Inhibition of cytokine signaling in human retinal endothelial cells through downregulation of sphingomyelinases by docosahexaenoic acid

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 6, 2010, Pages 3253-3263

  Opreanu, Madalina ^a   Lydic, Todd A ^a   Reid, Gavin E ^a,b   McSorley, kelly M ^a   Esselman, Walter J ^a   Busik, Julia V ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESIPRAMINE; DOCOSAHEXAENOIC ACID; ENZYME INHIBITOR; GW 4869; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; SPHINGOMYELIN PHOSPHODIESTERASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; CYTOKINE; SMALL INTERFERING RNA;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINAL ENDOTHELIAL CELL; SIGNAL TRANSDUCTION; UPREGULATION; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ELECTROSPRAY MASS SPECTROMETRY; ENZYMOLOGY; GENETICS; METABOLISM; POLYMERASE CHAIN REACTION; RETINA BLOOD VESSEL; TANDEM MASS SPECTROMETRY; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

BLOTTING, WESTERN; CYTOKINES; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; ENDOTHELIUM, VASCULAR; GENE SILENCING; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; POLYMERASE CHAIN REACTION; RETINAL VESSELS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPHINGOMYELIN PHOSPHODIESTERASE; TANDEM MASS SPECTROMETRY; VASCULAR CELL ADHESION MOLECULE-1;

EID: 77953272067     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4731     Document Type: Article

References (67)

1. Lecomte M,Paget C Ruggiero D,Wiernsperger N Lagarde M. Docosahexaenoic acid is a major n-3 polyunsaturated fatty acid in bovine retinal microvessels. J Neurochem. 1996;66:2160-2167.
2. SanGiovanni JP, Chew EY, Clemons TE, et al. The relationship of dietary lipid intake and age-related macular degeneration in a case-control study: AREDS report no. 20. Arch Ophthalmol. 2007; 125:671-679.
3. Decsi T, Minda H, Hermann R, et al. Polyunsaturated fatty acids in plasma and erythrocyte membrane lipids of diabetic children. Prostaglandins Leukot Essent Fatty Acids. 2002;67:203-210.
4. Futterman S, Kupfer C. The fatty acid composition of the retinal vasculature of normal and diabetic human eyes. Invest Ophthal-mol. 1968;7:105-08.
5. 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.
6. McLeod DS, Lefer DJ, Merges C, Lutty GA. Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol. 1995;147:642-653.
7. Joussen AM, Murata T, Tsujikawa A, Kirchhof B, Bursell SE, Adamis AP. Leukocyte-mediated endothelial cell injury and death in the diabetic retina. Am J Pathol. 2001;158:147-152.
8. Adamis AP. Is diabetic retinopathy an inflammatory disease? Br J Ophthalmol. 2002;86:363-365.
9. Limb GA, Chignell AH, Green W, LeRoy F, Dumonde DC. Distribution of TNF alpha and its reactive vascular adhesion molecules in fibrovascular membranes of proliferative diabetic retinopathy. Br J Ophthalmol. 1996;80:168-173.
10. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 2004;18: 1450-1452.
11. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endo-thelial growth factor levels in the vitreous of eyes with prolifera-tive diabetic retinopathy. Am J Ophthalmol. 1994;118:445-450.
12. 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.
13. Miyawaki-Shimizu K, Predescu D, Shimizu J, Broman M, Predescu S, Malik AB. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am J Physiol Lung Cell Mol Physiol. 2006;290:L405-L413.
14. Li S, Song KS, Lisanti MP. Expression and characterization of recombinant caveolin: purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes. J Biol Chem. 1996;271:568-573.
15. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A. 1995;92:10339-10343.
16. Anderson RG. Caveolae: where incoming and outgoing messengers meet. Proc Natl Acad Sci U S A. 1993;90:10909-10913.
17. Lisanti MP, Tang Z, Scherer PE, Kubler E, Koleske AJ, Sargiacomo M. Caveolae, transmembrane signalling and cellular transformation. Mol Membr Biol. 1995;12:121-124.
18. Edidin M. The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct. 2003;32:257-283.
19. Mathias S, Pena LA, Kolesnick RN. Signal transduction of stress via ceramide. Biochem J. 1998;335(pt 3):465-480.
20. Bilderback TR, Gazula VR, Lisanti MP, Dobrowsky RT. Caveolin interacts with Trk A and p75(NTR) and regulates neurotrophin signaling pathways. J Biol Chem. 1999;274:257-263.
21. Cremesti A, Paris F, Grassme H, et al. Ceramide enables fas to cap and kill. J Biol Chem. 2001;276:23954-23961.
22. Liu P, Anderson RG. Compartmentalized production of ceramide at the cell surface. J Biol Chem. 1995;270:27179-27185.
23. Marchesini N, Hannun YA. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol. 2004;82: 27-44.
24. Tani M, Hannun YA. Neutral sphingomyelinase 2 is palmitoylated on multiple cysteine residues: role of palmitoylation in subcellular localization. J Biol Chem. 2007;282:10047-10056.
25. Tani M, Ito M, Igarashi Y. Ceramide/sphingosine/sphingosine 1-phosphate metabolism on the cell surface and in the extracellular space. Cell Signal. 2007;19:229-237.
26. Grassme H, Schwarz H, Gulbins E. Molecular mechanisms of cer-amide-mediated CD95 clustering. Biochem Biophys Res Commun. 2001;284:1016-1030.
27. Schissel SL, Jiang X, Tweedie-Hardman J, et al. Secretory sphingo-myelinase, a product of the acid sphingomyelinase gene, can hydrolyze atherogenic lipoproteins at neutral pH: implications for atherosclerotic lesion development. J Biol Chem. 1998;273:2738- 2746.
28. Smith EL, Schuchman EH. The unexpected role of acid sphingo-myelinase in cell death and the pathophysiology of common diseases. FASEB J. 2008;22:3419-3431.
29. Kolesnick R. The therapeutic potential of modulating the cer-amide/sphingomyelin pathway. J Clin Invest. 2002;110:3-8.
30. Pierini LM, Maxfield FR. Flotillas of lipid rafts fore and aft. Proc Natl Acad Sci U S A. 2001;98:9471-9473.
31. Shaul PW, Anderson RG. Role of plasmalemmal caveolae in signal transduction. Am J Physiol. 1998;275:L843-L851.
32. Simons K, Ikonen E. Functional rafts in cell membranes. Nature.1997;387:569-572.
33. Smart EJ, Graf GA, McNiven MA, et al. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol. 1999;19:7289-7304.
34. Grassme H, Riethmuller J, Gulbins E. Biological aspects of ceram-ide-enriched membrane domains. Prog Lipid Res. 2007;46:161-170
35. Holopainen JM, Subramanian M, Kinnunen PK. Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcho-line/sphingomyelin membrane. Biochemistry. 1998;37:17562- 17570.
36. Kolesnick RN, Goni FM, Alonso A. Compartmentalization of cer-amide signaling: physical foundations and biological effects. J Cell Physiol. 2000;184:285-300.
37. Nurminen TA, Holopainen JM, Zhao H, Kinnunen PK. Observation of topical catalysis by sphingomyelinase coupled to microspheres. J Am Chem Soc. 2002;124:12129-12134.
38. Bertrand D. [Mental health and cultural issues: the return of Kh-mers from France to Cambodia for healing purposes]. Sante. 1997; 7:330-334.
39. Monks CR, Freiberg BA, Kupfer H, Sciaky N, Kupfer A. Three-dimensional segregation of supramolecular activation clusters in T cells. Nature. 1998;395:82-86.
40. Ko YG, Lee JS, Kang YS, Ahn JH, Seo JS. TNF-alpha-mediated apoptosis is initiated in caveolae-like domains. J Immunol. 1999; 162:7217-7223.
41. Martin MU, Wesche H. Summary and comparison of the signaling mechanisms of the Toll/interleukin-1 receptor family. Biochim Biophys Acta. 2002;1592:265-280.
42. Busik JV, Mohr S, Grant MB. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on para-crine mediators. Diabetes. 2008;57:1952-1965.
43. Jump DB, Clarke SD, MacDougald O, Thelen A. Polyunsaturated fatty acids inhibit S14 gene transcription in rat liver and cultured hepatocytes. Proc Natl Acad Sci U S A. 1993;90:8454-8458.
44. Botolin D, Jump DB. Selective proteolytic processing of rat hepatic sterol regulatory element binding protein-1 (SREBP-1) and SREBP-2 during postnatal development.
45. Biol Chem. 2003;278:6959- 6962.
46. Agardh E, Gustavsson C, Hagert P, Nilsson M, Agardh CD. Modifying a standard method allows simultaneous extraction of RNA and protein, enabling detection of enzymes in the rat retina with low expressions and protein levels. Metabolism. 2006;55:168-174.
47. Busik JV, Reid GE, Lydic TA. Global analysis of retina lipids by complementary precursor ion and neutral loss mode tandem mass spectrometry. Methods Mol Biol. 2009;579:33-70.
48. Kielczewski JL, Jarajapu Y, McFarland EL, et al. Insulin-like growth factor binding protein-3 mediates vascular repair by enhancing nitric oxide generation. Circ Res. 2009;105:897-905.
49. Heinrich M, Wickel M, Schneider-Brachert W, et al. Cathepsin D targeted by acid sphingomyelinase-derived ceramide. EMBO J. 1999;18:5252-5263.
50. Kolzer M, Werth N, Sandhoff K. Interactions of acid sphingomy-elinase and lipid bilayers in the presence of the tricyclic antide-pressant desipramine. FEBS Lett. 2004;559:96-98.
51. Marchesini N, Luberto C, Hannun YA. Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J Biol Chem. 2003;278:13775-13783.
52. 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 Ophthal-mol Vis Sci. 2007;48:18-26.
53. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr. 2006;83:1505S-519S.
54. Orlow Mathias CS, Younes A, Kan CI, Joseph C, Kolesnick RN. Activation of the sphingomyelin signaling pathway in intact EL4 cells and in a cell-free system by IL-1 beta. Science. 1993;259:519-522.
55. Yang Z, Costanzo M, Golde DW, Kolesnick RN. Tumor necrosis factor activation of the sphingomyelin pathway signals nuclear factor kappa B translocation in intact HL-60 cells. J Biol Chem. 1993;268:20520-20523.
56. Marathe S, Schissel SL, Yellin MJ, et al. Human vascular endothelial cells are a rich and regulatable source of secretory sphingo-myelinase: implications for early atherogenesis and ceramide-me-diated cell signaling. J Biol Chem. 1998;273:4081-4088.
57. York RD, Yao H, Dillon T, et al. Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature. 1998; 392:622-626.
58. Dressler KA, Mathias S, Kolesnick RN. Tumor necrosis factor-alpha activates the sphingomyelin signal transduction pathway in a cell-free system. Science. 1992;255:1715-1718.
59. Stylianou E, O'Neill LA, Rawlinson L, Edbrooke MR, Woo P, Sak-latvala J. Interleukin 1 induces NF-kappa B through its type I but not its type II receptor in lymphocytes. J Biol Chem. 1992;267: 15836-15841.
60. Monaco C, Paleolog E. Nuclear factor kappaB: a potential therapeutic target in atherosclerosis and thrombosis. Cardiovasc Res. 2004;61:671-682.
61. Natoli G, Costanzo A, Guido F, Moretti F, Levrero M. Apoptotic, non-apoptotic, and anti-apoptotic pathways of tumor necrosis factor signalling. Biochem Pharmacol. 1998;56:915-920.
62. Schutze S, Potthoff K, Machleidt T, Berkovic D, Wiegmann K, Kronke M. TNF activates NF-kappa B by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell. 1992;71:765-776.
63. Marcheselli VL, Hong S, Lukiw WJ, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and proinflammatory gene expression. J Biol Chem. 2003;278:43807- 43817.
64. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and pro-tectin D1 activate inflammation-resolution programmes. Nature. 2007;447:869-874.
65. Serhan CN, Hong S, Gronert K, et al. Resolvins: a family of bioac-tive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med. 2002;196:1025-1037.
66. Musiek ES, Brooks JD, Joo M, et al. Electrophilic cyclopentenone neuroprostanes are anti-inflammatory mediators formed from the peroxidation of the omega-3 polyunsaturated fatty acid docosa-hexaenoic acid. J Biol Chem. 2008;283:19927-19935.
67. Kolesnick R, Fuks Z. Radiation and ceramide-induced apoptosis. Oncogene. 2003;22:5897-5906.