Nuclear receptor nurr1 is expressed in and is associated with human restenosis and inhibits vascular lesion formation in mice involving inhibition of smooth muscle cell proliferation and inflammation

Circulation

Volumn 121, Issue 18, 2010, Pages 2023-2032

  Bonta, Peter I ^a   Pols, Thijs W H ^a   Van Tiel, Claudia M ^a   Vos, Mariska ^a   Arkenbout, E Karin ^a   Rohlena, Jakub ^a   Koch, Karel T ^a   De Maat, Moniek P M ^c   Tanck, Michael W T ^b   De Winter, Robbert J ^a   Pannekoek, Hans ^a   Biessen, Erik A L ^d   Bot, Ilze ^e   De Vries, Carlie J M ^a  

^a Clinical Epidemiology Biostatistics ^*  (Australia)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^e LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Inflammation; Muscle; Nuclear receptors; Nurr1 nuclear receptor; Restenosis; Smooth

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NUCLEAR RECEPTOR RELATED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAROTID ARTERY; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; CORONARY ARTERY BYPASS GRAFT; FEMALE; HAPLOTYPE; HEART INFARCTION; HUMAN; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; INFLAMMATION; LENTIVIRINAE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERCUTANEOUS CORONARY INTERVENTION; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; RESTENOSIS; SMOOTH MUSCLE FIBER; STENT;

ANGIOPLASTY, TRANSLUMINAL, PERCUTANEOUS CORONARY; ANIMALS; APOLIPOPROTEINS E; CELL DIVISION; CELLS, CULTURED; CORONARY ARTERY DISEASE; CORONARY RESTENOSIS; CORONARY VESSELS; DISEASE MODELS, ANIMAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MICE; MICE, MUTANT STRAINS; MUSCLE, SMOOTH, VASCULAR; NEOVASCULARIZATION, PHYSIOLOGIC; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; RISK FACTORS; STENTS; VASCULITIS;

EID: 77952240075     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.109.885673     Document Type: Article

References (37)

1. Serruys PW, Kutryk MJ, Ong AT. Coronary-artery stents. N Engl J Med. 2006;354:483-495.
2. Kastrati A, Dirschinger J, Schomig A. Genetic risk factors and restenosis after percutaneous coronary interventions. Herz. 2000;25:34-46.
3. Welt FG, Rogers C. Inflammation and restenosis in the stent era. Arte-rioscler Thromb Vasc Biol. 2002;22:1769-1776.
4. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation. 2005;111:2257-2273.
5. Stone GW, Moses JW, Ellis SG, Schofer J, Dawkins KD, Morice MC, Colombo A, Schampaert E, Grube E, Kirtane AJ, Cutlip DE, Fahy M, Pocock SJ, Mehran R, Leon MB. Safety and efficacy of sirolimus-and paclitaxel-eluting coronary stents. N Engl J Med. 2007;356:998-1008.
6. Farb A, Boam AB. Stent thrombosis redux: the FDA perspective. N Engl J Med. 2007;356:984-987.
7. Luscher TF, Steffel J, Eberli FR, Joner M, Nakazawa G, Tanner FC, Virmani R. Drug-eluting stent and coronary thrombosis: biological mechanisms and clinical implications. Circulation. 2007;115:1051-1058
8. Nuclear Receptor Nomenclature Committee. A unified nomenclature system for the nuclear receptor superfamily. Cell. 1999;97:161-163.
9. Philips A, Lesage S, Gingras R, Maira MH, Gauthier Y, Hugo P, Drouin J. Novel dimeric Nur77 signaling mechanism in endocrine and lymphoid cells. Mol Cell Biol. 1997;17:5946-5951.
10. Wallen-Mackenzie A, Mata de Urquiza A, Petersson S, Rodriguez FJ, Friling S, Wagner J, Ordentlich P, Lengqvist J, Heyman RA, Arenas E, Perlmann T. Nurr1-RXR heterodimers mediate RXR ligand-induced signaling in neuronal cells. Genes Dev. 2003;17:3036-3047.
11. Mix KS, Attur MG, Al-Mussawir H, Abramson SB, Brinckerhoff CE, Murphy EP. Transcriptional repression of matrix metalloproteinase gene expression by the orphan nuclear receptor NURR1 in cartilage. J Biol Chem. 2007;282:9492-9504.
12. Saijo K, Winner B, Carson CT, Collier JG, Boyer L, Rosenfeld MG, Gage FH, Glass CK. A Nurr1/CoREST pathway in microglia and astrocytes protects dopaminergic neurons from inflammation-induced death. Cell. 2009;137:47-59.
13. Zetterstrom RH, Solomin L, Jansson L, Hoffer BJ, Olson L, Perlmann T. Dopamine neuron agenesis in Nurr1-deficient mice. Science. 1997;276: 248-250.
14. Chu Y, Le W, Kompoliti K, Jankovic J, Mufson EJ, Kordower JH. Nurr1 in Parkinson's disease and related disorders. J Comp Neurol. 2006;494: 495-514.
15. Bonta PI, van Tiel CM, Vos M, van Thienen JV, Ferreira V, Arkenbout EK, Seppen J, Spek CA, van der Poll T, Pannekoek H, de Vries CJ. Nuclear receptors Nur77, Nurr1, and NOR-1 expressed in atherosclerotic lesion macrophages reduce lipid loading and inflammatory responses. Arterioscler Thromb Vasc Biol. 2006;26:2288-2294.
16. McEvoy AN, Murphy EA, Ponnio T, Conneely OM, Bresnihan B, FitzGerald O, Murphy EP. Activation of nuclear orphan receptor NURR1 transcription by NF-kappa B and cyclic adenosine 5'-monophosphate response element-binding protein in rheumatoid arthritis synovial tissue. J Immunol. 2002;168:2979-2987.
17. Rittersma SZ, de Winter RJ, Koch KT, Schotborgh CE, Bax M, Heyde GS, van Straalen JP, Mulder KJ, Tijssen JG, Sanders GT, Piek JJ. Preprocedural C-reactive protein is not associated with angiographic restenosis or target lesion revascularization after coronary artery stent placement. Clin Chem. 2004;50:1589-1596.
18. Kardys I, van Tiel CM, de Vries CJ, Pannekoek H, Uitterlinden AG, Hofman A, Witteman JC, de Maat MP. Haplotypes of the NR4A2/NURR1 gene and cardiovascular disease: the Rotterdam Study. Hum Mutat. 2009;30:417-423.
19. Souverein OW, Zwinderman AH, Tanck MW. Estimating haplotype effects on dichotomous outcome for unphased genotype data using a weighted penalized log-likelihood approach. Hum Hered. 2006;61: 104-110.
20. Arkenbout EK, de Waard V, van Bragt M, van Achterberg TA, Grim-bergen JM, Pichon B, Pannekoek H, de Vries CJ. Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation. 2002;106:1530-1535.
21. Krohn R, Raffetseder U, Bot I, Zernecke A, Shagdarsuren E, Liehn EA, van Santbrink PJ, Nelson PJ, Biessen EA, Mertens PR, Weber C. Y-box binding protein-1 controls CC chemokine ligand-5 (CCL5) expression in smooth muscle cells and contributes to neointima formation in atherosclerosis-prone mice. Circulation. 2007;116:1812-1820.
22. Schober A, Zernecke A, Liehn EA, von HP, Knarren S, Kuziel WA, Weber C. Crucial role of the CCL2/CCR2 axis in neointimal hyperplasia after arterial injury in hyperlipidemic mice involves early monocyte recruitment and CCL2 presentation on platelets. Circ Res. 2004;95: 1125-1133.
23. von der Thusen JH, Fekkes ML, Passier R, van Zonneveld AJ, Mainfroid V, van Berkel TJ, Biessen EA. Adenoviral transfer of endothelial nitric oxide synthase attenuates lesion formation in a novel murine model of postangioplasty restenosis. Arterioscler Thromb Vasc Biol. 2004;24: 357-362.
24. Komatsu R, Ueda M, Naruko T, Kojima A, Becker AE. Neointimal tissue response at sites of coronary stenting in humans: macroscopic, histolog-ical, and immunohistochemical analyses. Circulation. 1998;98:224-233.
25. Boehm M, Nabel EG. The cell cycle and cardiovascular diseases. Prog Cell Cycle Res. 2003;5:19-30.
26. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519.
27. Weber C, Schober A, Zernecke A. Chemokines: key regulators of mono-nuclear cell recruitment in atherosclerotic vascular disease. Arterioscler Thromb Vasc Biol. 2004;24:1997-2008.
28. Diatchenko L, Romanov S, Malinina I, Clarke J, Tchivilev I, Li X, Makarov SS. Identification of novel mediators of NF-kappaB through genome-wide survey of monocyte adherence-induced genes. J Leukoc Biol. 2005;78:1366-1377.
29. Castro DS, Hermanson E, Joseph B, Wallen A, Aarnisalo P, Heller A, Perlmann T. Induction of cell cycle arrest and morphological differentiation by Nurr1 and retinoids in dopamine MN9D cells. J Biol Chem. 2001;276:43277-43284.
30. Tanner FC, Yang ZY, Duckers E, Gordon D, Nabel GJ, Nabel EG. Expression of cyclin-dependent kinase inhibitors in vascular disease. Circ Res. 1998;82:396-403.
31. Volakakis N, Malewicz M, Kadkhodai B, Perlmann T, Benoit G. Characterization of the Nurr1 ligand-binding domain co-activator interaction surface. J Mol Endocrinol. 2006;37:317-326.
32. Wang Z, Benoit G, Liu J, Prasad S, Aarnisalo P, Liu X, Xu H, Walker NP, Perlmann T. Structure and function of Nurr1 identifies a class of ligand-independent nuclear receptors. Nature. 2003;423:555-560.
33. Dubois C, Hengerer B, Mattes H. Identification of a potent agonist of the orphan nuclear receptor Nurr1. ChemMedChem. 2006;1:955-958.
34. Ordentlich P, Yan Y, Zhou S, Heyman RA. Identification of the antineo-plastic agent 6-mercaptopurine as an activator of the orphan nuclear hormone receptor Nurr1. J Biol Chem. 2003;278:24791-24799.
35. Wansa KD, Harris JM, Yan G, Ordentlich P, Muscat GE. The AF-1 domain of the orphan nuclear receptor NOR-1 mediates trans-activation, coactivator recruitment, and activation by the purine anti-metabolite 6-mercaptopurine. J Biol Chem. 2003;278:24776-24790.
36. Hintermann S, Chiesi M, von KU, Mathe D, Felber R, Hengerer B. Identification of a series of highly potent activators of the Nurr1 signaling pathway. Bioorg Med Chem Lett. 2007;17:193-196.
37. Morita K, Kawana K, Sodeyama M, Shimomura I, Kagechika H, Makishima M. Selective allosteric ligand activation of the retinoid X receptor het-erodimers of NGFI-B and Nurr1. Biochem Pharmacol. 2005;71:98-107.