Cysteinyl leukotriene signaling through perinuclear CysLT1 receptors on vascular smooth muscle cells transduces nuclear calcium signaling and alterations of gene expression

Journal of Molecular Medicine

Volumn 90, Issue 10, 2012, Pages 1223-1231

  Eaton, Alison ^a   Nagy, Edit ^a   Pacault, Mathilde ^a   Fauconnier, Jérémy ^a,b   Bäck, Magnus ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MONTPELLIER   (France)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Atherosclerosis; Eicosanoids; Inflammation; Lipoxygenase; PAI 2

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALCIUM; CYSTEINYL LEUKOTRIENE 1 RECEPTOR; LEUKOTRIENE C4; LEUKOTRIENE RECEPTOR; LIPOPOLYSACCHARIDE; MESSENGER RNA; PEPTIDOLEUKOTRIENE; PLASMINOGEN ACTIVATOR INHIBITOR 2; UNCLASSIFIED DRUG; VERLUKAST;

ARTICLE; ATHEROSCLEROSIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CAROTID ENDARTERECTOMY; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY ATHEROSCLEROSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROARRAY ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ATHEROSCLEROSIS; CALCIUM SIGNALING; CELL NUCLEUS; CELLS, CULTURED; CORONARY VESSELS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; LEUKOTRIENE C4; LIPOPOLYSACCHARIDES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PLASMINOGEN ACTIVATOR INHIBITOR 2; RECEPTORS, LEUKOTRIENE; TRANSCRIPTIONAL ACTIVATION;

EID: 84867328563     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-012-0904-1     Document Type: Article

References (34)

1. Poeckel D, Funk CD (2010) The 5-lipoxygenase/leukotriene pathway in preclinical models of cardiovascular disease. Cardiovasc Res 86:243-253. doi:10.1093/cvr/cvq016
2. Bäck M, Hansson GK (2006) Leukotriene receptors in atherosclerosis. Ann Med 38:493-502
3. Houard X, Ollivier V, Louedec L, Michel JB, Bäck M (2009) Differential inflammatory activity across human abdominal aortic aneurysms reveals neutrophil-derived leukotriene B4 as a major chemotactic factor released from the intraluminal thrombus. FASEB J 23:1376-1383. doi:10.1096/fj.08-116202
4. Nagy E, Andersson DC, Caidahl K, Eriksson MJ, Eriksson P, Franco-Cereceda A, Hansson GK, Bäck M (2011) Upregulation of the 5-lipoxygenase pathway in human aortic valves correlates with severity of stenosis and leads to leukotriene-induced effects on valvular myofibroblasts. Circulation 123:1316-1325. doi:10.1161/CIRCULATIONAHA.110.966846
5. Piomelli D, Feinmark SJ, Cannon PJ (1987) Leukotriene biosynthesis by canine and human coronary arteries. J Pharmacol Exp Ther 241:763-770
6. Carry M, Korley V, Willerson JT, Weigelt L, Ford-Hutchinson AW, Tagari P (1992) Increased urinary leukotriene excretion in patients with cardiac ischemia. In vivo evidence for 5-lipoxygenase activation. Circulation 85:230-236
7. Mueller CF, Wassmann K, Widder JD, Wassmann S, Chen CH, Keuler B, Kudin A, Kunz WS, Nickenig G (2008) Multidrug resistance protein-1 affects oxidative stress, endothelial dysfunction, and atherogenesis via leukotriene C4 export. Circulation 117:2912-2918. doi:CIRCULATIONAHA.107.747667
8. Jawien J, Gajda M, Wolkow P, Zuranska J, Olszanecki R, Korbut R (2008) The effect of montelukast on atherogenesis in apoE/LDLR-double knockout mice. J Physiol Pharmacol 59:633-639
9. Kaetsu Y, Yamamoto Y, Sugihara S, Matsuura T, Igawa G, Matsubara K, Igawa O, Shigemasa C, Hisatome I (2007) Role of cysteinyl leukotrienes in the proliferation and the migration of murine vascular smooth muscle cells in vivo and in vitro. Cardiovasc Res 76:160-166. doi:10.1016/j.cardiores.2007.05.018
10. Bäck M, Dahlen SE, Drazen JM, Evans JF, Serhan CN, Shimizu T, Yokomizo T, Rovati GE (2011) International union of basic and clinical pharmacology. LXXXIV: leukotriene receptor nomenclature, distribution, and pathophysiological functions. Pharmacol Rev 63:539-584. doi:10.1124/pr.110. 004184
11. Lotzer K, Spanbroek R, Hildner M, Urbach A, Heller R, Bretschneider E, Galczenski H, Evans JF, Habenicht AJ (2003) Differential leukotriene receptor expression and calcium responses in endothelial cells and macrophages indicate 5-lipoxygenasedependent circuits of inflammation and atherogenesis. Arterioscler Thromb Vasc Biol 23:e32-e36. doi:10.1161/01. ATV. 0000082690.23131. CB
12. Ingelsson E, Yin L, Bäck M (2012) Nationwide cohort study of the leukotriene receptor antagonist montelukast and incident or recurrent cardiovascular disease. J Allergy Clin Immunol. doi:10.1016/j.jaci.2011.11.052
13. Bäck M (2002) Functional characteristics of cysteinyl-leukotriene receptor subtypes. Life Sci 71:611-622
14. Allen SP, Dashwood MR, Chester AH, Tadjkarimi S, Collins M, Piper PJ, Yacoub MH (1993) Influence of atherosclerosis on the vascular reactivity of isolated human epicardial coronary arteries to leukotriene C4. Cardioscience 4:47-54
15. Allen S, Dashwood M, Morrison K, Yacoub M (1998) Differential leukotriene constrictor responses in human atherosclerotic coronary arteries. Circulation 97:2406-2413
16. Kamohara M, Takasaki J, Matsumoto M, Matsumoto S, Saito T, Soga T, Matsushime H, Furuichi K (2001) Functional characterization of cysteinyl leukotriene CysLT (2) receptor on human coronary artery smooth muscle cells. Biochem Biophys Res Commun 287:1088-1092
17. Bäck M, Bu DX, Branström R, Sheikine Y, Yan ZQ, Hansson GK (2005) Leukotriene B4 signaling through NF-kappaB-dependent BLT1 receptors on vascular smooth muscle cells in atherosclerosis and intimal hyperplasia. Proc Natl Acad Sci U S A 102:17501-17506
18. Tavi P, Hansson A, Zhang SJ, Larsson NG, Westerblad H (2005) Abnormal Ca (2+) release and catecholamine-induced arrhythmias in mitochondrial cardiomyopathy. Hum Mol Genet 14:1069-1076. doi:10.1093/hmg/ddi119
19. Gronert K, Martinsson-Niskanen T, Ravasi S, Chiang N, Serhan CN (2001) Selectivity of recombinant human leukotriene D (4), leukotriene B (4), and lipoxin A (4) receptors with aspirintriggered 15-epi-LXA (4) and regulation of vascular and inflammatory responses. Am J Pathol 158:3-9. doi:10.1016/S0002-9440 (10) 63937-5
20. Mechiche H, Candenas L, Pinto FM, Nazeyrollas P, Clément C, 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
21. Palmberg L, Claesson HE, Thyberg J (1989) Effects of leukotrienes on phenotypic properties and growth of arterial smooth muscle cells in primary culture. J Cell Sci 93(Pt 3):403-408
22. Bkaily G, Choufani S, Hassan G, El-Bizri N, Jacques D, D'Orleans-Juste P (2000) Presence of functional endothelin-1 receptors in nuclear membranes of human aortic vascular smooth muscle cells. J Cardiovasc Pharmacol 36:S414-S417
23. Bkaily G, Sleiman S, Stephan J, Asselin C, Choufani S, Kamal M, Jacques D, Gobeil F Jr, D'Orleans-Juste P (2003) Angiotensin II AT1 receptor internalization, translocation and de novo synthesis modulate cytosolic and nuclear calcium in human vascular smooth muscle cells. Can J Physiol Pharmacol 81:274-287
24. Haller H, Lindschau C, Erdmann B, Quass P, Luft FC (1996) Effects of intracellular angiotensin II in vascular smooth muscle cells. Circ Res 79:765-772
25. Nielsen CK, Campbell JI, Ohd JF, Morgelin M, Riesbeck K, Landberg G, Sjolander A (2005) A novel localization of the Gproteincoupled CysLT1 receptor in the nucleus of colorectal adenocarcinoma cells. Cancer Res 65:732-742
26. Jiang Y, Borrelli LA, Kanaoka Y, Bacskai BJ, Boyce JA (2007) CysLT2 receptors interact with CysLT1 receptors and downmodulate cysteinyl leukotriene dependentmitogenic responses ofmast cells. Blood 110:3263-3270. doi:10.1182/blood-2007-07-100453
27. Hardingham GE, Bading H (1998) Nuclear calcium: a key regulator of gene expression. Biometals 11:345-358
28. Dichtl W, Stiko A, Eriksson P, Goncalves I, Calara F, Banfi C, Ares MP, Hamsten A, Nilsson J (1999) Oxidized LDL and lysophosphatidylcholine stimulate plasminogen activator inhibitor-1 expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 19:3025-3032
29. Tyson KL, Weissberg PL, Shanahan CM (2002) Heterogeneity of gene expression in human atheroma unmasked using cDNA representational difference analysis. Physiol Genomics 9:121-130. doi:10.1152/physiolgenomics.00116.2001
30. Beauchamp NJ, van Achterberg TA, Engelse MA, Pannekoek H, de Vries CJ (2003) Gene expression profiling of resting and activated vascular smooth muscle cells by serial analysis of gene expression and clustering analysis. Genomics 82:288-299
31. Schroder WA, Le TT, Major L, Street S, Gardner J, Lambley E, Markey K, MacDonald KP, Fish RJ, Thomas R et al (2010) A physiological function of inflammation-associated SerpinB2 is regulation of adaptive immunity. J Immunol 184:2663-2670. doi:10.4049/jimmunol.0902187
32. Feener EP, Northrup JM, Aiello LP, King GL (1995) Angiotensin II induces plasminogen activator inhibitor-1 and -2 expression in vascular endothelial and smooth muscle cells. J Clin Invest 95:1353-1362. doi:10.1172/JCI117786
33. Haller H, Lindschau C, Quass P, Distler A, Luft FC (1994) Nuclear calcium signaling is initiated by cytosolic calcium surges in vascular smooth muscle cells. Kidney Int 46:1653-1662
34. Park JM, Greten FR, Wong A, Westrick RJ, Arthur JS, Otsu K, Hoffmann A, Montminy M, Karin M (2005) Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis-CREB and NF-kappaB as key regulators. Immunity 23:319-329. doi:10.1016/j.immuni.2005.08.010