A novel β-oxa polyunsaturated fatty acid downregulates the activation of the IκB kinase/nuclear factor κB pathway, inhibits expression of endothelial cell adhesion molecules, and depresses inflammation

Circulation Research

Volumn 99, Issue 1, 2006, Pages 34-41

  Ferrante, Antonio ^a,c,i   Robinson, Brenton S ^a   Singh, Harmeet ^a   Jersmann, Hubertus P A ^a   Ferrante, Judith V ^a   Huang, Zhi H ^b   Trout, Neil A ^d   Pitt, Michael J ^e   Rathjen, Deborah A ^f   Easton, Christopher J ^g   Poulos, Alf ^a   Prager, Rolf H ^d   Lee, Frank S ^h   Hii, Charles S T ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^d FLINDERS UNIVERSITY   (Australia)

^e Therapeutic Goods and Administration   (Australia)

^f Bionomics Ltd   (Australia)

^g AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

ⁱ WOMEN S AND CHILDREN S HOSPITAL   (Australia)

Author keywords

Adhesion molecules; Endothelial cells; Lipoxygenase; Long chain fatty acids; NF B

Indexed keywords

CELL ADHESION MOLECULE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; POLYUNSATURATED FATTY ACID; TUMOR NECROSIS FACTOR ALPHA; VASCULAR ADHESION PROTEIN 1; ANTIINFLAMMATORY AGENT; ARACHIDONATE 12 LIPOXYGENASE; INTERCELLULAR ADHESION MOLECULE 1; UNSATURATED FATTY ACID; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE ADHERENCE; MOLECULAR DYNAMICS; NEUTROPHIL; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL CORD BLOOD; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; DRUG EFFECT; METABOLISM; MONOCYTE; MOUSE; PHYSIOLOGY; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ARACHIDONATE 12-LIPOXYGENASE; CELL ADHESION; CELLS, CULTURED; DOWN-REGULATION; ENDOTHELIAL CELLS; FATTY ACIDS, UNSATURATED; HUMANS; I-KAPPA B KINASE; INTERCELLULAR ADHESION MOLECULE-1; MICE; MICE, INBRED BALB C; MONOCYTES; NEUTROPHILS; NF-KAPPA B; RESPIRATORY BURST; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 33746207802     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000231292.66084.cd     Document Type: Article

References (33)

1. Samuelsson B. From studies of biochemical mechanisms to novel biological mediators: prostaglandin, endoperoxides, thromboxanes and leukotrienes. In: Les Prix Nobel, The Nobel Prizes, Nobel Prizes: Presentations, Biographies and Lectures. Stockholm, Sweden: Almquist & Wiksell; 1982:153-174.
2. Stamatiou P, Hamid Q, Taha R, Yu W, Issekutz TB, Rokach J, Khanapure SP, Powell WS. 5-oxo ETE induces pulmonary eosinophilia in an integrin-dependent manner in brown Norway rats. J Clin Invest. 1998;102:2165-2172.
3. 2 inhibitors and leukotriene synthesis inhibitors block TNF-induced NF-κB activation. Cytokine. 1999;11:104-110.
4. Serhan CN, Drazen JM. Anti-inflammatory potential of lipoxygenase-derived eicosanoids: a molecular switch at 5 and 15 positions. J Clin Invest. 1997;99:1147-1148.
5. Graber R, Sumida C, Nunez EA. Fatty acids and cell signal transduction. J Lipid Mediat Cell Signal. 1994;2:91-116.
6. Ferrante JV, Huang ZH, Nandoskar M, Hii CST, Robinson BS, Rathjen DA, Poulos A, Morris CP, Ferrante A. Altered responses of human macrophages to lipopolysaccharide by hydroperoxy eicosatetraenoic acid, hydroxy eicosatetraenoic acid and arachidonic acid: inhibition of TNF production. J Clin Invest. 1997;99:1445-1452.
7. Ferrante A, Goh DHB, Harvey DP, Robinson BS, Hii CST, Bates EJ, Hardy SJ, Johnson DW, Poulos A. Neutrophil migration inhibitory properties of polyunsaturated fatty acids: the role of fatty acid structure, metabolism and possible second messenger systems. J Clin Invest. 1994;93:1063-1070.
8. Ferrante A, Hii CST, Costabile M. Regulation of neutrophil functions by long chain fatty acids. In: Dimitry Gabrilovich, ed. The Neutrophils: New Outlook for Old Cells. 2nd ed. London, UK: Imperial College Press; 2005:201-228.
9. Li Y, Ferrante A, Poulos A, Harvey DP. Neutrophil oxygen radical generation: synergistic responses to tumour necrosis factor and mono/polyunsaturated fatty acids. J Clin Invest. 1996;97:1605-1609.
10. Hii CST, Ferrante A, Edwards YS, Huang ZH, Hartfield PJ, Rathjen DA, Poulos A, Murray AW. Activation of mitogen-activated protein kinase by arachidonic acid in rat liver epithelial WB cells by a protein kinase C-dependent mechanism. J Biol Chem. 1995;270:4201-4204.
11. Hii CST, Huang ZH, Bilney A, Costabile M, Murray AW, Rathjen DA, Der CJ, Ferrante A. Stimulation of p38 phosphorylation and activity by arachidonic acid in HeLa cells, HL60 promyelocytic leukemic cells, and human neutrophils. J Biol Chem. 1998;273:19277-19282.
12. Chuang TH, Bohl BP, Bokoch GM. Biologically active lipids are regulators of Rac. GDI complexation. J Biol Chem. 1993;15:268:26206-26211.
13. Simopoulos AP. Omega 3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr. 2002;21:495-505.
14. Pitt MJ, Easton CJ, Moody CJ, Ferrante A, Poulos A, Rathjen DA. Synthesis of polyunsaturated β-oxa fatty acid via rhodium mediated carbenoid insertion. Synthesis. 1997;1240-1242.
15. Pitt MJ, Easton CJ, Ferrante A, Poulos A, Rathjen DA. Synthesis of polyunsaturated β-thia and γ-thia fatty acids from naturally derived polyunsaturated fatty alcohols and in vitro evaluation of their susceptibility to β-oxidation. Chem Phys Lipids. 1998;92:63-69.
16. Huang ZH, Bates EJ, Ferrante JV, Hii CS, Poulos A, Robinson BS, Ferrante A. Inhibition of stimuli-induced endothelial cell intercellular adhesion molecule -1, E-selectin and vascular cellular adhesion molecule-1 expression by arachidonic acid and its hydroxy- and hydroperoxy-derivatives Circ Res. 1997;80:149-158.
17. Andrews NC, Faller DV. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucl Acids Res. 1992;19:2499.
18. Zhao Q, Lee FS. The transcriptional activity of the APP intracellular domain-Fe65 complex is inhibited by activation of the NF-kappaB pathway. Biochemistry. 2003;42:3627-3634.
19. Lee FS, Peters RT, Dang LC, Maniatis T. MEKKI activates both IκB kinase α and IκB kinase β. Proc Natl Acad Sci U S A. 1998;95:9319-9324.
20. Nutchey BK, Kaplan JS, Dwivedi PP, Omdhal JL, Ferrante A, May BK, Hii CS. Molecular action of 1,25-dihydroxyvitamin D3 and phorbol ester on the activation of the rat cytochrome P450C24 (CYP24) promoter: role of MAP kinase activities and identification of an important transcription factor binding site. Biochem J. 2005;389:753-762.
21. De Caterina R, Cybulsky MI, Clinton SK, Gimbrone MA Jr, Libby P. The omega-3 fatty acid docosahexaenoate reduces cytokine-induced expression of proatherogenic and proinflammatory proteins in human endothelial cells. Arterioscler Thromb. 1994;14:1929-1936.
22. Read MA, Whitley MZ, Gupta S, Pierce JW, Best J, Davis RJ, Collins T. Tumor necrosis factor alpha-induced E-selectin expression is activated by the nuclear factor-kappaB and c-JUN N-terminal kinase/p38 mitogen-activated protein kinase pathways. J Biol Chem. 1997;272:2753-2761.
23. Min W, Pober JS. TNF initiates E-selectin transcription in human endothelial cells through parallel TRAF-NF-kappa B and TRAF-RAC/CDC42-JNK-c-Jun/ ATF2 pathways. J Immunol. 1997;159:3508-3518.
24. Weber C, Erl E, Pietsch A, Danesch L, Weber P. Docosahexaenoic acid selectively attenuates induction of vascular cell adhesion molecule-1 and subsequent monocytic cell adhesion to human endothelial cells stimulated by tumor necrosis fact-α. Arterioscler Thromb Vasc Biol. 1995;15:622-628.
25. Costabile M, Hii CS, Robinson BS, Rathjen DA, Pitt M, Easton C, Miller RC, Poulos A, Murray AW, Ferrante A. A novel long chain polyunsaturated fatty acid, beta-Oxa 21:3n-3, inhibits T lymphocyte proliferation, cytokine production, delayed-type hypersensitivity, and carrageenan-induced paw reaction and selectively targets intracellular signals. J Immunol. 2001;167:3980-3987.
26. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994;76:301-314.
27. Kozak W, Archuleta I, Mayfield KP, Kpxak A, Rudolph K, Kluger MJ. Inhibitors of alternative pathways of arachidonate metabolism differentially affect fever in mice. Am J Physiol. 1998;275:R1031-R1040.
28. Hong SH, Avis I, Vos MD, Martinez A, Treston AM, Mulshine JL. Relationship of arachidonic acid metabolizing enzyme expression in epithelial cancer cell lines to the growth effect of selective biochemical inhibitors. Cancer Res. 1999;59:2223-2228.
29. Coffa G, Hill EM. Discovery of an 11 (R)- and 12(S)-lipoxygenase activity in ovaries of the mussel Mytilus edulis. Lipids. 2000;35:1195-1204.
30. Di Margo V, Gianfrani C, De Petrocellis L, Milone A, Cimino G. Polyunsaturated-fatty-acid oxidation in Hydra: regioselectivity, substrate-dependent enantioselectivity and possible biological role. Biochem J. 1994;300:501-507.
31. Marx N, Duez H, Fruchart JC, Staels B. Peroxisome proliferator-activated receptors and atherogenesis: regulators of gene expression in vascular cells. Circ Res. 2004;94:1168-1178.
32. Sethi S, Ziouzenkova O, Ni H, Wagner DD, Plutzky J, Mayadas TN. Oxidized omega-3 fatty acids in fish oil inhibit leukocyte-endothelial interactions through activation of PPAR alpha. Blood. 2002;100:1340-1346.
33. Mishra A, Chaudhary A, Sethi S. Oxidized omega-3 fatty acids inhibit NF-kappaB activation via a PPARalpha-dependent pathway. Arterioscler Thromb Vasc Biol. 2004;24:1621-1627.