Influence of acylation of a peptide corresponding to the amino-terminal region of endothelial nitric oxide synthase on the interaction with model membranes

Biochemistry

Volumn 45, Issue 4, 2006, Pages 1263-1270

  Yélamos, Belén ^a   Roncal, Fernando ^b   Albar, Juan P ^b   Rodríguez Crespo, Ignacio ^a   Gavilanes, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; FATTY ACIDS; HYDROPHOBICITY; MEMBRANES; NITROGEN OXIDES; PHOSPHOLIPIDS; THERMAL VARIABLES CONTROL;

ACIDIC PHOSPHOLIPIDS; ENDOTHELIAL NITRIC OXIDE SYNTHASE (ENOS); MODEL MEMBRANES; PALMITOYLATION;

ACYLATION;

ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; MYRISTIC ACID; PALMITIC ACID; PEPTIDE; PHOSPHOLIPID; SPHINGOMYELIN;

ACYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; COVALENT BOND; ENZYME MECHANISM; HYDROPHOBICITY; LIQUID; MEMBRANE BINDING; MODEL; PEPTIDE SYNTHESIS; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; THERMAL ANALYSIS;

ACYLATION; AMINO ACID SEQUENCE; CIRCULAR DICHROISM; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCINE; LIPOSOMES; MEMBRANES; MOLECULAR SEQUENCE DATA; MYRISTIC ACID; NITRIC OXIDE SYNTHASE TYPE III; PEPTIDE FRAGMENTS; PEPTIDES; PHOSPHOLIPIDS; SPECTROMETRY, FLUORESCENCE; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE; TRYPTOPHAN;

EID: 31544439354     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0514865     Document Type: Article

References (48)

1. Resh, M. D. (1999) Fatty acylation of proteins: New insights into membrane targeting of myristoylated and palmitoylated proteins, Biochim. Biophys. Acta 1451, 1-16.
2. Gordon, J. I., Duronio, R. J., Rudnick, D. A., Adams, S. P., and Goke, G. W. (1991) Protein N-myristoylation, J. Biol. Chem. 266, 8647-8650.
3. Weston, S. A., Gamble, R., Colls, J., Rosenbrock, G. M., Taylor, I., Egerton, M., Tucker, A. D., Tunnicliffe, A., Mistry, A., Mancia, T., de la Tortelle, E., Irwin, J., Bricogne, G., and Pauptit, R. A. (1998) Crystal structure of the anti-fungal target N-myristoyl transferase, Nat. Struct. Biol. 5, 213-221.
4. Bhatnagar, R. S., Futterer, K., Waksman, G., and Gordon, J. I. (1999) The structure of myristoyl-CoA:protein N-myristoyltransferase, Biochim. Biophys. Acta 1441, 162-172.
5. Under, M. E., and Deschenes, R. J. (2003) New insights into the mechanisms of protein palmitoylation, Biochemistry 42, 4311-4320.
6. Dunphy, J. T., and Linder, M. E. (1998) Signalling functions of protein palmitoylation, Biochim. Biophys. Acta 1436, 245-261.
7. Lobo, S., Greentree, W. K., Linder, M. E., and Deschenes, R. J. (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae, J. Biol. Chem. 277, 41268-41273.
8. Roth, A. P., Feng, Y., Chen, L., and Davis, N. G. (2002) The yeast DHHC cysteine-rich domain protein Akr1p is a palmitoyl transferase, J. Cell Biol. 159, 23-28.
9. Swarthout, J. T., Lobo, S., Farh, L., Croke, M. R., Greentree, W. K., Deschenes, R. J., and Linder, M. E. (2005) DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-ras, J. Biol. Chem. 280, 31141-31148.
10. Bañó, M. C., Jackson, C. S., and Magee, A. I. (1998) Pseudoenzymatic S-acylation of a myristoylated yes protein tyrosine kinase peptide in vitro may reflect non-enzymatic S-acylation in vivo, Biochem. J. 330, 723-731.
11. Duncan, J. A., and Gilman, A. G. (1996) Autoacylation of G protein α subunits, J. Biol. Chem. 271, 23594-23600.
12. Veit, M. (2000) Palmitoylation of the 25-kDa synaptosomal protein (SNAP-25) in vitro occurs in the absence of an enzyme, but is stimulated by binding to syntaxin, Biochem. J. 345, 145-151.
13. 2-adrenergic receptor peptides, FEBS Lett. 499, 59-64.
14. Navarro-Lérida, I., Álvarez-Barrientos, A., Gavilanes, F., and Rodríguez-Crespo, I. (2002) Distance-dependent cellular palmitoylation of de-novo-designed sequences and their translocation to plasma membrane subdomains, J. Cell Sci. 115, 3119-3130.
15. Moncada, S., and Higgs, A. (1993) The L-arginine-nitric oxide pathway, N. Engl. J. Med. 329, 2002-2012.
16. Bredt, D. S., and Snyder, S. H. (1994) Nitric oxide. A physiologic messenger molecule, Annu. Rev. Biochem. 63, 175-195.
17. Feron, O., Dessy, C., Moniotte, S., Desager, J. P., and Balligand, J. L. (1999) Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase, J. Clin. Invest. 103, 897-905.
18. Busconi, L., and Michel, T. (1993) Endothelial nitric oxide synthase. N-Terminal myristoylation determines subcellular localization, J. Biol. Chem. 268, 8410-8413.
19. Robinson, L. J., Busconi, L., and Michel, T. (1995) Agonist-modulated palmitoylation of endothelial nitric oxide synthase, J. Biol. Chem. 270, 995-998.
20. Liu, J., Hughes, T. E., and Sessa, W. C. (1997) The first 35 amino acids and fatty acylation sites determine the molecular targeting of endothelial nitric oxide synthase into the Golgi region of cells: A green fluorescent protein study, J. Cell Biol. 137, 1525-1535.
21. Sessa, W. C., Garcia-Cardena, G., Liu, J., Keh, A., Pollock, J. S., Bradley, J., Thiru, S., Braverman, I. M., and Desai, K. M. (1995) The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide, J. Biol. Chem. 270, 17641-17644.
22. Sakoda, T., Hirata, K., Kuroda, R., Miki, N., Suematsu, M., Kawashima, S., and Yokoyama, M. (1995) Myristoylation of endothelial cell nitric oxide synthase is important for extracellular release of nitric oxide, Mol. Cell. Biochem. 152, 143-148.
23. García-Cardeña, G., Oh, P., Liu, J., Schnitzer, J. E., and Sessa, W. C. (1996) Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: Implications for nitric oxide signaling, Proc. Natl. Acad. Sci. U.S.A. 93, 6448-6453.
24. Michel, J. B., Feron, O., Sacks, D., and Michel, T. (1997) Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase, J. Biol. Chem. 272, 15583-15586.
25. King, D. S., Fields, C. G., and Fields, G. B. (1990) A cleavage method which minimizes side reactions following Fmoc solid-phase peptide synthesis, Int. J. Pept. Protein Res. 36, 255-266.
26. Beekman, N. J. C. M., Schaaper, W. M. M., Tesser, G. I., Dalsgaard, K., Kamstrup, S., Langeveld, J. P. M., Boshuizen, R. S., and Meloen, R. H. (1997) Synthetic peptide vaccines: Palmitoylation of peptide antigens by a thioester bond increases immunogenicity, J. Pept. Res. 50, 357-364.
27. Eftink, M. R. (1991) Fluorescence techniques for studying protein structure, Methods Biochem. Anal. 35, 127-205.
28. Lentz, B. R., Barenholz, Y., and Thompson, T. E. (1976) Fluorescence depolarization studies of phase transitions and fluidity in phospholipid bilayers. 2. Two-component phosphatidylcholine liposomes, Biochemistry 15, 4529-4537.
29. Andrich, M. P., and Vanderkooi, J. M. (1976) Temperature dependence of 1,6-diphenyl-1,3,5-hexatriene fluorescence in phophoslipid artificial membranes, Biochemistry 15, 1257-1261.
30. Prendergast, F. G., Haugland, P. J., and Callahan, P. J. (1981) 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: Synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers, Biochemistry 20, 7333-7338.
31. Kaiser, R. D., and London, E. (1998) Location of diphenylhexatriene (DPH) and its derivatives within membranes: Comparison of different fluorescence quenching analyses of membrane depth, Biochemistry 37, 8180-8190.
32. London, E. (2002) Insights into lipid raft strtucture and formation from experiments in model membranes, Curr. Opin. Struct. Biol. 12, 480-486.
33. Brown, D. A., and London, E. (1998) Structure and origin of ordered lipid domains in biological membranes, J. Membr. Biol. 164, 103-114.
34. Laczko, I., Hollosi, M., Vass, E., and Toth, G. K. (1998) Liposome-induced conformational changes of an epitopic peptide and its palmitoylated derivative of influenza virus hemagglutinin, Biochem. Biophys. Res. Commun. 249, 213-217.
35. Szyperski, T., Vandenbussche, G., Curstedt, T., Ruysschaert, J. M., Wuthrich, K., and Johansson, J. (1998) Pulmonary surfactant-associated polypeptide C in a mixed organic solvent transforms from a monomeric α-helical state into insoluble β-sheet aggregates, Protein Sci. 7, 2533-2540.
36. Creuwels, L. A., Demel, R. A., van Golde, L. M., Benson, B. J., and Haagsman, H. P. (1993) Effect of acylation on structure and function of surfactant protein C at the air-liquid interface, J. Biol. Chem. 268, 26752-26758.
37. 1H nuclear magnetic resonance studies of synthetic peptides, Biochemistry 29, 8998-9006.
38. Raman, C. S., Li, H., Martasek, P., Kral, V., Masters, B. S., and Poulos, T. L. (1998) Crystal structure of constitutive endothelial nitric oxide synthase: A paradigm for pterin function involving a novel metal center, Cell 95, 939-950.
39. Harishchandran, A., and Nagaraj, R. (2005) Interaction of a pseudosubstrate of protein kinase C and its myristoylated form with lipid vesicles: Only the myristoylated form translocates into the lipid bilayer, Biochim. Biophys. Acta 1713, 73-82.
40. Plasencia, I., Rivas, L., Keough, K. M. W., Marsh, D., and Perez-Gil, J. (2004) The N-terminal segment of pulmonary surfactant lipopeptide SP-C has intrinsic propensity to interact with and perturb phospholipid bilayers, Biochem. J. 377, 183-193.
41. Pallavi, B., and Nagaraj, R. (2003) Palmitoylated peptides from the cysteine-rich domain of SNAP-23 cause membrane fusion depending on peptide length, position of cysteines, and extent of palmitoylation, J. Biol. Chem. 278, 12737-12744.
42. Resh, M. D. (2004) Membrane targeting of lipid modified signal transduction proteins, in Subcellular Biochemistry (Quinn, P. J., Ed.) Vol. 37, pp 217-232, Kluwer Academic/Plenum Publishers, New York.
43. Papahadjopoulos, D., Moscarello, M., Eylar, E. H., and Isac, T. (1975) Effects of proteins on thermotropic phase transitions of phospholipid membranes, Biochim. Biophys. Acta 401, 317-335.
44. Venema, R. C., Sayegh, H. S., Arnal, J. F., and Harrison, D. G. (1995) Role of the enzyme calmodulin-binding domain in membrane association and phospholipid inhibition of endothelial nitric oxide synthase, J. Biol. Chem. 270, 14705-14711.
45. 2-terminal domain of gi1α is sufficient to target a green fluorescent protein reporter to caveolin-enriched plasma membrane domains. Palmitoylation of caveolin-1 is required for the recognition of dually acylated g-protein α subunits in vivo, J. Biol. Chem. 274, 5843-5850.
46. Zacharias, D. A., Violin, J. D., Newton, A. C., and Tsien, R. Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells, Science 296, 913-916.
47. McCabe, J. B., and Berthiaume, L. G. (1999) Functional roles for fatty acylated amino-terminal domains in subcellular localization, Mol. Biol. Cell 10, 3771-3786.
48. Simons, K., and Toomre, D. (2000) Lipid rafts and signal transduction, Nat. Rev. Mol. Cell Biol. 1, 31-39.