ACh-induced endothelial NO synthase translocation, NO release and vasodilation in the hamster microcirculation in vivo

Journal of Physiology

Volumn 544, Issue 3, 2002, Pages 883-896

  Figueroa, Xavier F ^a   González, Daniel R ^a   Martínez, Agustín D ^a   Durán, Walter N ^b   Boric, Mauricio P ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; CAVEOLIN 1; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENZYME INHIBITOR; N(G) NITROARGININE; VASODILATOR AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD FLOW; BLOOD VESSEL DIAMETER; CAVEOLA; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CHEEK POUCH; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LOCALIZATION; GOLGI COMPLEX; HAMSTER; HYPOTHESIS; IN VIVO STUDY; INHIBITION KINETICS; MALE; MEMBRANE BINDING; MICROCIRCULATION; MICROSOME; MICROVASCULARIZATION; NONHUMAN; PRIORITY JOURNAL; TIME; TRANSPORT KINETICS; VASCULAR ENDOTHELIUM; VASODILATATION; VENULE; WESTERN BLOTTING; ANIMAL; CHEEK; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; SYRIAN HAMSTER; TRANSPORT AT THE CELLULAR LEVEL; VASCULARIZATION; ADULT; CHLORIDE CONDUCTANCE; CYTOSOL; ENZYME INHIBITION; PROTEIN TRANSPORT; REPRODUCIBILITY;

ACETYLCHOLINE; ANIMALS; BIOLOGICAL TRANSPORT; CHEEK; CRICETINAE; ENZYME INHIBITORS; MALE; MESOCRICETUS; MICROCIRCULATION; MICROSOMES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; NITROARGININE; VASODILATION; VASODILATOR AGENTS;

EID: 0036850809     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.021972     Document Type: Article

References (56)

1. ANDRIES, L. J., BRUTSAERT, D. L. & SYS, S. U. (1998). Nonuniformity of endothelial constitutive nitric oxide synthase distribution in cardiac endothelium. Circulation Research 82, 195-203.
2. ARCHER, S. (1993). Measurement of nitric oxide in biological models. FASEB Journal 7, 349-360.
3. 2+ and nitric oxide in bradykinin-stimulated vascular endothelial cells. Circulation Research 76, 922-924.
4. BOHLEN, H. G. (1998). Mechanism of increased vessel wall nitric oxide concentrations during intestinal absorption. American Journal of Physiology 275, H542-550.
5. BORIC, M. P., DONOSO, V., FOURNIER, A., ST PIERRE, S. & HUIDOBRO-TORO, J. P. (1990). Endothelin reduces microvascular blood flow by acting on arterioles and venules of the hamster cheek pouch. European Journal of Pharmacology 190, 123-133.
6. BORIC, M. P., FIGUEROA, X. F., DONOSO, M. V., PAREDES, A., POBLETE, I. & HUIDOBRO-TORO, J. P. (1999). Rise in endothelium-derived NO after stimulation of rat perivascular sympathetic mesenteric nerves. American Journal of Physiology 277, H1027-1035.
7. BORIC, M. P., MARTINEZ, A., DONOSO, M. V. & HUIDOBRO-TORO, J. P. (1995). Neuropeptide Y is a vasoconstrictor and adrenergic modulator in the hamster microcirculation by acting on neuropeptide Y1 and Y2 receptors. European Journal of Pharmacology 294, 391-401.
8. BUSCONI, L. & MICHEL, T. (1993). Endothelial nitric oxide synthase. N-terminal myristoylation determines subcellular localization. Journal of Biological Chemistry 268, 8410-8413.
9. + channels in mediating heterogeneous microvascular responses to acetylcholine in different vascular beds. Journal of Pharmacology and Experimental Therapeutics 282, 1473-1479.
10. CLOUGH, G. F. (1999). Role of nitric oxide in the regulation of microvascular perfusion in human skin in vivo. Journal of Physiology 516, 549-557.
11. COHEN, R. A., PLANE, F., NAJIBI, S., HUK, I, MALINSKI, T. & GARLAND, C. J. (1997). Nitric oxide is the mediator of both endotheliumdependent relaxation and hyperpolarization of the rabbit carotid artery. Proceedings of the National Academy of Sciences of the USA 94, 4193-4198.
12. DIMMELER, S., FLEMING, I., FISSLTHALER, B., HERMANN, C., BUSSE, R. & ZEIHER, A. M. (1999). Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605.
13. DORNYEI, G., KALEY, G. & KOLLER, A. (1997). Release of nitric oxide and prostaglandin H2 to acetylcholine in skeletal muscle venules. American Journal of Physiology 272, H2541-2546.
14. DRAB, M., VERKADE, P., ELGER, M., KASPER, M., LOHN, M., LAUTERBACH, B., MENNE, J., LINDSCHAU, C., MENDE, F., LUFT, F. C., SCHEDI,, A., HALLER, H. & KURZCHALIA, T. V. (2001). Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449-2452.
15. DUNNETT, C. (1964). New tables for multiple comparisons with a control. Biometrics 22, 482-491.
16. DURÁN, W. N., SEYAMA, A., YOSHIMURA, K., GONZALEZ, D. R., JARA, P. I., FIGUEROA, X. F. & BORIC, M. P. (2000). Stimulation of NO production and of eNOS phosphorylation in the microcirculation in vivo. Microvascular Research 60, 104-111.
17. FELETOU, M. & VANHOUTTE, P. M. (1999). The alternative: EDHF. Journal of Molecular and Cellular Cardiology 31, 15-22.
18. FENG, Y., VENEMA, V. J., VENEMA, R. C., TSAI, N. & CALDWELL, R. B. (1999). VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochemical and Biophysical Research Communications 256, 192-197.
19. FERON, O., BELHASSEN, L., KOBZIK, L., SMITH, T. W., KELLY, R. A. & MICHEL, T. (1996). Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. Journal of Biological Chemistry 271, 22810-22814.
20. FERON, O., SALDANA, F., MICHEL, J. B. & MICHEL, T. (1998). The endothelial nitric-oxide synthase-caveolin regulatory cycle. Journal of Biological Chemistry 273, 3125-3128.
21. FIGUEROA, X. F., MARTINEZ, A. D., GONZALEZ, D. R., JARA, P. I., AYALA, S. & BORIC, M. P. (2001a). In vivo assessment of microvascular nitric oxide production and its relation with blood flow. American Journal of Physiology - Heart and Circulatory Physiology 280, H1222-1231.
22. FIGUEROA, X. F., POBLETE, M. I, BORIC, M. P., MENDIZABAL, V. E., ADLER-GRASCHINSKY, E. & HUIDOBRO-TORO, J. P. (2001b). Clonidine-induced nitric oxide-dependent vasorelaxation mediated by endothelial alpha(2)-adrenoceptor activation. British Journal of Pharmacology 134, 957-968.
23. FULTON, D., FONTANA, J, SOWA, G., GRATTON, J. P., LIN, M., LI, K. X., MICHELL, B., KEMP, B. E., RODMAN, D. & 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. Journal of Biological Chemistry 277, 4277-4284.
24. FULTON, D., GRATTON, J. P., MCCABE, T. J., FONTANA, J., FUJIO, Y., WALSH, K., FRANKE, T. F., PAPAPETROPOULOS, A. & SESSA, W. C. (1999). Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399, 597-601.
25. FURCHGOTT, R. F. & ZAWADZKI, J. V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376.
26. GARCIA-CARDEÑA, G., MARTASEK, P., MASTERS, B. S., SKIDD, P. M., COUET, J., LI, S., LISANTI, M. P. & SESSA, W. C. (1997). Dissecting the interaction between nitric oxide synthase (NOS). and caveolin. Functional significance of the NOS caveolin binding domain in vivo. Journal of Biological Chemistry 272, 25437-25440.
27. GOETZ, R. M., THATTE, H. S., PRABHAKAR, P., CHO, M. R., MICHEL, T. & GOLAN, D. E. (1999). Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the USA 96, 2788-2793.
28. ISHII, K., CHANG, B., KERWIN, J. F. JR, HUANG, Z. J. & MURAD, F. (1990). N omega-nitro-L-arginine: a potent inhibitor of endothelium-derived relaxing factor formation. European Journal of Pharmacology 176, 219-223.
29. JU, H., ZOU, R., VENEMA, V. J. & VENEMA, R. C. (1997). Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. Journal of Biological Chemistry 272, 18522-18525.
30. KANAI, A. J., STRAUSS, H. C., TRUSKEY, G. A., CREWS, A. L., GRUNFELD, S. & MALINSKI, T. (1995). Shear stress induces ATP-independent transient nitric oxide release from vascular endothelial cells, measured directly with a porphyrinic microsensor. Circulation Research 77, 284-293.
31. KAWANAKA, H., JONES, M. K., SZABO, I. L., BAATAR, D., PAI, R., TSUGAWA, K., SUGIMACHI, K., SARFEH, I. J. & TARNAWSKI, A. S. (2002). Activation of eNOS in rat portal hypertensive gastric mucosa is mediated by TNF-alpha via the PI 3-kinase-Akt signaling pathway. Hepatology 35, 393-402.
32. KOLLER, A. & KALEY, G. (1991). Endothelial regulation of wall shear stress and blood flow in skeletal muscle microcirculation. American Journal of Physiology 260, H862-868.
33. KUO, L., CHILIAN, W. M. & DAVIS, M. J. (1991). Interaction of pressure-and flow-induced responses in porcine coronary resistance vessels. American Journal of Physiology 261, H1706-1715.
34. LAUER, T., PREIK, M., RASSAF, T., STRAUER, B. E., DEUSSEN, A., FEELISCH, M. & KELM, M. (2001). Plasma nitrite rather than nitrate reflects regional endothelial nitric oxide synthase activity but lacks intrinsic vasodilator action. Proceedings of the National Academy of Sciences of the USA 98, 12814-12819.
35. LIU, J., HUGHES, T. E. & 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. Journal of Cell Biology 137, 1525-1535.
36. MALINSKI, T. & TAHA, Z. (1992). Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature 358, 676-678.
37. 2+-calmodulin and caveolin. Journal of Biological Chemistry 272, 15583-15586.
38. MICHEL, J. B., FERON, O., SASE, K., PRABHAKAR, P. & MICHEL, T. (1997b). Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. Journal of Biological Chemistry 272, 25907-25912.
39. MICHEL, T., LI, G. K. & BUSCONI, L. (1993). Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proceedings of the National Academy of Sciences of the USA 90, 6252-6256.
40. MONCADA, S., PALMER, R. M. & HIGGS, E. A. (1991). Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacological Reviews 43, 109-142.
41. O'BRIEN, A. J., YOUNG, H. M., POVEY, J. M. & FURNESS, J. B. (1995). Nitric oxide synthase is localized predominantly in the Golgi apparatus and cytoplasmic vesicles of vascular endothelial cells. Histochemistry and Cell Biology 103, 221-225.
42. PRABHAKAR, P., THATTE, H. S., GOETZ, R. M., CHO, M. R., GOLAN, D. E. & MICHEL, T. (1998). Receptor-regulated translocation of endothelial nitric-oxide synthase. Journal of Biological Chemistry 273, 27383-27388.
43. RAZANI, B., ENGELMAN, J. A., WANG, X. B., SCHUBERT, W., ZHANG, X. L., MARKS, C. B., MACALUSO, F., RUSSELL, R. G., LI, M., PESTELL, R. G., DI VIZIO, D., HOU, H. JR, KNEITZ, B., LAGAUD, G., CHRIST, G. J., EDELMANN, W. & LISANTI, M. P. (2001). Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. Journal of Biological Chemistry 276, 38121-38138.
44. RIZZO, V., MCINTOSH, D. P., OH, P. & SCHNITZER, J. E. (1998). In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. Journal of Biological Chemistry 273, 34724-34729.
45. ROBINSON, L. J., BUSCONI, L. & MICHEL, T. (1995). Agonist-modulated palmitoylation of endothelial nitric oxide synthase. Journal of Biological Chemistry 270, 995-998.
46. ROBINSON, L. J. & MICHEL, T. (1995). Mutagenesis of palmitoylation sites in endothelial nitric oxide synthase identifies a novel motif for dual acylation and subcellular targeting. Proceedings of the National Academy of Sciences of the USA 92, 11776-11780.
47. SEGAL, S. S., BRETT, S. E. & SESSA, W. C. (1999). Codistribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle of hamsters. American Journal of Physiology 277, H1167-1177.
48. SIMONSEN, U., WADSWORTH, R. M., BUUS, N. H. & MULVANY, M. J. (1999). In vitro simultaneous measurements of relaxation and nitric oxide concentration in rat superior mesenteric artery. Journal of Physiology 516, 271-282.
49. SOWA, G., LIU, J., PAPAPETROPOULOS, A., REX-HAFFNER, M., HUGHES, T. E. & SESSA, W. C. (1999). Trafficking of endothelial nitric-oxide synthase in living cells. Quantitative evidence supporting the role of palmitoylation as a kinetic trapping mechanism limiting membrane diffusion. Journal of Biological Chemistry 274, 22524-22531.
50. SUN, D., KALEY, G. & KOLLER, A. (1994). Characteristics and origin of myogenic response in isolated gracilis muscle arterioles. American Journal of Physiology 266, H1177-1183.
51. THURINGER, D., RUCKER-MARTIN, C. & FRELIN, C. (2000). Cardiac capillary cells release biologically active nitric oxide at an early stage of in vitro development. Cardiovascular Research 47, 726-737.
52. i in activation of eNOS in pressurized arterioles by agonists and wall shear stress. American Journal of Physiology - Heart and Circulatory Physiology 281, H606-612.
53. VENEMA, V. J., MARRERO, M. B. & VENEMA, R. C. (1996). Bradykinin-stimulated protein tyrosine phosphorylation promotes endothelial nitric oxide synthase translocation to the cytoskeleton. Biochemical and Biophysical Research Communications 226, 703-710.
54. VENEMA, V. J., ZOU, R., JU, H., MARRERO, M. B. & VENEMA, R. C. (1997). Caveolin-1 detergent solubility and association with endothelial nitric oxide synthase is modulated by tyrosine phosphorylation. Biochemical and Biophysical Research Communications 236, 155-161.
55. WANG, Q., PATTON, W. F., HECHTMAN, H. B. & SHEPRO, D. (1997). A novel anti-inflammatory peptide inhibits endothelial cell cytoskeletal rearrangement, nitric oxide synthase translocation, and paracellular permeability increases. Journal of Cellular Physiology 172, 171-182.
56. (2+)-calmodulin. Journal of Biological Chemistry 274, 33148-33154.