12/15-Lipoxygenase-Derived Lipid Metabolites Induce Retinal Endothelial Cell Barrier Dysfunction: Contribution of NADPH Oxidase

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Othman, Amira ^a,b   Ahmad, Saif ^a   Megyerdi, Sylvia ^a   Mussell, Rene ^a   Choksi, Karishma ^a   Maddipati, Krishna Rao ^c   Elmarakby, Ahmed ^a   Rizk, Nasser ^d   Al Shabrawey, Mohamed ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b MANSOURA UNIVERSITY   (Egypt)

^c WAYNE STATE UNIVERSITY   (United States)

^d Qatar University ^*  (Qatar)

Author keywords

[No Author keywords available]

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXYICOSATETRAENOIC ACID; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; BAICALEIN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; OXIDOREDUCTASE INHIBITOR; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 2;

ANIMAL CELL; ARTICLE; BLOOD RETINA BARRIER; BLOOD VESSEL PERMEABILITY; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC RETINOPATHY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; IMPEDANCE; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MONOLAYER CULTURE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; RETINA CELL; RETINA ENDOTHELIUM CELL;

12-HYDROXY-5,8,10,14-EICOSATETRAENOIC ACID; ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONATE 15-LIPOXYGENASE; BIOLOGICAL TRANSPORT; CELL MEMBRANE PERMEABILITY; DEXTRANS; DIABETIC RETINOPATHY; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; ENZYME INHIBITORS; FLAVANONES; FLUORESCEIN-5-ISOTHIOCYANATE; GENE EXPRESSION; HYDROXYEICOSATETRAENOIC ACIDS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; NADPH OXIDASE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; REACTIVE OXYGEN SPECIES; RETINA; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84874282084     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057254     Document Type: Article

References (56)

1. Antonetti DA, Lieth E, Barber AJ, Gardner TW, (1999) Molecular mechanisms of vascular permeability in diabetic retinopathy. Semin Ophthalmol 14: 240-248.
2. Antonetti DA, Barber AJ, Hollinger LA, Wolpert EB, Gardner TW, (1999) Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors. J Biol Chem 274: 23463-23467.
3. Leal EC, Manivannan A, Hosoya K, Terasaki T, Cunha-Vaz J, et al. (2007) Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest Ophthalmol Vis Sci 48: 5257-5265.
4. Khan ZA, Chakrabarti S, (2007) Cellular signaling and potential new treatment targets in diabetic retinopathy. Exp Diabetes Res 2007: 31867.
5. Khalfaoui T, Lizard G, Ouertani-Meddeb A, (2008) Adhesion molecules (ICAM-1 and VCAM-1) and diabetic retinopathy in type 2 diabetes. J Mol Histol 39: 243-249.
6. Chen W, Jump DB, Grant MB, Esselman WJ, Busik JV, (2003) Dyslipidemia, but not hyperglycemia, induces inflammatory adhesion molecules in human retinal vascular endothelial cells. Invest Ophthalmol Vis Sci 44: 5016-5022.
7. Bhatia S, Shukla R, Venkata Madhu S, Kaur Gambhir J, Madhava Prabhu K, (2003) Antioxidant status, lipid peroxidation and nitric oxide end products in patients of type 2 diabetes mellitus with nephropathy. Clin Biochem 36: 557-562.
8. Yamamoto S, (1992) Mammalian lipoxygenases: molecular structures and functions. Biochim Biophys Acta 1128: 117-131.
9. Funk CD, Keeney DS, Oliw EH, Boeglin WE, Brash AR, (1996) Functional expression and cellular localization of a mouse epidermal lipoxygenase. J Biol Chem 271: 23338-23344.
10. Al-Shabrawey M, Mussell R, Kahook K, Tawfik A, Eladl M, et al. (2011) Increased Expression and Activity of 12-Lipoxygenase in Oxygen-Induced Ischemic Retinopathy and Proliferative Diabetic Retinopathy: Implications in Retinal Neovascularization. Diabetes 60: 614-624.
11. Cyrus T, Witztum JL, Rader DJ, Tangirala R, Fazio S, et al. (1999) Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J Clin Invest 103: 1597-1604.
12. Nozawa K, Tuck ML, Golub M, Eggena P, Nadler JL, et al. (1990) Inhibition of lipoxygenase pathway reduces blood pressure in renovascular hypertensive rats. Am J Physiol 259: H1774-1780.
13. Natarajan R, Nadler JL, (2003) Lipoxygenases and lipid signaling in vascular cells in diabetes. Front Biosci 8: s783-795.
14. Haneda M, Araki S, Togawa M, Sugimoto T, Isono M, et al. (1997) Mitogen-activated protein kinase cascade is activated in glomeruli of diabetic rats and glomerular mesangial cells cultured under high glucose conditions. Diabetes 46: 847-853.
15. Gubitosi-Klug RA, Talahalli R, Du Y, Nadler JL, Kern TS, (2008) 5-Lipoxygenase, but not 12/15-lipoxygenase, contributes to degeneration of retinal capillaries in a mouse model of diabetic retinopathy. Diabetes 57: 1387-1393.
16. Talahalli R, Zarini S, Sheibani N, Murphy RC, Gubitosi-Klug RA, (2010) Increased synthesis of leukotrienes in the mouse model of diabetic retinopathy. Invest Ophthalmol Vis Sci 51: 1699-1708.
17. Yang LP, Sun HL, Wu LM, Guo XJ, Dou HL, et al. (2009) Baicalein reduces inflammatory process in a rodent model of diabetic retinopathy. Invest Ophthalmol Vis Sci 50: 2319-2327.
18. Ellis EA, Guberski DL, Somogyi-Mann M, Grant MB, (2000) Increased H2O2, vascular endothelial growth factor and receptors in the retina of the BBZ/Wor diabetic rat. Free Radic Biol Med 28: 91-101.
19. Inoguchi T, Tsubouchi H, Etoh T, Kakimoto M, Sonta T, et al. (2003) A possible target of antioxidative therapy for diabetic vascular complications-vascular NAD(P)H oxidase. Curr Med Chem 10: 1759-1764.
20. Sonta T, Inoguchi T, Tsubouchi H, Sekiguchi N, Kobayashi K, et al. (2004) Evidence for contribution of vascular NAD(P)H oxidase to increased oxidative stress in animal models of diabetes and obesity. Free Radic Biol Med 37: 115-123.
21. Griendling KK, Sorescu D, Ushio-Fukai M, (2000) NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501.
22. Al-Shabrawey M, Bartoli M, El-Remessy AB, Ma G, Matragoon S, et al. (2008) Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Invest Ophthalmol Vis Sci 49: 3231-3238.
23. Al-Shabrawey M, Rojas M, Sanders T, Behzadian A, El-Remessy A, et al. (2008) Role of NADPH oxidase in retinal vascular inflammation. Invest Ophthalmol Vis Sci 49: 3239-3244.
24. Li J, Wang JJ, Yu Q, Chen K, Mahadev K, et al. (2010) Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4. Diabetes 59: 1528-1538.
25. Al-Shabrawey M, Bartoli M, El-Remessy AB, Platt DH, Matragoon S, et al. (2005) Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy. Am J Pathol 167: 599-607.
26. Barber AJ, Antonetti DA, Kern TS, Reiter CE, Soans RS, et al. (2005) The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci 46: 2210-2218.
27. Behzadian MA, Wang XL, Al-Shabrawey M, Caldwell RB, (1998) Effects of hypoxia on glial cell expression of angiogenesis-regulating factors VEGF and TGF-beta. Glia 24: 216-225.
28. Ablonczy Z, Crosson CE, (2007) VEGF modulation of retinal pigment epithelium resistance. Exp Eye Res 85: 762-771.
29. Whittles CE, Pocock TM, Wedge SR, Kendrew J, Hennequin LF, et al. (2002) ZM323881, a novel inhibitor of vascular endothelial growth factor-receptor-2 tyrosine kinase activity. Microcirculation 9: 513-522.
30. Cao R, Jensen LD, Soll I, Hauptmann G, Cao Y, (2008) Hypoxia-induced retinal angiogenesis in zebrafish as a model to study retinopathy. PLoS One 3: e2748.
31. Endo A, Fukuhara S, Masuda M, Ohmori T, Mochizuki N, (2003) Selective inhibition of vascular endothelial growth factor receptor-2 (VEGFR-2) identifies a central role for VEGFR-2 in human aortic endothelial cell responses to VEGF. J Recept Signal Transduct Res 23: 239-254.
32. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD, Davidson BL, (1998) Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res 82: 1298-1305.
33. Hordijk PL, (2006) Regulation of NADPH oxidases: the role of Rac proteins. Circ Res 98: 453-462.
34. Rojas M, Zhang W, Lee DL, Romero MJ, Nguyen DT, et al. (2010) Role of IL-6 in angiotensin II-induced retinal vascular inflammation. Invest Ophthalmol Vis Sci 51: 1709-1718.
35. Tawfik A, Sanders T, Kahook K, Akeel S, Elmarakby A, et al. (2009) Suppression of retinal peroxisome proliferator-activated receptor gamma in experimental diabetes and oxygen-induced retinopathy: role of NADPH oxidase. Invest Ophthalmol Vis Sci 50: 878-884.
36. Cheung CM, Vania M, Ang M, Chee SP, Li J, (2012) Comparison of aqueous humor cytokine and chemokine levels in diabetic patients with and without retinopathy. Mol Vis 18: 830-837.
37. Brash AR, (1999) Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J Biol Chem 274: 23679-23682.
38. Natarajan R, Nadler JL, (2004) Lipid inflammatory mediators in diabetic vascular disease. Arterioscler Thromb Vasc Biol 24: 1542-1548.
39. Kuhn H, Walther M, Kuban RJ, (2002) Mammalian arachidonate 15-lipoxygenases structure, function, and biological implications. Prostaglandins Other Lipid Mediat 68-69: 263-290.
40. Chen XS, Kurre U, Jenkins NA, Copeland NG, Funk CD, (1994) cDNA cloning, expression, mutagenesis of C-terminal isoleucine, genomic structure, and chromosomal localizations of murine 12-lipoxygenases. J Biol Chem 269: 13979-13987.
41. Cui L, Zhang X, Yang R, Liu L, Wang L, et al. (2010) Baicalein is neuroprotective in rat MCAO model: role of 12/15-lipoxygenase, mitogen-activated protein kinase and cytosolic phospholipase A2. Pharmacol Biochem Behav 96: 469-475.
42. Zarbock A, Distasi MR, Smith E, Sanders JM, Kronke G, et al. (2009) Improved survival and reduced vascular permeability by eliminating or blocking 12/15-lipoxygenase in mouse models of acute lung injury (ALI). J Immunol 183: 4715-4722.
43. Ma J, Natarajan R, LaPage J, Lanting L, Kim N, et al. (2005) 12/15-lipoxygenase inhibitors in diabetic nephropathy in the rat. Prostaglandins Leukot Essent Fatty Acids 72: 13-20.
44. Wen Y, Gu J, Vandenhoff GE, Liu X, Nadler JL, (2008) Role of 12/15-lipoxygenase in the expression of MCP-1 in mouse macrophages. Am J Physiol Heart Circ Physiol 294: H1933-1938.
45. Bolick DT, Orr AW, Whetzel A, Srinivasan S, Hatley ME, et al. (2005) 12/15-lipoxygenase regulates intercellular adhesion molecule-1 expression and monocyte adhesion to endothelium through activation of RhoA and nuclear factor-kappaB. Arterioscler Thromb Vasc Biol 25: 2301-2307.
46. Kang SW, Natarajan R, Shahed A, Nast CC, LaPage J, et al. (2003) Role of 12-lipoxygenase in the stimulation of p38 mitogen-activated protein kinase and collagen alpha5(IV) in experimental diabetic nephropathy and in glucose-stimulated podocytes. J Am Soc Nephrol 14: 3178-3187.
47. Woo CH, Lee ZW, Kim BC, Ha KS, Kim JH, (2000) Involvement of cytosolic phospholipase A2, and the subsequent release of arachidonic acid, in signalling by rac for the generation of intracellular reactive oxygen species in rat-2 fibroblasts. Biochem J 348 Pt 3: 525-530.
48. Choi JA, Kim EY, Song H, Kim C, Kim JH, (2008) Reactive oxygen species are generated through a BLT2-linked cascade in Ras-transformed cells. Free Radic Biol Med 44: 624-634.
49. Nardi M, Feinmark SJ, Hu L, Li Z, Karpatkin S, (2004) Complement-independent Ab-induced peroxide lysis of platelets requires 12-lipoxygenase and a platelet NADPH oxidase pathway. J Clin Invest 113: 973-980.
50. Ushio-Fukai M, (2006) Redox signaling in angiogenesis: role of NADPH oxidase. Cardiovasc Res 71: 226-235.
51. Ushio-Fukai M, (2007) VEGF signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 9: 731-739.
52. Conrad M, Sandin A, Forster H, Seiler A, Frijhoff J, et al. (2010) 12/15-lipoxygenase-derived lipid peroxides control receptor tyrosine kinase signaling through oxidation of protein tyrosine phosphatases. Proc Natl Acad Sci U S A 107: 15774-15779.
53. Tabet F, Schiffrin EL, Callera GE, He Y, Yao G, et al. (2008) Redox-sensitive signaling by angiotensin II involves oxidative inactivation and blunted phosphorylation of protein tyrosine phosphatase SHP-2 in vascular smooth muscle cells from SHR. Circ Res 103: 149-158.
54. Young BA, Sui X, Kiser TD, Hyun SW, Wang P, et al. (2003) Protein tyrosine phosphatase activity regulates endothelial cell-cell interactions, the paracellular pathway, and capillary tube stability. Am J Physiol Lung Cell Mol Physiol 285: L63-75.
55. Gaits F, Li RY, Ragab A, Ragab-Thomas JM, Chap H, (1995) Increase in receptor-like protein tyrosine phosphatase activity and expression level on density-dependent growth arrest of endothelial cells. Biochem J 311 (Pt 1): 97-103.
56. Guo DQ, Wu LW, Dunbar JD, Ozes ON, Mayo LD, et al. (2000) Tumor necrosis factor employs a protein-tyrosine phosphatase to inhibit activation of KDR and vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 275: 11216-11221.