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

Journal of Cell Biology

Volumn 137, Issue 7, 1997, Pages 1525-1535

  Liu, Jianwei ^a   Hughes, Thomas E ^b   Sessa, William C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ACYLATION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; ENDOTHELIUM CELL; ENZYME ACTIVITY; FLUORESCENCE; GOLGI COMPLEX; IMMUNOBLOTTING; MOUSE; MYRISTYLATION; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALIA;

EID: 0030920365     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.7.1525     Document Type: Article

References (48)

1. Bredt, D.S., and S.H. Snyder. 1990. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA. 87:682-685.
2. Chalfie, M., Y. Tu, G. Euskirchen, W.W. Ward, and D.C. Prasher. 1994. Green fluorescent protein as a marker for gene expression. Science (Wash. DC). 263:802-805.
3. Chun, M., U.K. Liyanage, M.P. Lisanti, H.F. Lodish. 1994. Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc. Natl. Acad. Sci. USA. 91:11728-11732.
4. Conrad, P.A., E.J. Smart, Y. Ying, R.G.W. Anderson, and G.S. Bloom. 1995. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131:1421-1433.
5. Denker, S.P., J.M. McCaffery, G.E. Palade, P.A. Insel, and M.G. Farquhar. 1996. Differential distribution of α subunits and βγ subunits of heterotrimeric G proteins on Golgi membranes of the exocrine pancreas. J. Cell Biol. 133:1027-1040.
6. Dunphy, J.T., W.K. Greentree, C.L. Manahan, and M.E. Linder. 1996. G-protein palmitoyltransferase activity is enriched in plasma membranes. J. Biol. Chem. 271:7154-7159.
7. Feron, O., L. Beihassen, L. Kobzik, T.W. Smith, R.A. Kelly, and T. Michel. 1996. Endothelial nitric oxide synthase targeting to caveolae. J. Biol. Chem. 271:22810-22814.
8. Forstermann, U., J.S. Pollock, H.H.H.W. Schmidt, M. Heller, and F. Murad. 1991. Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA. 88:1788-1792.
9. García-Cardeña, G., P. Oh, J. Liu, J.E. Schnitzer, and W.C. Sessa. 1996a. Targeting of nitric oxide synthase to endothelial caveolae via palmitoylation. Proc. Natl. Acad. Sci. USA. 93:6448-6453.
10. García-Cardeña, G., R. Fan, D.F. Stern, J. Liu, and W.C. Sessa. 1996b. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts wilh caveolin-1. J. Biol. Chem. 271:27237-27240.
11. fyn src homology 4 domain define a motif for immune receptor-based activation motif (ITAM) binding and for plasma membrane localization. J. Cell Biol. 133:1007-1015.
12. Gutierrez, L., and A.I. Magee. 1991. Characterization of an acyltransferase acting on p21N-ras protein in a cell-free system. Biochem. Biophys. Acta. 1078:147-154.
13. Htun H., J. Barsony, I. Renyi, D.L. Gould, and G.L. Hager. 1996. Visualization of glucocorticoid receptor translocation and intranuclear organization in living cells with a green fluorescent protein chimera. Proc. Natl. Acad. Sci. USA. 93:4845-1850.
14. Kantor, D.B., M. Lanzrein, S.J. Stary, G.M. Sandoval, W.B. Smith, B.M. Sullivan, N. Davidson, and E.M. Schuman. 1996. A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science (Wash. DC). 274:1744-1748.
15. Ley, S.C., M. Marsh, C.R. Bebbington, K. Proudfoot, and P. Jordan. 1994. Distinct intracellular localization of Lck and Fyn protein tyrosine kinases in human T lymphocytes. J. Cell Biol. 125:639-649.
16. Liu, J., and W.C. Sessa. 1994. Identification of covalently bound amino-terminal myristic acid in endothelial nitric oxide synthase. J. Biol. Chem. 269:11691-11694.
17. Liu, J., G. García-Cardeña, and W.C. Sessa. 1995. Biosynthesis and palmitoylation of endothelial nitric oxide synthase: mutagenesis of palmitoylation sites, cysteine 15 and/or 26, argue against depalmitoylation induced translocation of the enzyme. Biochemistry. 34:12333-12340.
18. Liu, J., G. García-Cardeña, and W.C. Sessa. 1996. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry. 35:13277-13281.
19. Marshall, J., M. Raymond, G.W.J. Moss, J.R. Howe, and T.E. Hughes. 1995. The jellyfish green fluorescent protein: a new tool for studying ion channel expression and function. Neuron. 14:211-215.
20. Michel, T., G.K. Li, and L. Busconi. 1993. Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA. 90:6252-6256.
21. Moreman, K.W., and O. Touster. 1986. Topology of mannosidase II in rat liver Golgi membranes and release of the catalytic domain by selective proteolysis. J. Biol. Chem. 261:10945-10951.
22. Moriyoshi, K., L.J. Richards, C. Akazawa, D.D.M. O'Leary, and S. Nakanishi. 1996. Labeling neural cells using adenoviral gene transfer of membrane targeted GFP. Neuron. 16:255-260.
23. Mumby, S.M., C. Kleuss, and A.G. Gilman. 1994. Receptor regulation of G-protein palmitoylation. Proc. Natl. Acad. Sci. USA. 91:2800-2804.
24. Murata, M., J. Peranen, R. Schreiner, F. Wieland, T.V. Kurzchalia, and K. Simons. 1995. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. USA. 92:10339-10343.
25. Peitzsch, R.M., and S. McLaughlin. 1993. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:10436-10443.
26. Pollock, J.S., U. Forstermann, J.A. Mitchell, T.D. Warner, H.H.H.W. Schmidt, M. Nakane, and F. Murad. 1991. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. USA. 88:10480-10484.
27. Prasher, D.C., V.K. Eckenrode, W.W. Ward, F.G. Prendergast, and M.J. Cormier. 1992. Primary structure of the Aequorea victoria green-fluorescent protein. Gene (Amst.). 111:229-233.
28. Resh, M.D. 1994. Myristoylation and palmitoylation of Src family members: the fats of the matter. Cell. 76:411-413.
29. Robbins, S.M., N.A. Quintrell, and J.M. Bishop. 1995. Myristoylation and differential palmitoylation of the HCK protein-tyrosine kinases govern their attachment to membranes and association with caveolae. Mol. Cell. Biol. 15: 3507-3515.
30. Robinson, L.J., and T. Michel. 1995. Mutagenesis of palmitoylation sites in endothelial nitric oxide synthase identifies a novel motif for dual acylation and subcellular targeting. Proc. Natl. Acad. Sci. USA. 92: 11776-11780.
31. Schmidt, J.W., and W.A. Catterall. 1987. Palmitoylation, sulfation, and glycosylation of the alpha subunit of the sodium channel. Role of post-translational modifications in channel assembly. J. Biol. Chem. 262:13713-13723.
32. Schnitzer, J.E., P. Oh, E. Pinney, and J. Allard. 1994. Filipin-sensilive caveolaemediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J. Cell Biol. 127: 1217-1232.
33. Schnitzer, J.E., J. Liu, and P. Oh. 1995. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexin, and GTPases. J. Biol. Chem. 270:14399-14404.
34. Schnitzer, J.E., P. Oh, and D.P. McIntosh. 1996. Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science (Wash. DC). 274:239-242.
35. Sessa, W.C., C.M. Barber, and K.R. Lynch. 1993. Mutation of N-myristoylation site converts endothelial cell nitric oxide synthase from a membrane to a cytosolic protein. Circ. Res. 72:921-924.
36. Sessa, W.C., G. García-Cardeña, J. Liu, A. Keh, J.S. Pollock, J. Bradley, S. Thiru, I.M. Braverman, and K.M. Desai. 1995. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J. Biol. Chem. 270:17641-17644.
37. Shaul, P.W., E.J. Smart, L.J. Robinson, Z. German, I.S. Yuhanna, Y. Ying, R.G.W. Anderson, and T. Michel. 1996. Acylation targets endothelia nitric-oxide synthase to plasmalemmal caveolae. J. Biol. Chem. 271:6518-6522.
38. Shenoy-Scaria, A.M., D.J. Dietzen, J. Kwong, D.C. Link, and D.M. Lublin. 1994. Cysteine 3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. J. Cell Biol. 126:353-363.
39. Shi, Y., B. Veit, and S. Baekkeskov. 1994. Amino acid residues 24-31 hut not palmitoylation of cysteines 30 and 45 are required for membrane anchoring of glutamic acid decarboxylase. GAD65. J. Cell Biol. 124:927-934.
40. Smart, E.J., Y. Ying, P.A. Conrad, and R.G.W. Anderson. 1994a. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127:1185-1197.
41. Smart, E.J., D.C. Foster, Y. Ying, B.A. Kamen, and R.G.W. Anderson. 1994b. Protein kinase C activators inhibit receptor-mediated potocytosis by preventing internalization of caveolae. J. Cell Biol. 124:307-313.
42. Smart, E.J., Y. Ying, and R.G.W. Anderson. 1995. Hormonal regulation of caveolae internalization. J. Cell Biol. 131:929-938.
43. Solimena, M., R. Dirkx, Jr., M. Radzynski, O. Mundigl, and P. De Camilli. 1994. A signal located within amino acids 1-27 of GAD65 is required for its targeting to the Golgi complex region. J. Cell Biol. 126:331-341.
44. Stauber, R., G.A. Gaitanaris, and G.N. Pavlakis. 1995. Analysis of trafficking of Rev and transdominant Rev proteins in living cells using green fluorescent protein fusions: transdominant Rev blocks the export of Rev from the nucleus to the cytoplasm. Virology. 213:439-449.
45. Stow, J.L., J.B. de Almeida, E.J. Narula, E.J. Holtzman, L. Ercolani, and D.A. Ausiello. 1991. A heterotrimeric G protein. Gαi-3, on Golgi membranes regulates the secretion of a heparan sulfate proteoglycan in LLC-PK1 epithelial cells. J. Cell Biol. 114:1113-1124.
46. 2-terminal myristoylation and palmitoylation at cysteine-3. J. Cell Biol. 136:1023-1035.
47. Venema, V.J., M.B. Marrero, and R.C. Venema. 1996. Bradykinin-stimulated protein tyrosine phosphorylation promotes endothelial nitric oxide synthase translocation to the cytoskeleton. Biochem. Biophys. Res. Commun. 226:703-710.
48. Wedegaertner, P.B., P.T. Wilson, and H.R. Bourne. 1995. Lipid modifications of trimeric G proteins. J. Biol. Chem. 270:503-506.