Intracellular endothelin type B receptor-driven Ca2+ signal elicits nitric oxide production in endothelial cells

Journal of Biological Chemistry

Volumn 287, Issue 49, 2012, Pages 41023-41031

  Deliu, Elena ^a   Brailoiu, G Cristina ^b   Mallilankaraman, Karthik ^a   Wang, Hong ^a   Madesh, Muniswamy ^a   Undieh, Ashiwel S ^b   Koch, Walter J ^a   Brailoiu, Eugen ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOLIC; CYTOSOLIC CALCIUM; DOSE-DEPENDENT; ENDOTHELIAL FUNCTION; ENDOTHELIN; ENDOTHELIN-1; IMAGING METHOD; MICRO-INJECTION; MICROAUTOPHAGY; NITRIC OXIDE FORMATION; NUCLEAR MEMBRANES; PHOSPHOLIPASE C; PLASMALEMMA; PROTEIN COUPLED RECEPTORS; TRANSFECTED CELLS;

CELL MEMBRANES; CYTOLOGY; ENDOTHELIAL CELLS; NITRIC OXIDE; SUGARS;

CALCIUM;

CALCIUM; ENDOTHELIN 1; ENDOTHELIN B RECEPTOR; NITRIC OXIDE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; MICROAUTOPHAGY; MICROINJECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR UPREGULATION;

ANIMALS; AUTOPHAGY; CALCIUM; CALCIUM SIGNALING; CELL NUCLEUS; CELLS, CULTURED; CYTOSOL; ENDOSOMES; ENDOTHELIAL CELLS; ENDOTHELIN-1; LYSOSOMES; MICROCIRCULATION; MODELS, BIOLOGICAL; NITRIC OXIDE; OXIDATION-REDUCTION; RATS; RECEPTOR, ENDOTHELIN B; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84870324879     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.418533     Document Type: Article

References (61)

1. Calebiro, D., Nikolaev, V. O., and Lohse, M. J. (2010) Imaging of persistent cAMP signaling by internalized G protein-coupled receptors. J. Mol. Endocrinol. 45, 1-8
2. Re, R. N., and Cook, J. L. (2007) Mechanisms of disease: Intracrine physiology in the cardiovascular system. Nat. Clin. Pract. Cardiovasc. Med. 4, 549-557 (Pubitemid 47490762)
3. Tadevosyan, A., Vaniotis, G., Allen, B. G., Hébert, T. E., and Nattel, S. (2012) G protein-coupled receptor signalling in the cardiac nuclear membrane: evidence and possible roles in physiological and pathophysiological function. J. Physiol. 590, 1313-1330
4. Avedanian, L., Riopel, J., Bkaily, G., Nader, M., D'Orleans-Juste, P., and Jacques, D. (2010) ETA receptors are present in human aortic vascular endothelial cells and modulate intracellular calcium. Can. J. Physiol. Pharmacol. 88, 817-829
5. Bkaily, G., Avedanian, L., Al-Khoury, J., Provost, C., Nader, M., D'Orléans-Juste, P., and Jacques, D. (2011) Nuclear membrane receptors for ET-1 in cardiovascular function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R251-263
6. Loesch, A. (2005) Localisation of endothelin-1 and its receptors in vascular tissue as seen at the electron microscopic level. Curr. Vasc. Pharmacol. 3, 381-392
7. Abe, Y., Nakayama, K., Yamanaka, A., Sakurai, T., and Goto, K. (2000) Subtype-specific trafficking of endothelin receptors. J. Biol. Chem. 275, 8664-8671 (Pubitemid 30180217)
8. Bremnes, T., Paasche, J. D., Mehlum, A., Sandberg, C., Bremnes, B., and Attramadal, H. (2000) Regulation and intracellular trafficking pathways of the endothelin receptors. J. Biol. Chem. 275, 17596-17604 (Pubitemid 30430805)
9. Oksche, A., Boese, G., Horstmeyer, A., Furkert, J., Beyermann, M., Bienert, M., and Rosenthal, W. (2000) Late endosomal/lysosomal targeting and lack of recycling of the ligand-occupied endothelin B receptor. Mol. Pharmacol. 57, 1104-1113 (Pubitemid 30354382)
10. Eguchi, S., Hirata, Y., Imai, T., and Marumo, F. (1995) Endothelin-1 as an autocrine growth factor for endothelial cells. J. Cardiovasc. Pharmacol. 26, S279-283
11. Mazzuca, M. Q., and Khalil, R. A. (2012) Vascular endothelin receptor type B: Structure, function and dysregulation in vascular disease. Biochem. Pharmacol. 84, 147-162
12. Schiffrin, E. L. (2005) Vascular endothelin in hypertension. Vascul. Pharmacol. 43, 19-29
13. Brailoiu, G. C., Brailoiu, E., Parkesh, R., Galione, A., Churchill, G. C., Patel, S., and Dun, N. J. (2009) NAADP-mediated channel "chatter" in neurons of the rat medulla oblongata. Biochem. J. 419, 91-97, 92 p following 97
14. Brailoiu, G. C., Deliu, E., Tica, A. A., Chitravanshi, V. C., and Brailoiu, E. (2012) Urocortin 3 elevates cytosolic calcium in nucleus ambiguus neurons. J. Neurochem. 122, 1129-1136
15. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450 (Pubitemid 15114340)
16. Brailoiu, G. C., Oprea, T. I., Zhao, P., Abood, M. E., and Brailoiu, E. (2011) Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J. Biol. Chem. 286, 29166-29174
17. Deliu, E., Tica, A. A., Motoc, D., Brailoiu, G. C., and Brailoiu, E. (2011) Intracellular angiotensin II activates rat myometrium. Am. J. Physiol. Cell Physiol. 301, C559-565
18. Tica, A. A., Dun, E. C., Tica, O. S., Gao, X., Arterburn, J. B., Brailoiu, G. C., Oprea, T. I., and Brailoiu, E. (2011) G protein-coupled estrogen receptor 1-mediated effects in the rat myometrium. Am. J. Physiol. Cell Physiol. 301, C1262-1269
19. Deliu, E., Brailoiu, G. C., Arterburn, J. B., Oprea, T. I., Benamar, K., Dun, N. J., and Brailoiu, E. (2012) G protein-coupled estrogen receptor 1-mediated effects in the rat myometrium. J. Pain 13, 742-754
20. 2+-entry antagonist LU 52396: its inhibitory activity depends on the activation state of the cells. Cell Calcium 22, 91-97
21. Rubin, D. B., Drab, E. A., and Bauer, K. D. (1989) Endothelial cell subpopulations in vitro: cell volume, cell cycle, and radiosensitivity. J. Appl. Physiol. 67, 1585-1590 (Pubitemid 19276414)
22. Brailoiu, G. C., Gurzu, B., Gao, X., Parkesh, R., Aley, P. K., Trifa, D. I., Galione, A., Dun, N. J., Madesh, M., Patel, S., Churchill, G. C., and Brailoiu, E. (2010) Acidic NAADP-sensitive calcium stores in the endothelium: agonist-specific recruitment and role in regulating blood pressure. J. Biol. Chem. 285, 37133-37137
23. Tang, L., Luo, B., Patel, R. P., Ling, Y., Zhang, J., and Fallon, M. B. (2007) Modulation of pulmonary endothelial endothelin B receptor expression and signaling: implications for experimental hepatopulmonary syndrome. Am. J. Physiol. Lung. Cell Mol. Physiol. 292, L1467-1472 (Pubitemid 47077363)
24. Betina, V. (1992) Biological effects of the antibiotic brefeldinA(decumbin, cyanein, ascotoxin, synergisidin): a retrospective. Folia Microbiol. 37, 3-11
25. Bowman, E. J., Siebers, A., and Altendorf, K. (1988) Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. 85, 7972-7976
26. Kunz, J. B., Schwarz, H., and Mayer, A. (2004) Determination of four sequential stages during microautophagy in vitro. J. Biol. Chem. 279, 9987-9996 (Pubitemid 38372601)
27. Berg, T. O., Strømhaug, E., Løvdal, T., Seglen, O., and Berg, T. (1994) Use of glycyl-L-phenylalanine 2-naphthylamide, a lysosome-disrupting cathepsin C substrate, to distinguish between lysosomes and prelysosomal endocytic vacuoles. Biochem. J. 300, 229-236 (Pubitemid 24151040)
28. Naylor, E., Arredouani, A., Vasudevan, S. R., Lewis, A. M., Parkesh, R., Mizote, A., Rosen, D., Thomas, J. M., Izumi, M., Ganesan, A., Galione, A., and Churchill, G. C. (2009) Identification of a chemical probe for NAADP by virtual screening. Nat. Chem. Biol. 5, 220-226
29. Schneider, M. P., Boesen, E. I., and Pollock, D. M. (2007) Contrasting actions of endothelin ET(A) and ET(B) receptors in cardiovascular disease. Annu. Rev. Pharmacol. Toxicol. 47, 731-759
30. Bourque, S. L., Davidge, S. T., and Adams, M. A. (2011) The interaction between endothelin-1 and nitric oxide in the vasculature: new perspectives. Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R1288-1295
31. Black, S. M., and Fineman, J. R. (2006) Oxidative and nitrosative stress in pediatric pulmonary hypertension: roles of endothelin-1 and nitric oxide. Vascul. Pharmacol. 45, 308-316 (Pubitemid 44765294)
32. Jafri, F., and Ergul, A. (2003) Nuclear localization of endothelin-converting enzyme-1: subisoform specificity. Arterioscler. Thromb. Vasc. Biol. 23, 2192-2196 (Pubitemid 37532319)
33. Russell, F. D., and Davenport, A. P. (1999) Evidence for intracellular endothelin-converting enzyme-2 expression in cultured human vascular endothelial cells. Circ. Res. 84, 891-896 (Pubitemid 29196733)
34. 2+ increases in A7r5 vascular smooth muscle cells. Eur. J. Pharmacol. 420, 9-18
35. Haller, H., Lindschau, C., Erdmann, B., Quass, P., and Luft, F. C. (1996) Effects of intracellular angiotensin II in vascular smooth muscle cells. Circ. Res. 79, 765-772 (Pubitemid 26317824)
36. 2+ mobilization by stimulating intracellular AT1 receptors in proximal tubule cells. Am. J. Physiol. Renal. Physiol. 290, F1382-1390
37. Bénard, G., Massa, F., Puente, N., Lourenço, J., Bellocchio, L., Soria-Gómez, E., Matias, I., Delamarre, A., Metna-Laurent, M., Cannich, A., Hebert-Chatelain, E., Mulle, C., Ortega-Gutiérrez, S., Martín-Fontecha, M., Klugmann, M., Guggenhuber, S., Lutz, B., Gertsch, J., Chaouloff, F., López- Rodríguez, M. L., Grandes, P., Rossignol, R., and Marsicano, G. (2012) Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat. Neurosci. 15, 558-564
38. den Boon, F. S., Chameau, P., Schaafsma-Zhao, Q., van Aken, W., Bari, M., Oddi, S., Kruse, C. G., Maccarrone, M., Wadman, W. J., and Werkman, T. R. (2012) Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc. Natl. Acad. Sci. 109, 3534-3539
39. Revankar, C. M., Cimino, D. F., Sklar, L. A., Arterburn, J. B., and Prossnitz, E. R. (2005) A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307, 1625-1630 (Pubitemid 40354745)
40. Loesch, A., Gajkowska, B., Dashwood, M. R., Fioretto, E. T., Gagliardo, K. M., Lima, A. R., and Ribeiro, A. A. (2005) Endothelin-1 and endothelin receptors in the basilar artery of the capybara. J. Mol. Histol. 36, 25-34 (Pubitemid 40614379)
41. O'Brien, R. F., Robbins, R. J., and McMurtry, I. F. (1987) Endothelial cells in culture produce a vasoconstrictor substance. J. Cell Physiol. 132, 263-270 (Pubitemid 17151479)
42. Yanagisawa, M., Kurihara, H., Kimura, S., Tomobe, Y., Kobayashi, M., Mitsui, Y., Yazaki, Y., Goto, K., and Masaki, T. (1988) A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332, 411-415 (Pubitemid 18090241)
43. +-ATPase and the Golgi apparatus in the recycling of PTH/ PTHrP receptor. Am. J. Physiol. Endocrinol. Metab. 286, E704-710
44. Foster, N., Loi, T. H., Owe-Young, R., and Stanley, K. K. (2003) Lysosomal traffic of liganded endothelin B receptor. Biochim. Biophys. Acta 1642, 45-52 (Pubitemid 37338277)
45. Boya, P. (2012) Lysosomal function and dysfunction: mechanism and disease. Antioxid. Redox. Signal. 17, 766-774
46. Gruenberg, J. (2001) The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2, 721-730
47. Sorkin, A., and von Zastrow, M. (2009) Endocytosis and signalling: inter-twining molecular networks. Nat. Rev. Mol. Cell Biol. 10, 609-622
48. Li, W. W., Li, J., and Bao, J. K. (2012) Microautophagy: lesser-known self-eating. Cell Mol. Life Sci. 69, 1125-1136
49. Patel, S., Marchant, J. S., and Brailoiu, E. (2010) Two-pore channels: Regulation byNAADPand customized roles in triggering calcium signals. Cell Calcium 47, 480-490
50. 2+ release via acid store IP3 receptors. Proc. Natl. Acad. Sci. U.S.A. 106, 10758-10763
51. Matsuzawa, Y., and Hostetler, K. Y. (1980) Properties of phospholipase C isolated from rat liver lysosomes. J. Biol. Chem. 255, 646-652 (Pubitemid 10112368)
52. Griffith, O. W., and Stuehr, D. J. (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu. Rev. Physiol. 57, 707-736
53. Nathan, C., and Xie, Q. W. (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78, 915-918 (Pubitemid 24292319)
54. 2+ release modulates endothelial nitric-oxide synthase via extracellular signal-regulated kinase (ERK) 1/2-mediated serine 635 phosphorylation. J. Biol. Chem. 286, 20100-20108
55. Cook, J. L., and Re, R. N. (2012) Lessons from in vitro studies and a related intracellular angiotensin II transgenic mouse model. Am. J. Physiol. Regul. Integr. Comp. Physiol. 302, R482-493
56. Re, R. N., and Cook, J. L. (2011) Noncanonical intracrine action. J. Am. Soc. Hypertens. 5, 435-448
57. Barton, M., and Yanagisawa, M. (2008) Endothelin: 20 years from discovery to therapy. Can. J. Physiol. Pharmacol. 86, 485-498
58. Muller, G., and Morawietz, H. (2009) Nitric oxide, NAD(P)H oxidase, and atherosclerosis. Antioxid. Redox. Signal. 11, 1711-1731
59. Takayanagi, R., Kitazumi, K., Takasaki, C., Ohnaka, K., Aimoto, S., Tasaka, K., Ohashi, M., and Nawata, H. (1991) Presence of non-selective type of endothelin receptor on vascular endothelium and its linkage to vasodilation. FEBS Lett. 282, 103-106
60. Bagnall, A. J., Kelland, N. F., Gulliver-Sloan, F., Davenport, A. P., Gray, G. A., Yanagisawa, M., Webb, D. J., and Kotelevtsev, Y. V. (2006) Deletion of endothelial cell endothelin B receptors does not affect blood pressure or sensitivity to salt. Hypertension 48, 286-293 (Pubitemid 44309825)
61. Li, X. C., Cook, J. L., Rubera, I., Tauc, M., Zhang, F., and Zhuo, J. L. (2011) Intrarenal transfer of an intracellular fluorescent fusion of angiotensin II selectively in proximal tubules increases blood pressure in rats and mice. Am. J. Physiol. Renal. Physiol. 300, F1076-1088