.
4. Connor KM, et al. (2007) Increased dietary intake of omega-3- polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 13(7):868-873.
5. Wolk A, Larsson SC, Johansson JE, Ekman P (2006) Long-term fatty fish consumption and renal cell carcinoma incidence in women. JAMA 296(11):1371-1376.
6. Hall MN, Chavarro JE, Lee IM, Willett WC, Ma J (2008) A 22-year prospective study of fish, n-3 fatty acid intake, and colorectal cancer risk in men. Cancer Epidemiol Bio-markers Prev 17(5):1136-1143.
7. Brasky TM, Lampe JW, Potter JD, Patterson RE, White E (2010) Specialty supplements and breast cancer risk in the VITamins And Lifestyle (VITAL) Cohort. Cancer Epidemiol Biomarkers Prev 19(7):1696-1708.
8. Berquin IM, et al. (2007) Modulation of prostate cancer genetic risk by omega-3 and omega-6 fatty acids. J Clin Invest 117(7):1866-1875.
9. Rose DP, Connolly JM (1999) Omega-3 fatty acids as cancer chemopreventive agents. Pharmacol Ther 83(3):217-244.
10. Szymczak M, Murray M, Petrovic N (2008) Modulation of angiogenesis by omega-3 polyunsaturated fatty acids is mediated by cyclooxygenases. Blood 111(7):3514-3521.
11. Bagga D, Wang L, Farias-Eisner R, Glaspy JA, Reddy ST (2003) Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion. Proc Natl Acad Sci USA 100(4):1751-1756.
12. Sapieha P, et al. (2011) 5-Lipoxygenase metabolite 4-HDHA is a mediator of the an-tiangiogenic effect of ω-3 polyunsaturated fatty acids. Sci Transl Med 3(69):69ra12.
13. Serhan CN, Petasis NA (2011) Resolvins and protectins in inflammation resolution. Chem Rev 111(10):5922-5943.
14. Capdevila JH, Falck JR, Estabrook RW (1992) Cytochrome P450 and the arachidonate cascade. FASEB J 6(2):731-736.
15. Zeldin DC (2001) Epoxygenase pathways of arachidonic acid metabolism. J Biol Chem 276(39):36059-36062.
16. Arnold C, et al. (2010) Arachidonic acid-metabolizing cytochrome P450 enzymes are targets of omega-3 fatty acids. J Biol Chem 285(43):32720-32733.
17. Jump DB (2002) The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277(11):8755-8758.
18. Arterburn LM, Hall EB, Oken H (2006) Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr 83(6, Suppl):1467S-1476S.
19. Shearer GC, Harris WS, Pedersen TL, Newman JW (2010) Detection of omega-3 oxylipins in human plasma and response to treatment with omega-3 acid ethyl esters. J Lipid Res 51(8):2074-2081.
20. Zivkovic A, et al. (2012) Serum oxylipin profiles in IgA nephropathy patients reflect kidney functional alterations. Metabolomics 8(6):1102-1113.
21. Node K, et al. (1999) Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 285(5431):1276-1279.
22. Morisseau C, et al. (2010) Naturally occurring monoepoxides of eicosapentaenoic acid and docosahexaenoic acid are bioactive antihyperalgesic lipids. J Lipid Res 51(12): 3481-3490.
23. Fisslthaler B, et al. (1999) Cytochrome P450 2C is an EDHF synthase in coronary arteries. Nature 401(6752):493-497.
24. Ye D, et al. (2002) Cytochrome p-450 epoxygenase metabolites of docosahexaenoate potently dilate coronary arterioles by activating large-conductance calcium-activated potassium channels. J Pharmacol Exp Ther 303(2):768-776.
25. Cheranov SY, et al. (2008) An essential role for SRC-activated STAT-3 in 14, 15-EET-induced VEGF expression and angiogenesis. Blood 111(12):5581-5591.
26. Michaelis UR, Fleming I (2006) From endothelium-derived hyperpolarizing factor (EDHF) to angiogenesis: Epoxyeicosatrienoic acids (EETs) and cell signaling. Pharmacol Ther 111(3):584-595.
27. Pozzi A, et al. (2005) Characterization of 5, 6-and 8, 9-epoxyeicosatrienoic acids (5, 6-and 8, 9-EET) as potent in vivo angiogenic lipids. J Biol Chem 280(29):27138-27146.
28. Panigrahy D, et al. (2012) Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice. J Clin Invest 122(1):178-191.
29. Adini A, et al. (2009) Matrigel cytometry: A novel method for quantifying angio-genesis in vivo. J Immunol Methods 342(1-2):78-81.
30. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669-676.
31. Folkman J (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1(1):27-31.
32. Dormond O, Foletti A, Paroz C, Rüegg C (2001) NSAIDs inhibit alpha V beta 3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and an-giogenesis. Nat Med 7(9):1041-1047.
33. Borowsky AD, et al. (2005) Syngeneic mouse mammary carcinoma cell lines: Two closely related cell lines with divergent metastatic behavior. Clin Exp Metastasis 22(1): 47-59.
34. Catella F, Lawson JA, Fitzgerald DJ, FitzGerald GA (1990) Endogenous biosynthesis of arachidonic acid epoxides in humans: Increased formation in pregnancy-induced hypertension. Proc Natl Acad Sci USA 87(15):5893-5897.
35. Imig JD, Hammock BD (2009) Soluble epoxide hydrolase as a therapeutic target for cardiovascular diseases. Nat Rev Drug Discov 8(10):794-805.
36. Morisseau C, Hammock BD (2013) Impact of soluble epoxide hydrolase and epox-yeicosanoids on human health. Annu Rev Pharmacol Toxicol 53:37-58.
37. Hwang SH, Morisseau C, Do Z, Hammock BD (2006) Solid-phase combinatorial approach for the optimization of soluble epoxide hydrolase inhibitors. Bioorg Med Chem Lett 16(22):5773-5777.
38. Chaffer CL, Weinberg RA (2011) A perspective on cancer cell metastasis. Science 331(6024):1559-1564.
39. O'Reilly MS, et al. (1994) Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315-328.
40. Panigrahy D, Kaipainen A, Greene ER, Huang S (2010) Cytochrome P450-derived ei-cosanoids: The neglected pathway in cancer. Cancer Metastasis Rev 29(4):723-735.
41. Skobe M, et al. (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7(2):192-198.
42. Chen HX, Cleck JN (2009) Adverse effects of anticancer agents that target the VEGF pathway. Nat Rev Clin Oncol 6(8):465-477.
43. Frömel T, et al. (2012) Soluble epoxide hydrolase regulates hematopoietic progenitor cell function via generation of fatty acid diols. Proc Natl Acad Sci USA 109(25): 9995-10000.
44. Hu J, Popp R, Fleming I (2011) Genetic deletion and pharmacological inhibition of the soluble epoxide hydrolase attenuate angiogenesis in the murine retina. Acta Physi-ologica 201(Supplement 682):P045.
45. Newman JW, Morisseau C, Hammock BD (2005) Epoxide hydrolases: Their roles and interactions with lipid metabolism. Prog Lipid Res 44(1):1-51.
46. Jiang J-G, et al. (2005) Cytochrome P450 2J2 promotes the neoplastic phenotype of carcinoma cells and is up-regulated in human tumors. Cancer Res 65(11):4707-4715.
47. Murray GI, Patimalla S, Stewart KN, Miller ID, Heys SD (2010) Profiling the expression of cytochrome P450 in breast cancer. Histopathology 57(2):202-211.
48. Mitra R, et al. (2011) CYP3A4 mediates growth of estrogen receptor-positive breast cancer cells in part by inducing nuclear translocation of phospho-Stat3 through biosynthesis of (±)-14, 15-epoxyeicosatrienoic acid (EET). J Biol Chem 286(20):17543-17559.
49. Jiang J-G, et al. (2007) Cytochrome p450 epoxygenase promotes human cancer metastasis. Cancer Res 67(14):6665-6674.
50. Liu JY, et al. (2009) Sorafenib has soluble epoxide hydrolase inhibitory activity, which contributes to its effect profile in vivo. Mol Cancer Ther 8(8):2193-2203.
51. Yang J, Schmelzer K, Georgi K, Hammock BD (2009) Quantitative profiling method for oxylipin metabolome by liquid chromatography electrospray ionization tandem mass spectrometry. Anal Chem 81(19):8085-8093.