Synthesis of cysteinyl leukotrienes in human endothelial cells: Subcellular localization and autocrine signaling through the CysLT 2 receptor

FASEB Journal

Volumn 25, Issue 10, 2011, Pages 3519-3528

  Carnini, Chiara ^a,c   Accomazzo, Maria Rosa ^a   Borroni, Emanuele ^a   Vitellaro Zuccarello, Laura ^a   Durand, Thierry ^b   Folco, Giancarlo ^a   Rovati, G Enrico ^a   Capra, Valerie ^a   Sala, Angelo ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITÉ DE MONTPELLIER   (France)

^c CHIESI FARMACEUTICI S P A   (Italy)

Author keywords

Intracellular Ca 2+; Microsomal glutathione S transferase II; Signal transduction

Indexed keywords

3 [3 TERT BUTYLTHIO 1 (4 CHLOROBENZYL) 5 ISOPROPYL 2 INDOLYL] 2,2 DIMETHYLPROPIONIC ACID; GLUTATHIONE TRANSFERASE; LEUKOTRIENE A4; LEUKOTRIENE C4; LEUKOTRIENE C4 SYNTHASE; LEUKOTRIENE RECEPTOR; PEPTIDOLEUKOTRIENE; PEPTIDOLEUKOTRIENE 1 RECEPTOR; PEPTIDOLEUKOTRIENE 2 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; AUTOCRINE EFFECT; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG SYNTHESIS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IC 50; IMMUNOGOLD ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SIGNAL TRANSDUCTION; SUICIDE; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING;

ANIMALS; AUTOCRINE COMMUNICATION; BIOLOGICAL TRANSPORT; BLOOD PLATELETS; CALCIUM SIGNALING; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; HUMANS; LEUKOTRIENE A4; LEUKOTRIENE C4; RECEPTORS, LEUKOTRIENE;

EID: 80053904558     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-177030     Document Type: Article

References (52)

1. Murphy, R. C., Hammaström, S., and Samuelsson, B. (1979) Leukotriene C: slow-reacting substance from murine mastocytoma cells. Proc. Natl. Acad. Sci. U. S. A. 76, 4275-4279 (Pubitemid 9256544)
2. 4 synthesized by polymorphonuclear leukocytes. J. Biol. Chem. 261, 16466-16472
3. Zarini, S., Gijon, M. A., Ransome, A. E., Murphy, R. C., and Sala, A. (2009) Transcellular biosynthesis of cysteinyl leukotrienes in vivo during mouse peritoneal inflammation. Proc. Natl. Acad. Sci. U. S. A. 106, 8296-8301
4. Sala, A., Rossoni, G., Berti, F., Buccellati, C., Bonazzi, A., Maclouf, J., and Folco, G. (2000) Monoclonal anti-CD18 antibody prevents transcellular biosynthesis of cysteinyl leukotrienes in vitro and in vivo and protects against leukotriene-dependent increase in coronary vascular resistance and myocardial stiffness. Circulation 101, 1436-1440 (Pubitemid 30169867)
5. Di Gennaro, A., Carnini, C., Buccellati, C., Ballerio, R., Zarini, S., Fumagalli, F., Viappiani, S., Librizzi, L., Hernandez, A., Murphy, R. C., Constantin, G., De Curtis, M., Folco, G., and Sala, A. (2004) Cysteinyl-leukotrienes receptor activation in brain inflammatory reactions and cerebral edema formation: a role for transcellular biosynthesis of cysteinyl-leukotrienes. FASEB J. 18, 842-844
6. Capra, V., Thompson, M. D., Sala, A., Cole, D. E., Folco, G., and Rovati, G. E. (2007) Cysteinyl-leukotrienes and their receptors in asthma and other inflammatory diseases: critical update and emerging trends. Med. Res. Rev. 27, 469-527 (Pubitemid 46984658)
7. Rovati, G. E., and Capra, V. (2007) Cysteinyl-leukotriene receptors and cellular signals. Scientific World J. 7, 1375-1392 (Pubitemid 47435434)
8. Ciana, P., Fumagalli, M., Trincavelli, M. L., Verderio, C., Rosa, P., Lecca, D., Ferrario, S., Parravicini, C., Capra, V., Gelosa, P., Guerrini, U., Belcredito, S., Cimino, M., Sironi, L., Tremoli, E., Rovati, G. E., Martini, C., and Abbracchio, M. P. (2006) The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J. 25, 4615- 4627
9. 4 in mice lacking the cysteinyl leukotriene 1 and 2 receptors. Proc. Natl. Acad. Sci. U. S. A. 105, 16695-16700
10. Kamohara, M., Takasaki, J., Matsumoto, M., Matsumoto, S., Saito, T., Soga, T., Matsushime, H., and Furuichi, K. (2001) Functional characterization of cysteinyl leukotriene CysLT2 receptor on human coronary artery smooth muscle cells. Biochem. Biophys. Res. Commun. 287, 1088-1092 (Pubitemid 32980563)
11. Mellor, E. A., Frank, N., Soler, D., Hodge, M. R., Lora, J. M., Austen, K. F., and Boyce, J. A. (2003) Expression of the type 2 receptor for cysteinyl leukotrienes (CysLT2R) by human mast cells: Functional distinction from CysLT1R. Proc. Natl. Acad. Sci. U. S. A. 100, 11589-11593 (Pubitemid 37205980)
12. Mechiche, H., Candenas, L., Pinto, F. M., Nazeyrollas, P., Clement, C., and Devillier, P. (2004) Characterization of cysteinyl leukotriene receptors on human saphenous veins: antagonist activity of montelukast and its metabolites. J. Cardiovasc. Pharmacol. 43, 113-120 (Pubitemid 38032072)
13. Mita, H., Hasegawa, M., Saito, H., and Akiyama, K. (2001) Levels of cysteinyl leukotriene receptormRNAin human peripheral leucocytes: significantly higher expression of cysteinyl leukotriene receptor 2 mRNA in eosinophils. Clin. Exp. Allergy 31, 1714-1723 (Pubitemid 34204428)
14. Sjostrom, M., Johansson, A. S., Schroder, O., Qiu, H., Palmblad, J., and Haeggstrom, J. Z. (2003) Dominant expression of the CysLT2 receptor accounts for calcium signaling by cysteinyl leukotrienes in human umbilical vein endothelial cells. Arterioscler. Thromb. Vasc. Biol. 23, e37-41
15. Lotzer, K., Spanbroek, R., Hildner, M., Urbach, A., Heller, R., Bretschneider, E., Galczenski, H., Evans, J. F., and Habenicht, A. J. (2003) Differential leukotriene receptor expression and calcium responses in endothelial cells and macrophages indicate 5-lipoxygenase-dependent circuits of inflammation and atherogenesis. Arterioscler. Thromb. Vasc. Biol. 23, e32-e36
16. 4 stimulates the migration but not proliferation of endothelial cells mediated by the cysteinyl leukotriene cysLT1 receptor via the extracellular signal-regulated kinase pathway. J. Pharmacol. Sci. 109, 285-292
17. Maciag, T., Hoover, G. A., and Weinstein, R. (1982) High and low molecular weight forms of endothelial cell growth factor. J. Biol. Chem. 257, 5333-5336 (Pubitemid 12015906)
18. Gordon, P. B., Sussman, I. I., and Hatcher, V. B. (1983) Long-term culture of human endothelial cells. In Vitro 19, 661-671 (Pubitemid 15212476)
19. 4 synthase. Biochem. J. 328, 225-229
20. Patscheke, H. (1981) Shape and functional properties of human platelets washed with acid citrate. Haemostasis 10, 14-27
21. 4 from human polymorphonuclear leukocytes. J. Biol. Chem. 271, 17944-17948
22. Capra, V., Ravasi, S., Accomazzo, M. R., Citro, S., Grimoldi, M., Abbracchio, M. P., and Rovati, G. E. (2005) CysLT1 receptor is a target for extracellular nucleotide-induced heterologous desensitization: a possible feedback mechanism in inflammation. J. Cell Sci. 118, 5625-5636 (Pubitemid 43079301)
23. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450
24. Rovati, G. E. (1998) Ligand-binding studies: old beliefs and new strategies. Trends Pharmacol. Sci. 19, 365-369
25. Munson, P. J., and Rodbard, D. (1980) Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal. Biochem. 107, 220-239
26. De Lean, A., Munson, P. J., and Rodbard, D. (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am. J. Physiol. Endocrinol. Metab. 235, E97-E102 (Pubitemid 9159876)
27. 4 hydrolase/aminopeptidase. Ann. N. Y. Acad. Sci. 744, 31-38
28. Heise, C. E., O'Dowd, B. F., Figueroa, D. J., Sawyer, N., Nguyen, T., Im, D. S., Stocco, R., Bellefeuille, J. N., Abramovitz, M., Cheng, R., Williams, D. L., Jr., Zeng, Z., Liu, Q., Ma, L., Clements, M. K., Coulombe, N., Liu, Y., Austin, C. P., George, S. R., O'Neill, G. P., Metters, K. M., Lynch, K. R., and Evans, J. F. (2000) Characterization of the human cysteinyl leukotriene 2 receptor. J. Biol. Chem. 275, 30531-30536
29. Capra, V., Nicosia, S., Ragnini, D., Mezzetti, M., Keppler, D., and Rovati, G. E. (1998) Identification and characterization of two cysteinyl-leukotriene high affinity binding sites with receptor characteristics in human lung parenchyma. Mol. Pharmacol. 53, 750-758 (Pubitemid 28196499)
30. 4 in differentiated U937 cells. Prostaglandins Other Lipid Mediat. 71, 235-251
31. Takasaki, J., Saito, T., Taniguchi, M., Kawasaki, T., Moritani, Y., Hayashi, K., and Kobori, M. (2004) A novel Gαq/11-selective inhibitor. J. Biol. Chem. 279, 47438-47445
32. Folco, G., Rossoni, G., Buccellati, C., Berti, F., Maclouf, J., and Sala, A. (2000) Leukotrienes in cardiovascular diseases. Am. J. Respir. Crit. Care Med. 161, S112-S116 (Pubitemid 30129427)
33. Lefer, A. M. (1988) Thromboxane A2 and leukotrienes are eicosanoid mediators of shock and ischemic disorders. Prog. Clin. Biol. Res. 264, 101-114
34. De Caterina, R., Giannessi, D., Lazzerini, G., Bernini, W., Sicari, R., Cupelli, F., Lenzi, S., Rugolotto, M. M., Madonna, R., and Maclouf, J. (2010) Sulfido-peptide leukotrienes in coronary heart disease - relationship with disease instability and myocardial ischaemia. Eur. J. Clin. Invest. 40, 258-272
35. Rossoni, G., Sala, A., Berti, F., Testa, T., Buccellati, C., Molta, C., Muller-Peddinghaus, R., Maclouf, J., and Folco, G. C. (1996) Myocardial protection by the leukotriene synthesis inhibitor BAY X1005: importance of transcellular biosynthesis of cysteinyl-leukotrienes. J. Pharmacol. Exp. Ther. 276, 335-341 (Pubitemid 26150973)
36. Welt, K., Fitzl, G., and Mark, B. (2000) Lipoxygenase inhibitor FLM 5011, an effective protectant of myocardial microvessels against ischemia-reperfusion injury? An ultrastructural-morphometric study. Exp. Toxicol. Pathol. 52, 27-36 (Pubitemid 30176948)
37. Helgadottir, A., Manolescu, A., Thorleifsson, G., Gretarsdottir, S., Jonsdottir, H., Thorsteinsdottir, U., Samani, N. J., Gudmundsson, G., Grant, S. F., Thorgeirsson, G., Sveinbjornsdottir, S., Valdimarsson, E. M., Matthiasson, S. E., Johannsson, H., Gudmundsdottir, O., Gurney, M. E., Sainz, J., Thorhallsdottir, M., Andresdottir, M., Frigge, M. L., Topol, E. J., Kong, A., Gudnason, V., Hakonarson, H., Gulcher, J. R., and Stefansson, K. (2004) The gene encoding 5-lipoxygenase activating protein confers risk of myocardial infarction and stroke. Nat. Genet. 36, 233-239 (Pubitemid 38282747)
38. Helgadottir, A., Gretarsdottir, S., St Clair, D., Manolescu, A., Cheung, J., Thorleifsson, G., Pasdar, A., Grant, S. F., Whalley, L. J., Hakonarson, H., Thorsteinsdottir, U., Kong, A., Gulcher, J., Stefansson, K., and MacLeod, M. J. (2005) Association between the gene encoding 5-lipoxygenase-activating protein and stroke replicated in a Scottish population. Am. J. Hum. Genet. 76, 505-509 (Pubitemid 40250529)
39. 4 synthase gene promoter polymorphism and coronary artery calcium in young women: the Muscatine study. Arterioscler. Thromb. Vasc. Biol. 27, 394-399
40. Hakonarson, H., Thorvaldsson, S., Helgadottir, A., Gudbjartsson, D., Zink, F., Andresdottir, M., Manolescu, A., Arnar, D. O., Andersen, K., Sigurdsson, A., Thorgeirsson, G., Jonsson, A., Agnarsson, U., Bjornsdottir, H., Gottskalksson, G., Einarsson, A., Gudmundsdottir, H., Adalsteinsdottir, A. E., Gudmundsson, K., Kristjansson, K., Hardarson, T., Kristinsson, A., Topol, E. J., Gulcher, J., Kong, A., Gurney, M., and Stefansson, K. (2005) Effects of a 5-lipoxygenase-activating protein inhibitor on biomarkers associated with risk of myocardial infarction: a randomized trial. JAMA 293, 2245-2256 (Pubitemid 40629191)
41. Tardif, J. C., L'Allier, P., L., Ibrahim, R., Gregoire, J. C., Nozza, A., Cossette, M., Kouz, S., Lavoie, M. A., Paquin, J., Brotz, T. M., Taub, R., and Pressacco, J. (2010) Treatment with 5-lipoxygenase inhibitor VIA-2291 (Atreleuton) in patients with recent acute coronary syndrome. Circ. Cardiovasc. Imaging 3, 298-307
42. Poeckel, D., and Funk, C. D. (2010) The 5-lipoxygenase/leukotriene pathway in preclinical models of cardiovascular disease. Cardiovasc. Res. 86, 243-253
43. Lam, B. K., Owen, W. F., Jr., Austen, K. F., and Soberman, R. J. (1989) The identification of a distinct export step following the biosynthesis of leukotriene C4 by human eosinophils. J. Biol. Chem. 264, 12885-12889 (Pubitemid 19194859)
44. 4 via microsomal glutathione S-transferase type 2 and express the CysLT1 receptor. Eur. J. Biochem. 268, 2578-2586
45. Schroder, O., Sjostrom, M., Qiu, H., Stein, J., Jakobsson, P. J., and Haeggstrom, J. Z. (2003) Molecular and catalytic properties of three rat leukotriene C4 synthase homologs. Biochem. Biophys. Res. Commun. 312, 271-276 (Pubitemid 37448567)
46. 4 stimulate human endothelial cells to synthesize platelet-activating factor and bind neutrophils. Proc. Natl. Acad. Sci. U. S. A. 83, 2204-2208
47. Uzonyi, B., Lotzer, K., Jahn, S., Kramer, C., Hildner, M., Bretschneider, E., Radke, D., Beer, M., Vollandt, R., Evans, J. F., Funk, C. D., and Habenicht, A. J. (2006) Cysteinyl leukotriene 2 receptor and protease-activated receptor 1 activate strongly correlated early genes in human endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 103, 6326-6331
48. Zhao, L., Moos, M. P., Grabner, R., Pedrono, F., Fan, J., Kaiser, B., John, N., Schmidt, S., Spanbroek, R., Lotzer, K., Huang, L., Cui, J., Rader, D. J., Evans, J. F., Habenicht, A. J., and Funk, C. D. (2004) The 5-lipoxygenase pathway promotes pathogenesis of hyperlipidemia-dependent aortic aneurysm. Nat. Med. 10, 966-973 (Pubitemid 39273738)
49. Jiang, W., Hall, S. R., Moos, M. P., Cao, R. Y., Ishii, S., Ogunyankin, K. O., Melo, L. G., and Funk, C. D. (2008) Endothelial cysteinyl leukotriene 2 receptor expression mediates myocardial ischemia-reperfusion injury. Am. J. Pathol. 172, 592-602 (Pubitemid 351354533)
50. Woszczek, G., Chen, L. Y., Nagineni, S., Alsaaty, S., Harry, A., Logun, C., Pawliczak, R., and Shelhamer, J. H. (2007) IFN-γ induces cysteinyl leukotriene receptor 2 expression and enhances the responsiveness of human endothelial cells to cysteinyl leukotrienes. J. Immunol. 178, 5262-5270 (Pubitemid 46595311)
51. Zhou, G., Zhou, Z., Ge, S., Liu, D., Zhang, R., Xu, G., Zhu, W., Yin, Q., Chen, A. F., and Liu, X. (2009) IL-18 accelerates the cell apoptosis by up-regulating cysteinyl leukotriene 2 receptor expression in human umbilical vein endothelial cells at the early stage of administration. Vascul. Pharmacol. 50, 171-177
52. Riccioni, G., Capra, V., D'Orazio, N., Bucciarelli, T., and Bazzano, L. A. (2008) Leukotriene modifiers in the treatment of cardiovascular diseases. J. Leukoc. Biol. 84, 1374-1378 (Pubitemid 352774472)