Receptor-regulated dynamic interaction between endothelial nitric oxide synthase and calmodulin revealed by fluorescence resonance energy transfer in living cells

Biochemistry

Volumn 42, Issue 40, 2003, Pages 11716-11725

  Jobin, Charles M ^a   Chen, Hongjie ^b   Lin, Alison J ^a   Yacono, Patrick W ^a   Igarashi, Junsuke ^b   Michel, Thomas ^b,c   Golan, David E ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c VA BOSTON HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENERGY TRANSFER; FLUORESCENCE; IMAGING TECHNIQUES; MEMBRANES;

CONFOCAL IMAGES;

ENZYMES;

CALMODULIN; CALMODULIN BINDING PROTEIN; NITRIC OXIDE SYNTHASE; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUORESCENCE; GENETIC TRANSFECTION; IMAGE ANALYSIS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL PROTEINS; CALCIUM SIGNALING; CALCIUM-BINDING PROTEINS; CALMODULIN; CATTLE; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; DROSOPHILA PROTEINS; ENDOTHELIUM, VASCULAR; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; INTRACELLULAR FLUID; LUMINESCENT PROTEINS; MEMBRANE PROTEINS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; RECEPTORS, CELL SURFACE; RECOMBINANT FUSION PROTEINS; SUBCELLULAR FRACTIONS; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 0141885307     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035066w     Document Type: Article

References (34)

1. Fleming, I., and Busse, R. (2003) Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase, Am. J. Physiol. 284, R1-R12.
2. Michel, T., and Feron, O. (1997) Nitric oxide synthase: which, where, how, and why? J. Clin. Invest. 100, 2146-2152.
3. Ju, H., Zou, R., Venema, V. J., and Venema, R. C. (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity, J. Biol. Chem. 272, 18522-18525.
4. Shaul, P. W. (2002) Regulation of endothelial nitric oxide synthase: location, location, location, Annu. Rev. Physiol. 64, 749-774.
5. Prabhakar, P., Thatte, H. S., Goetz, R. M., Cho, M. R., Golan, D. E., and Michel, T. (1998) Receptor-regulated translocation of endothelial nitric-oxide synthase, J. Biol. Chem. 273, 27383-27388.
6. Gonzalez, E., Kou, R., Lin, A. J., Golan, D. E., and Michel, T. (2002) Subcellular targeting and agonist-induced site-specific phosphorylation of endothelial nitric-oxide synthase, J. Biol. Chem. 277, 39554-39560.
7. Fulton, D., Fontana, J., Sowa, G., Gratton, J. P., Lin, M., Li, K. X., Michell, B., Kemp, B. E., Rodman, D., and Sessa, W. C. (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.
8. Govers, R., and Rabelink, T. J. (2001) Cellular regulation of endothelial nitric oxide synthase, Am. J. Physiol. 280, F193-F206.
9. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: structure, function and inhibition, Biochem. J. 357, 593-615.
10. Fleming, I., and Busse, R. (1999) Signal transduction of eNOS activation, Cardiovasc. Res. 43, 532-541.
11. Klee, C. B., Crouch, T. H., and Richman, P. G. (1980) Calmodulin, Annu. Rev. Biochem. 49, 489-515.
12. Chan, F. K., Siegel, R. M., Zacharias, D., Swofford, R., Holmes, K. L., Tsien, R. Y., and Lenardo, M. J. (2001) Fluorescence resonance energy transfer analysis of cell surface receptor interactions and signaling using spectral variants of the green fluorescent protein, Cytometry 44, 361-368.
13. Kenworthy, A. K. (2001) Imaging protein-protein interactions using fluorescence resonance energy transfer microscopy, Methods 24, 289-296.
14. Gordon, G. W., Berry, G., Liang, X. H., Levine, B., and Herman, B. (1998) Quantitative fluorescence resonance energy transfer measurements using fluorescence microscopy, Biophys. J. 74, 2702-2713.
15. 2+ based on green fluorescent proteins and calmodulin, Nature 388, 882-887.
16. Tsien, R. Y. (1998) The green fluorescent protein, Annu. Rev. Biochem. 67, 509-544.
17. Robinson, L. J., and Michel, T. (1995) Agonist-modulated palmitoylation of endothelial nitric oxide synthase, Proc. Natl. Acad. Sci. U.S.A. 92, 11776-11780.
18. Igarashi, J., and Michel, T. (2000) Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae: eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingolipid signal transduction, J. Biol. Chem. 275, 32363-32370.
19. Lamas, S., Marsden, P. A., Li, G. K., Tempst, P., and Michel, T. (1992) Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform, Proc. Natl. Acad. Sci. U.S.A. 89, 6348-6352.
20. Feron, O., Michel, J. B., Sase, K., and Michel, T. (1998) Dynamic regulation of endothelial nitric oxide synthase: complementary roles of dual acylation and caveolin interactions, Biochemistry 37, 193-200.
21. Damelin, M., and Silver, P. A. (2000) Mapping interactions between nuclear transport factors in living cells reveals pathways through the nuclear pore complex, Mol. Cell 5, 133-140.
22. Kenworthy, A. K., and Edidin, M. (1998) Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of <100 Å using imaging fluorescence resonance energy transfer, J. Cell Biol. 142, 69-84.
23. He, H., Venema, V. J., Gu, X., Venema, R. C., Marrero, M. B., and Caldwell, R. B. (1999) Vascular endothelial growth factor signals endothelial cell production of nictric oxide and prostacyclin through flk-1/KDR activation of c-Src, J. Biol. Chem. 274, 25130-25135.
24. Kantor, D. B., Lanzrein, M., Stary, S. J., Sandoval, G. M., Smith, W. B., Sullivan, B. M., Davidson, N., and Schuman, E. M. (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue, Science 274, 1744-1748.
25. Igarashi, J., and Michel, T. (2001) Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase beta. Evidence for divergence and convergence of receptor-regulated endothelial nitric-oxide synthase signaling pathways, J. Biol. Chem. 276, 36281-36288.
26. 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.
27. 2+-calmodulin and caveolin, J. Biol. Chem. 272, 15583-15586.
28. Michel, J. B., Feron, O., Sase, K., Prabhakar, P., and Michel, T. (1997) Caveolin versus calmodulin, J. Biol. Chem. 272, 25907-25912.
29. 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.
30. Kojima, H., Sakurai, K., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y., and Nagano, T. (1998) Development of a fluorescent indicator for nitric oxide based on the fluorescein chromophore, Chem. Pharm. Bull. 46, 373-375.
31. Nakatsubo, N., Kojima, H., Kikuchi, K., Nagoshi, H., Hirata, Y., Maeda, D., Imai, Y., Irimura, T., and Nagano, T. (1998) Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators-diaminofluoresceins, FEBS Lett. 427, 263-266.
32. Shaul, P. W., and Anderson, R. G. W. (1998) Role of plasmalemmal caveolae in signal transduction, Am. J. Physiol. 275, L843-L851.
33. Lisanti, M. P., Scherer, P. E., Vidugiriene, J., Tang, Z., Hermanowski-Vosatka, A., Tu, Y. H., Cook, R. F., and Sargiacomo, M. (1994) Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease, J. Cell Biol. 126, 111-126.
34. Okamoto, T., Schlegel, A., Scherer, P. E., and Lisanti, M. P. (1998) Caveolins, a family of scaffolding proteins for organizaing "preassembled signaling complexes" at the plasma membrane, J. Biol. Chem. 273, 5419-5422.