15-lipoxygenase-mediated modification of HDL3 impairs eNOS activation in human endothelial cells

Lipids

Volumn 49, Issue 4, 2014, Pages 317-326

  Cutuli, Lucia ^a   Pirillo, Angela ^b,c   Uboldi, Patrizia ^a   Kuehn, Hartmut ^d   Catapano, Alberico L ^a,c  

^a UNIVERSITY OF MILAN   (Italy)

^b Bassini Hospital   (Italy)

^c IRCCS MULTIMEDICA   (Italy)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

15 Lipoxygenase; Caveolae; Endothelial cells; High density lipoprotein; Nitric oxide

Indexed keywords

ARACHIDONATE 15 LIPOXYGENASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; NITRIC OXIDE; NOS3 PROTEIN, HUMAN; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B;

BIOSYNTHESIS; CAVEOLA; CELL MEMBRANE; CHEMISTRY; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION; VASODILATATION;

ARACHIDONATE 15-LIPOXYGENASE; CAVEOLAE; CELL MEMBRANE; CHOLESTEROL, HDL; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; SCAVENGER RECEPTORS, CLASS B; SIGNAL TRANSDUCTION; VASODILATION;

EID: 84898838807     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-014-3888-5     Document Type: Article

References (47)

1. Aird WC (2004) Endothelium as an organ system. Crit Care Med 32:S271-S279
2. Mineo C, Shaul PW (2012) Regulation of eNOS in caveolae. Adv Exp Med Biol 729:51-62
3. Shaul PW (2003) Endothelial nitric oxide synthase, caveolae and the development of atherosclerosis. J Physiol 547:21-33
4. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG (1992) Caveolin, a protein component of caveolae membrane coats. Cell 68:673-682
5. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K (1995) VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92:10339-10343
6. Smart EJ, Ying Y, Donzell WC, Anderson RG (1996) A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271:29427-29435
7. Insel PA, Patel HH (2009) Membrane rafts and caveolae in cardiovascular signaling. Curr Opin Nephrol Hypertens 18:50-56
8. Patel HH, Insel PA (2009) Lipid rafts and caveolae and their role in compartmentation of redox signaling. Antioxid Redox Signal 11:1357-1372
9. Feron O, Saldana F, Michel JB, Michel T (1998) The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem 273:3125-3128
10. Ju H, Zou R, Venema VJ, Venema RC (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 272:18522-18525
11. Fleming I, Busse R (1999) Signal transduction of eNOS activation. Cardiovasc Res 43:532-541
12. Searles CD (2006) Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression. Am J Physiol Cell Physiol 291:C803-C816
13. Fulton D, Fontana J, Sowa G, Gratton JP, Lin M, Li KX, Michell B, Kemp BE, Rodman D, Sessa WC (2002) 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 277:4277-4284
14. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597-601
15. McCabe TJ, Fulton D, Roman LJ, Sessa WC (2000) Enhanced electron flux and reduced calmodulin dissociation may explain "calcium-independent" eNOS activation by phosphorylation. J Biol Chem 275:6123-6128
16. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ (1999) Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem 274:32512-32519
17. Florentin M, Liberopoulos EN, Wierzbicki AS, Mikhailidis DP (2008) Multiple actions of high-density lipoprotein. Curr Opin Cardiol 23:370-378
18. Mineo C, Deguchi H, Griffin JH, Shaul PW (2006) Endothelial and antithrombotic actions of HDL. Circ Res 98:1352-1364
19. Yuhanna IS, Zhu Y, Cox BE, Hahner LD, Osborne-Lawrence S, Lu P, Marcel YL, Anderson RG, Mendelsohn ME, Hobbs HH, Shaul PW (2001) High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat Med 7:853-857
20. Nofer JR, van der Giet M, Tolle M, Wolinska I, von Wnuck Lipinski K, Baba HA, Tietge UJ, Godecke A, Ishii I, Kleuser B, Schafers M, Fobker M, Zidek W, Assmann G, Chun J, Levkau B (2004) HDL induces NO-dependent vasorelaxation via the lysophospholipid receptor S1P3. J Clin Invest 113:569-581
21. Mineo C, Yuhanna IS, Quon MJ, Shaul PW (2003) High density lipoprotein-induced endothelial nitric-oxide synthase activation is mediated by Akt and MAP kinases. J Biol Chem 278:9142-9149
22. Yla-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Witztum JL, Steinberg D (1990) Colocalization of 15-lipoxygenase mRNA and protein with epitopes of oxidized low density lipoprotein in macrophage-rich areas of atherosclerotic lesions. Proc Natl Acad Sci USA 87:6959-6963
23. Pirillo A, Uboldi P, Kuhn H, Catapano AL (2006) 15-Lipoxygenase-mediated modification of high-density lipoproteins impairs SR-BI- and ABCA1-dependent cholesterol efflux from macrophages. Biochim Biophys Acta 1761:292-300
24. Pirillo A, Uboldi P, Bolego C, Kuhn H, Catapano AL (2008) The 15-lipoxygenase-modified high density lipoproteins 3 fail to inhibit the TNF-alpha-induced inflammatory response in human endothelial cells. J Immunol 181:2821-2830
25. Pirillo A, Uboldi P, Ferri N, Corsini A, Kuhn H, Catapano AL (2012) Upregulation of lectin-like oxidized low density lipoprotein receptor 1 (LOX-1) expression in human endothelial cells by modified high density lipoproteins. Biochem Biophys Res Commun 428:230-233
26. Jaffe EA, Nachman RL, Becker CG, Minick CR (1973) Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 52:2745-2756
27. Havel RJ, Eder HA, Bragdon JH (1955) The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 34:1345-1353
28. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
29. Norata GD, Tibolla G, Seccomandi PM, Poletti A, Catapano AL (2006) Dihydrotestosterone decreases tumor necrosis factor-alpha and lipopolysaccharide-induced inflammatory response in human endothelial cells. J Clin Endocrinol Metab 91:546-554
30. Drew BG, Fidge NH, Gallon-Beaumier G, Kemp BE, Kingwell BA (2004) High-density lipoprotein and apolipoprotein AI increase endothelial NO synthase activity by protein association and multisite phosphorylation. Proc Natl Acad Sci USA 101:6999-7004
31. Rosenson RS, Brewer HB Jr, Davidson WS, Fayad ZA, Fuster V, Goldstein J, Hellerstein M, Jiang XC, Phillips MC, Rader DJ, Remaley AT, Rothblat GH, Tall AR, Yvan-Charvet L (2012) Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation 125:1905-1919
32. Tall AR (2008) Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J Intern Med 263:256-273
33. Besler C, Heinrich K, Rohrer L, Doerries C, Riwanto M, Shih DM, Chroni A, Yonekawa K, Stein S, Schaefer N, Mueller M, Akhmedov A, Daniil G, Manes C, Templin C, Wyss C, Maier W, Tanner FC, Matter CM, Corti R, Furlong C, Lusis AJ, von Eckardstein A, Fogelman AM, Luscher TF, Landmesser U (2011) Mechanisms underlying adverse effects of HDL on eNOS-activating pathways in patients with coronary artery disease. J Clin Invest 121:2693-2708
34. Terasaka N, Westerterp M, Koetsveld J, Fernandez-Hernando C, Yvan-Charvet L, Wang N, Sessa WC, Tall AR (2010) ATP-binding cassette transporter G1 and high-density lipoprotein promote endothelial NO synthesis through a decrease in the interaction of caveolin-1 and endothelial NO synthase. Arterioscler Thromb Vasc Biol 30:2219-2225
35. Norata GD, Pirillo A, Catapano AL (2006) Modified HDL: biological and physiopathological consequences. Nutr Metab Cardiovasc Dis 16:371-386
36. Feng H, Li XA (2009) Dysfunctional high-density lipoprotein. Curr Opin Endocrinol Diabetes Obes 16:156-162
37. Yla-Herttuala S (1992) Gene expression in atherosclerotic lesions. Herz 17:270-276
38. Frank PG (2010) Endothelial caveolae and caveolin-1 as key regulators of atherosclerosis. Am J Pathol 177:544-546
39. Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, Lisanti MP (2004) Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol 24:98-105
40. Fernandez-Hernando C, Yu J, Davalos A, Prendergast J, Sessa WC (2010) Endothelial-specific overexpression of caveolin-1 accelerates atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol 177:998-1003
41. Ramet ME, Ramet M, Lu Q, Nickerson M, Savolainen MJ, Malzone A, Karas RH (2003) High-density lipoprotein increases the abundance of eNOS protein in human vascular endothelial cells by increasing its half-life. J Am Coll Cardiol 41:2288-2297
42. Gomaraschi M, Ossoli A, Favari E, Adorni MP, Sinagra G, Cattin L, Veglia F, Bernini F, Franceschini G, Calabresi L (2013) Inflammation impairs eNOS activation by HDL in patients with acute coronary syndrome. Cardiovasc Res 100:36-43
43. White J, Guerin T, Swanson H, Post S, Zhu H, Gong M, Liu J, Everson WV, Li XA, Graf GA, Ballard HO, Ross SA, Smart EJ (2008) Diabetic HDL-associated myristic acid inhibits acetylcholine-induced nitric oxide generation by preventing the association of endothelial nitric oxide synthase with calmodulin. Am J Physiol Cell Physiol 294:C295-C305
44. Matsuo Y, Oberbach A, Till H, Inge TH, Wabitsch M, Moss A, Jehmlich N, Volker U, Muller U, Siegfried W, Kanesawa N, Kurabayashi M, Schuler G, Linke A, Adams V (2013) Impaired HDL function in obese adolescents: impact of lifestyle intervention and bariatric surgery. Obesity (Silver Spring) 21:E687-E695
45. Mineo C, Shaul PW (2012) Functions of scavenger receptor class B, type I in atherosclerosis. Curr Opin Lipidol 23:487-493
46. Seetharam D, Mineo C, Gormley AK, Gibson LL, Vongpatanasin W, Chambliss KL, Hahner LD, Cummings ML, Kitchens RL, Marcel YL, Rader DJ, Shaul PW (2006) High-density lipoprotein promotes endothelial cell migration and reendothelialization via scavenger receptor-B type I. Circ Res 98:63-72
47. Pan B, Ma Y, Ren H, He Y, Wang Y, Lv X, Liu D, Ji L, Yu B, Wang Y, Chen YE, Pennathur S, Smith JD, Liu G, Zheng L (2012) Diabetic HDL is dysfunctional in stimulating endothelial cell migration and proliferation due to down regulation of SR-BI expression. PLoS One 7:e48530