Peptide-stimulation enhances compartmentalization and the catalytic activity of lung endothelial NOS

Cellular Physiology and Biochemistry

Volumn 24, Issue 5-6, 2009, Pages 471-482

  Hutchinson, Tarun E ^b   Kuchibhotla, Sudeep ^b   Block, Edward R ^a,b   Patel, Jawaharlal M ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Caveolae; Compartmentalization; Endothelial Cells; Golgi Complex; Plasma membrane; Vasorelaxation

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; CHOLESTEROL OXIDASE; METHYL BETA CYCLODEXTRIN; NITRIC OXIDE SYNTHASE; PEPTIDE DERIVATIVE;

ANIMAL CELL; ARTERY ENDOTHELIUM; ARTICLE; CATALYSIS; CAVEOLA; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME LOCALIZATION; GOLGI COMPLEX; IMMUNOFLUORESCENCE; IMMUNOGOLD LABELING; IMMUNOPRECIPITATION; LUNG CIRCULATION; LUNG ENDOTHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; SWINE;

EID: 70450242879     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000257487     Document Type: Article

References (46)

1. Marletta MA: Nitric oxide synthase structure and mechanism. J Biol Chem 1993;268:12231-12234.
2. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T: Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 1996;271(37):22810-22814.
3. García-Cardeña G, Oh P, Liu J, Schnitzer JE, Sessa WC: Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci USA 1996;93:6448-6453. (Pubitemid 26230326)
4. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM: Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605.
5. García-Cardeña G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC: Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 1998;392:821-824.
6. Michel T, Feron O: Nitric oxide synthases: which, where, how, and why? J Clin Invest 1997;100:2146-2152.
7. Sowa G, Pypaert M, Sessa WC: Distinction between signaling mechanisms in lipid rafts vs. caveolae. Proc Natl Acad Sci USA 2001;98:14072-14077.
8. Chen PF, Tsai AL, Wu KK: Cysteine 184 of endothelial nitric oxide synthase is involved in heme coordination and catalytic activity. J Biol Chem 1994;269:25062-25066.
9. Chen PF, Tsai AL, Wu KK: Cysteine 99 of endothelial nitric oxide synthase (NOS-III) is critical for tetrahydrobiopterin-dependent NOS-III stability and activity. Biochem Biophys Res Commun 1995;215:1119-1129.
10. Zhang JL, Patel JM, Li YD, Block ER: Reductase domain cysteines 1048 and 1114 are critical for catalytic activity of human endothelial cell nitric oxide synthase as probed by site directed mutagenesis. Biochem Biophys Res Commun 1996;226:293-300.
11. Liu J, García-Cardeña G, Sessa WC: Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry 1996;35:13277-13281. (Pubitemid 26349419)
12. Shaul P W, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson RG, Michel T: Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem 1996;271:6518-6522. (Pubitemid 26095467)
13. Feron O, Michel JB, Sase K, Michel T: Dynamic regulation of endothelial nitric oxide synthase: complementary roles of dual acylation and caveolin interactions. Biochemistry 1998;37:193-200.
14. Feron O, Saldana F, Michel JB, Michel T: The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem 1998;273:3125-3128.
15. Goligorsky MS, Li H, Brodsky S, Chen J: Relationships between caveolae and eNOS: everything in proximity and the proximity of everything. Am J Physiol Renal Physiol 2002;283:F1-10.
16. Williams TM, Lisanti MP: The Caveolin genes: from cell biology to medicine. Ann Med 2004;36:584-595.
17. García-Cardeña G, Fan R, Stern DF, Liu J, Sessa WC: Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 1996;271:27237-27240.
18. García-Cardeña G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC: 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.
19. Ju H, Venema VJ, Marrero MB, Venema RC: Inhibitory interactions of the bradykinin B2 receptor with endothelial nitric-oxide synthase. J Biol Chem 1998;273:24025-24029.
20. Michel T, Li GK, Busconi L: Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 1993;90:6252-6256.
21. Nishida E, Koyasu S, Sakai H, Yahara I: Calmodulin-regulated binding of the 90-kDa heat shock protein to actin filaments. J Biol Chem 1986;261:16033-16036.
22. Chikani G, Zhu W, Smart EJ: Lipids: potential regulators of nitric oxide generation. Am J Physiol Endocrinol Metab 2004;287:E386-E389.
23. Feron O, Dessy C, Moniotte S, Desager JP, Balligand JL: Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase. J Clin Invest 1999;103:897-905.
24. Sowa G, Liu J, Papapetropoulos A, Rex-Haffner M, Hughes TE, Sessa WC: Trafficking of endothelial nitric-oxide synthase in living cells. Quantitative evidence supporting the role of palmitoylation as a kinetic trapping mechanism limiting membrane diffusion. J Biol Chem 1999;274:22524-22531.
25. Akoi T, Nomura R, Fujimoto T: Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999;253:629-636.
26. Maniatis NA, Brovkovych V, Allen SE, John TA, Shajahan AN, Tiruppathi C, Vogel SM, Skidgel RA, Malik AB, Minshall RD: Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res 2006;99:870-877.
27. 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.
28. Murata M, Peränen J, Schreiner R, Wieland F, Kurzchalia T V, Simons K: VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 1995;92:10339-10343.
29. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ: Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem 1999;274:32512-32519.
30. Schnitzer JE, Oh P, Pinney E, Allard J: Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 1994;127:1217-1232.
31. Smart EJ, Ying YS, Conrad PA, Anderson RG: Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J Cell Biol 1994;127:1185-1197.
32. Bergdahl A, Gomez MF, Dreja K, Xu SZ, Adner M, Beech DJ, Broman J, Hellstrand P, Swärd K: Cholesterol depletion impairs vascular reactivity to endothelin-1 by reducing store-operated Ca2+ entry dependent on TRPC1. Circ Res 2003;93:839-847.
33. Hailstones D, Sleer LS, Parton RG, Stanley KK: Regulation of caveolin and caveolae by cholesterol in MDCK cells. J Lipid Res 1998;39: 369-379.
34. Meerarani P, Smart EJ, Toborek M, Boissonneault GA, Hennig B: Cholesterol attenuates linoleic acid-induced endothelial cell activation. Metabolism 2003;52:493-500.
35. Hu H, Xin M, Belayev LL, Zhang J, Block ER, Patel JM: Autoinhibitory domain fragment of endothelial NOS enhances pulmonary artery vasorelaxation by the NO-cGMP pathway. Am J Physiol Lung Cell Mol Physiol 2004;286:L1066-L1074.
36. Patel JM, Edwards DA, Block ER, Raizada MK: Effect of nitrogen dioxide on surface membrane fluidity and insulin receptor binding of pulmonary endothelial cells. Biochem Pharmacol 1988;37:1497-1507.
37. Yang B, van Hoek AN, Verkman AS: Very high single channel water permeability of aquaporin-4 in baculovirus-infected insect cells and liposomes reconstituted with purified aquaporin-4. Biochemistry 1997;36:7625-7632.
38. Hu YK, Kaplan JH. Site-directed chemical labeling of extracellular loops in a membrane protein. The topology of the Na,K-ATPase alpha-subunit. J Biol Chem 2000;275:19185-19191.
39. Seshadri RM, Klein JD, Smith T, Sands JM, Handlogten ME, Verlander JW, Weiner ID: Changes in subcellular distribution of the ammonia transporter, Rhcg, in response to chronic metabolic acidosis. Am J Physiol Renal Physiol 2006;290:F1443-F1452.
40. Patel JM, Block ER: Sulfhydryl-disulfide modulation and the role of disulfide oxidoreductases in regulation of the catalytic activity of nitric oxide synthase in pulmonary artery endothelial cells. Am J Respir Cell Mol Biol 1995;13:352-359
41. Statistical Principles in Experimental Design. New York: McGraw-Hill, 1991, p. Winer BJ. 210-219.
42. Fernández-Hernando C, Fukata M, Bernatchez PN, Fukata Y, Lin MI, Bredt DS, Sessa WC: Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. Cell Biol 2006;174:369-377.
43. Fulton D, Fontana J, Sowa G, Gratton JP, Lin M, Li KX, Michell B, Kemp BE, Rodman D, Sessa WC: 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.
44. Jagnandan D, Sessa WC, Fulton D: Intracellular location regulates calcium-calmodulin dependent activation of organelle-restricted eNOS. Am J Physiol Cell Physiol 2005;289:C1024-C1033.
45. Sánchez FA, Savalia NB, Durán RG, Lal BK, Boric MP, Durán WN: Functional significance of differential eNOS translocation. Am J Physiol Heart Circ Physiol 2006;291:H1058-H1064.
46. Rothberg KG, Ying YS, Kolhouse JF, Kamen BA, Anderson RG: The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J Cell Biol 1990;110:637-649