Docosahexaenoic acid improves the nitroso-redox balance and reduces VEGF-mediated angiogenic signaling in microvascular endothelial cells

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 12, 2010, Pages 6815-6825

  Matesanz, Nuria ^a   Park, Grace ^a   McAllister, Hollie ^a   Leahey, William ^a   Devine, Adrian ^a   Mcveigh, Gary E ^a   Gardiner, Tom A ^a   Mcdonald, Denise M ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; DOCOSAHEXAENOIC ACID; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ICOSAPENTAENOIC ACID; NITRITE; NITROSO DERIVATIVE; OMEGA 3 FATTY ACID; SUPEROXIDE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; FRACTIONATION; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; RETINA; RETINA BLOOD VESSEL; RETINA NEOVASCULARIZATION; SUCROSE GRADIENT; WESTERN BLOTTING; WOUND HEALING IMPAIRMENT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CATTLE; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; ENDOTHELIUM, VASCULAR; FLUORESCENT DYES; IN SITU NICK-END LABELING; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; NITROSATION; OXIDATION-REDUCTION; RETINAL VESSELS; SIGNAL TRANSDUCTION; SUPEROXIDES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

EID: 79955978712     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-5339     Document Type: Article

References (54)

1. Yang SP, Morita I, Murota S-I. Eicosapentaenoic acid attenuates vascular endothelial growth factor-induced proliferation via inhibiting Flk-1 receptor expression in bovine carotid artery endothelial cells. J Cell Physiol. 1998;176:342-349.
2. Tsuji M, Murota S, Morita I. Docosapentaenoic acid (22:5, n-3) suppressed tube-forming activity in endothelial cells induced by vascular endothelial growth factor. Prostaglandins Leukot Essent Fatty Acids. 2003;68:337-342.
3. Karmali R, Marsh J, Fuchs C. Effect of omega-3 fatty acids on growth of a rat mammary tumor. J Natl Cancer Inst. 1984;73:457-461.
4. Connor KM, SanGiovanni JP, Lofqvist C, et al. Increased dietary intake of [omega]-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med. 2007;13:868-873.
5. Brooks SE, Gu X, Samuel S, et al. Reduced severity of oxygeninduced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci. 2001;42:222-228.
6. Saito Y, Uppal A, Byfield G, Budd S, Hartnett ME. Activated NAD(P)H oxidase from supplemental oxygen induces neovascularization independent of VEGF in retinopathy of prematurity model. Invest Ophthalmol Vis Sci. 2008;49:1591-1598.
7. Uno K, Merges CA, Grebe R, Lutty GA, Prow TW. Hyperoxia inhibits several critical aspects of vascular development. Dev Dyn. 2007;236:981-990.
8. Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, et al. Transarachidonic acids generated during nitrative stress induce a thrombospondin- 1-dependent microvascular degeneration. Nat Med. 2005;11:1339-1345.
9. Ziche M, Morbidelli L, Choudhuri R, et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest. 1997;99:2625-2634.
10. Papapetropoulos A, García-Carden ̃a G, Madri J, Sessa W. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest. 1997;100:3131-3139.
11. Ushio-Fukai M, Alexander R. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem. 2004;264:85-97.
12. Al-Shabrawey M, Bartoli M, El-Remessy AB, et al. Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy. Am J Pathol. 2005;167:599-607.
13. El-Remessy AB, Al-Shabrawey M, Platt DH, et al. Peroxynitrite mediates VEGF's angiogenic signal and function via a nitrationindependent mechanism in endothelial cells. Am J Pathol. 2007; 21:2528-2539.
14. Shaul PW, Smart EJ, Robinson LJ, et al. Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem. 1996;271:6518-6522.
15. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Beliveau R. Regulation of vascular endothelial growth factor receptor- 2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell. 2003;14:334-347.
16. Yang B, Rizzo V. TNF- potentiates protein-tyrosine nitration through activation of NADPH oxidase and eNOS localized in membrane rafts and caveolae of bovine aortic endothelial cells. Am J Physiol Heart Circ Physiol. 2007;292:H954-H962.
17. Garcia-Cardena G, Martasek P, Masters BS, et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin: functional significance of the NOS caveolin binding domain in vivo. J Biol Chem. 1997;272:25437-25440.
18. Fulton D, Fontana J, Sowa G, et al. Localization of endothelial nitric-oxide synthase phosphorylated on serine 1179 and nitric oxide in Golgi and plasma membrane defines the existence of two pools of active enzyme. J Biol Chem. 2002;277:4277-4284.
19. Ma DWL, Seo J, Davidson LA, et al. n-3 PUFA alter caveolae lipid composition and resident protein localization in mouse colon. FASEB J. 2004;18:1040-1042.
20. Chen W, Jump DB, Esselman WJ, Busik JV. Inhibition of cytokine signaling in human retinal endothelial cells through modification of caveolae/lipid rafts by docosahexaenoic acid. Invest Ophthalmol Vis Sci. 2007;48:18-26.
21. Jump DB. The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem. 2002;277:8755-8758.
22. Fischer S, Weber P, Dyerberg J. The prostacyclin/thromboxane balance is favourably shifted in Greenland Eskimos. Prostaglandins. 1986;32:235-241.
23. Webler AC, Michaelis UR, Popp R, et al. Epoxyeicosatrienoic acids are part of the VEGF-activated signaling cascade leading to angiogenesis. Am J Physiol Cell Physiol. 2008;295:C1292-C1301.
24. Mukherjee P, Marcheselli V, Serhan C, Bazan N. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc Natl Acad Sci U S A. 2004;101:8491-8496.
25. Szymczak M, Murray M, Petrovic N. Modulation of angiogenesis by (omega)-3 polyunsaturated fatty acids is mediated by cyclooxygenases. Blood. 2008;111:3514-3521.
26. Li Q, Zhang Q, Wang M, et al. Docosahexaenoic acid affects endothelial nitric oxide synthase in caveolae. Arch Biochem Biophys. 2007;466:250-259.
27. Li Q, Zhang Q, Wang M, et al. Eicosapentaenoic acid modifies lipid composition in caveolae and induces translocation of endothelial nitric oxide synthase. Biochimie (Paris). 2007;89:169-177.
28. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand J-L, Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res. 2001;89:866-873.
29. Mori TA, Bao DQ, Burke V, Puddey IB, Beilin LJ. Docosahexaenoic acid but not eicosapentaenoic acid lowers ambulatory blood pressure and heart rate in humans. Hypertension. 1999;34:253-260.
30. Gitlin J, D'Amore P. Culture of retinal capillary cells using selective growth media. Microvasc Res. 1983;26:74-80.
31. Chen W, Esselman WJ, Jump DB, Busik JV. Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci. 2005;46:4342-4347.
32. Lepage G, Roy CC. Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res. 1984;25:1391-1396.
33. Stitt AW, McGoldrick C, Rice-McCaldin A, et al. Impaired retinal angiogenesis in diabetes: role of advanced glycation end products and galectin-3. Diabetes. 2005;54:785-794.
34. Dimmeler S, Dernbach E, Zeiher AM. Phosphorylation of the endothelial nitric oxide synthase at Ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett. 2000;477: 258-262.
35. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. J Biol Chem. 1996;271:9690-9697.
36. McDonald D, Alp N, Channon K. Functional comparison of the endothelial nitric oxide synthase Glu298Asp polymorphic variants in human endothelial cells. Pharmacogenetics. 2004;14: 831-839.
37. Kuriki K, Nagaya T, Tokudome Y, et al. Plasma concentrations of (n-3) highly unsaturated fatty acids are good biomarkers of relative dietary fatty acid intakes: a cross-sectional study. J Nutr. 2003;133: 3643-3650.
38. McDonald D, Coleman G, Bhatwadekar A, Gardiner T, Stitt A. Advanced glycation of the Arg-Gly-Asp (RGD) tripeptide motif modulates retinal microvascular endothelial cell dysfunction. Mol Vis. 2009;15:1509-1520.
39. Massaro M, Habib A, Lubrano L, et al. The omega-3 fatty acid docosahexaenoate attenuates endothelial cyclooxygenase-2 induction through both NADP(H) oxidase and PKC-[1] inhibition. Proc Natl Acad Sci U S A. 2006;103:15184-15189.
40. Guzik TJ, Mussa S, Gastaldi D, et al. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation. 2002;105:1656-1662.
41. Dimmeler S, Haendeler J, Nehls M, Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1(beta)-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32- like proteases. J Exp Med. 1997;185:601-608.
42. Zachary I, Gliki G. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family. Cardiovasc Res. 2001;49:568-581.
43. Webb Y, Hermida-Matsumoto L, Resh MD. Inhibition of protein palmitoylation, raft localization, and T cell signaling by 2-bromopalmitate and polyunsaturated fatty acids. J Biol Chem. 2000;275: 261-270.
44. Stulnig TM, Huber J, Leitinger N, et al. polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J Biol Chem. 2001;276:37335-37340.
45. Woodman SE, Ashton AW, Schubert W, et al. Caveolin-1 knockout mice show an impaired angiogenic response to exogenous stimuli. Am J Path. 2003;162:2059-2068.
46. Sonveaux P, Martinive P, DeWever J, et al. Caveolin-1 expression is critical for vascular endothelial growth factor-induced ischemic hindlimb collateralization and nitric oxide-mediated angiogenesis. Circ Res. 2004;95:154-161.
47. Murohara T, Witzenbichler B, Spyridopoulos I, et al. Role of endothelial nitric oxide synthase in endothelial cell migration. Arterioscler Thromb Vasc Biol. 1999;19:1156-1161.
48. Ebrahimian TG, Heymes C, You D, et al. NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemicneovascularization in mice with type 1 diabetes. Am J Pathol. 2006;169:719-728.
49. Haddad P, Dussault S, Groleau J, et al. Nox2-containing NADPH oxidase deficiency confers protection from hindlimb ischemia in conditions of increased oxidative stress. Arterioscler Thromb Vasc Biol. 2009;29:1522-1528.
50. Li Calzi S, Purich DL, Chang KH, et al. Carbon monoxide and nitric oxide mediate cytoskeletal reorganization in microvascular cells via vasodilator-stimulated phosphoprotein phosphorylation. Diabetes. 2008;57:2488-2494.
51. Ceradini DJ, Yao D, Grogan RH, et al. Decreasing intracellular superoxide corrects defective ischemia-induced new vessel formation in diabetic mice. J Biol Chem. 2008;283:10930 -10938.
52. Emanueli C, Monopoli A, Kraenkel N, et al. Nitropravastatin stimulates reparative neovascularisation and improves recovery from limb ischaemia in type-1 diabetic mice. Br J Pharmacol. 2007;150:873-882.
53. De Caterina RCM, 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;14:1829-1836.
54. McLennan P, Howe P, Abeywardena M, et al. The cardiovascular protective role of docosahexaenoic acid. Eur J Pharmacol. 1996; 300:83-89.