The activation function-1 of estrogen receptor alpha prevents arterial neointima development through a direct effect on smooth muscle cells

Circulation Research

Volumn 117, Issue 9, 2015, Pages 770-777

  Smirnova, Natalia F ^a   Fontaine, Coralie ^a   Buscato, Mélissa ^a   Lupieri, Adrien ^a   Vinel, Alexia ^a   Valera, Marie Cécile ^a   Guillaume, Maeva ^a   Malet, Nicole ^a   Foidart, Jean Michel ^b   Raymond Letron, Isabelle ^c   Lenfant, Francoise ^a   Gourdy, Pierre ^a   Katzenellenbogen, Benita S ^d   Katzenellenbogen, John A ^d   Laffargue, Muriel ^a   Arnal, Jean Francois ^a  

^a Université de Toulouse   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

estradiol; estrogen receptor alpha; mice; myocytes; smooth muscle

Indexed keywords

ANGIOGENESIS INHIBITOR; CONJUGATED ESTROGEN DERIVATIVE; ESTETROL; ESTRADIOL; ESTROGEN DENDRIMER CONJUGATE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA ACTIVATION FUNCTION 1; PLACEBO; SELECTIVE ESTROGEN RECEPTOR MODULATOR; TAMOXIFEN; UNCLASSIFIED DRUG; VASCULAR TARGETING AGENT; ACTIN; CD31 ANTIGEN; ESTROGEN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTERY INTIMA PROLIFERATION; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG TARGETING; EXPERIMENTAL ARTERY INJURY; FEMALE; FEMORAL ARTERY; HEMATOPOIETIC CELL; MOLECULAR PATHOLOGY; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; ARTERY; C57BL MOUSE; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; DRUG EFFECTS; GENETICS; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; INJURIES; INTIMA; KNOCKOUT MOUSE; METABOLISM; OVARIECTOMY; PATHOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ACTINS; ANIMALS; ANTIGENS, CD31; ARTERIES; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; ENDOTHELIUM, VASCULAR; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMORAL ARTERY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; OVARIECTOMY; TUNICA INTIMA;

EID: 84943643272     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.306416     Document Type: Article

References (41)

1. Hui DY, Intimal hyperplasia in murine models. Curr Drug Targets 2008 9 251 260
2. Smirnova NF, Gayral S, Pedros C, Loirand G, Vaillant N, Malet N, Kassem S, Calise D, Goudounèche D, Wymann MP, Hirsch E, Gadeau AP, Martinez LO, Saoudi A, Laffargue M, Targeting PI3Kγ activity decreases vascular trauma-induced intimal hyperplasia through modulation of the Th1 response. J Exp Med 2014 211 1779 1792. doi: 10.1084/jem.20131276
3. Costa MA, Simon DI, Molecular basis of restenosis and drug-eluting stents. Circulation 2005 111 2257 2273. doi: 10.1161/01.CIR.0000163587.36485.A7
4. Chandrasekar B, Sirois MG, Geoffroy P, Lauzier D, Nattel S, Tanguay JF, Local delivery of 17beta-estradiol improves reendothelialization and decreases inflammation after coronary stenting in a porcine model. Thromb Haemost 2005 94 1042 1047. doi: 10.1160/TH04-12-0823
5. Chandrasekar B, Tanguay JF, Local delivery of 17-beta-estradiol decreases neointimal hyperplasia after coronary angioplasty in a porcine model. J Am Coll Cardiol 2000 36 1972 1978
6. Ishibahshi T, Obayashi S, Sakamoto S, Aso T, Ishizaka M, Azuma H, Estrogen replacement effectively improves the accelerated intimal hyperplasia following balloon injury of carotid artery in the ovariectomized rats. J Cardiovasc Pharmacol 2006 47 37 45
7. Selzman CH, Gaynor JS, Turner AS, Johnson SM, Horwitz LD, Whitehill TA, Harken AH, Ovarian ablation alone promotes aortic intimal hyperplasia and accumulation of fibroblast growth factor. Circulation 1998 98 2049 2054
8. Brouchet L, Krust A, Dupont S, Chambon P, Bayard F, Arnal JF, Estradiol accelerates reendothelialization in mouse carotid artery through estrogen receptor-alpha but not estrogen receptor-beta. Circulation 2001 103 423 428. doi: 10.1161/01.CIR.103.3.423
9. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M, Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000 127 4277 4291
10. Pare G, Krust A, Karas RH, Dupont S, Aronovitz M, Chambon P, Mendelsohn ME, Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ Res 2002 90 1087 1092. doi: 10.1161/01.RES.0000021114.92282.FA
11. Toutain CE, Filipe C, Billon A, Fontaine C, Brouchet L, Guéry JC, Gourdy P, Arnal JF, Lenfant F, Estrogen receptor alpha expression in both endothelium and hematopoietic cells is required for the accelerative effect of estradiol on reendothelialization. Arterioscler Thromb Vasc Biol 2009 29 1543 1550. doi: 10.1161/ATVBAHA.109.192849
12. Stender JD, Kim K, Charn TH, Komm B, Chang KC, Kraus WL, Benner C, Glass CK, Katzenellenbogen BS, Genome-wide analysis of estrogen receptor alpha DNA binding and tethering mechanisms identifies Runx1 as a novel tethering factor in receptor-mediated transcriptional activation. Mol Cell Biol 2010 30 3943 3955. doi: 10.1128/MCB.00118-10
13. Smith CL, O'Malley BW, Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 2004 25 45 71. doi: 10.1210/er.2003-0023
14. Feng Q, O'Malley BW, Nuclear receptor modulation-role of coregulators in selective estrogen receptor modulator (SERM) actions. Steroids 2014 90 39 43. doi: 10.1016/j.steroids.2014.06.008
15. Abot A, Fontaine C, Raymond-Letron I, Flouriot G, Adlanmerini M, Buscato M, Otto C, Bergès H, Laurell H, Gourdy P, Lenfant F, Arnal JF, The AF-1 activation function of estrogen receptor is necessary and sufficient for uterine epithelial cell proliferation in vivo. Endocrinology 2013 154 2222 2233. doi: 10.1210/en.2012-2059
16. Billon-Galés A, Fontaine C, Filipe C, Douin-Echinard V, Fouque MJ, Flouriot G, Gourdy P, Lenfant F, Laurell H, Krust A, Chambon P, Arnal JF, The transactivating function 1 of estrogen receptor alpha is dispensable for the vasculoprotective actions of 17beta-estradiol. Proc Natl Acad Sci U S A 2009 106 2053 2058. doi: 10.1073/pnas.0808742106
17. Billon-Galés A, Krust A, Fontaine C, Abot A, Flouriot G, Toutain C, Berges H, Gadeau AP, Lenfant F, Gourdy P, Chambon P, Arnal JF, Activation function 2 (AF2) of estrogen receptor-alpha is required for the atheroprotective action of estradiol but not to accelerate endothelial healing. Proc Natl Acad Sci U S A 2011 108 13311 13316. doi: 10.1073/pnas.1105632108
18. Ueda K, Karas RH, Emerging evidence of the importance of rapid, non-nuclear estrogen receptor signaling in the cardiovascular system. Steroids 2013 78 589 596. doi: 10.1016/j.steroids.2012.12.006
19. Wu Q, Chambliss K, Umetani M, Mineo C, Shaul PW, Non-nuclear estrogen receptor signaling in the endothelium. J Biol Chem 2011 286 14737 14743. doi: 10.1074/jbc.R110.191791
20. Adlanmerini M, Solinhac R, Abot A, Mutation of the palmitoylation site of estrogen receptor in vivo reveals tissue-specific roles for membrane versus nuclear actions. Proc Natl Acad Sci U S A 2014 111 E283 E290. doi: 10.1073/pnas.1322057111
21. Chambliss KL, Wu Q, Oltmann S, Non-nuclear estrogen receptor alpha signaling promotes cardiovascular protection but not uterine or breast cancer growth in mice. J Clin Invest 2010 120 2319 2330. doi: 10.1172/JCI38291
22. Billon-Galés A, Fontaine C, Douin-Echinard V, Delpy L, Berges H, Calippe B, Lenfant F, Laurell H, Guéry JC, Gourdy P, Arnal JF, Endothelial estrogen receptor-alpha plays a crucial role in the atheroprotective action of 17beta-estradiol in low-density lipoprotein receptor-deficient mice. Circulation 2009 120 2567 2576. doi: 10.1161/CIRCULATIONAHA.109.898445
23. Wendling O, Bornert JM, Chambon P, Metzger D, Efficient temporally-controlled targeted mutagenesis in smooth muscle cells of the adult mouse. Genesis 2009 47 14 18. doi: 10.1002/dvg.20448
24. Abot A, Fontaine C, Buscato M, The uterine and vascular actions of estetrol delineate a distinctive profile of estrogen receptor modulation, uncoupling nuclear and membrane activation. EMBO Mol Med 2014 6 1328 1346. doi: 10.15252/emmm.201404112
25. Fontaine C, Abot A, Billon-Galés A, Flouriot G, Bergès H, Grunenwald E, Vinel A, Valera MC, Gourdy P, Arnal JF, Tamoxifen elicits atheroprotection through estrogen receptor AF-1 but does not accelerate reendothelialization. Am J Pathol 2013 183 304 312. doi: 10.1016/j.ajpath.2013.03.010
26. Deanfield JE, Halcox JP, Rabelink TJ, Endothelial function and dysfunction: testing and clinical relevance. Circulation 2007 115 1285 1295. doi: 10.1161/CIRCULATIONAHA.106.652859
27. Suzuki A, Mizuno K, Ino Y, Okada M, Kikkawa F, Mizutani S, Tomoda Y, Effects of 17 beta-estradiol and progesterone on growth-factor-induced proliferation and migration in human female aortic smooth muscle cells in vitro. Cardiovasc Res 1996 32 516 523
28. Geraldes P, Sirois MG, Tanguay JF, Specific contribution of estrogen receptors on mitogen-activated protein kinase pathways and vascular cell activation. Circ Res 2003 93 399 405. doi: 10.1161/01.RES.0000088640.18462.42
29. Hogg ME, Vavra AK, Banerjee MN, Martinez J, Jiang Q, Keefer LK, Chambon P, Kibbe MR, The role of estrogen receptor and β in regulating vascular smooth muscle cell proliferation is based on sex. J Surg Res 2012 173 e1 10. doi: 10.1016/j.jss.2011.09.021
30. Krom YD, Pires NM, Jukema JW, de Vries MR, Frants RR, Havekes LM, van Dijk KW, Quax PH, Inhibition of neointima formation by local delivery of estrogen receptor alpha and beta specific agonists. Cardiovasc Res 2007 73 217 226. doi: 10.1016/j.cardiores.2006.10.024
31. Karas RH, Hodgin JB, Kwoun M, Krege JH, Aronovitz M, Mackey W, Gustafsson JA, Korach KS, Smithies O, Mendelsohn ME, Estrogen inhibits the vascular injury response in estrogen receptor beta-deficient female mice. Proc Natl Acad Sci U S A 1999 96 15133 15136
32. Haas E, Bhattacharya I, Brailoiu E, Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res 2009 104 288 291. doi: 10.1161/CIRCRESAHA.108.190892
33. Antal MC, Krust A, Chambon P, Mark M, Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERbeta-null mutant. Proc Natl Acad Sci U S A 2008 105 2433 2438. doi: 10.1073/pnas.0712029105
34. Langer G, Bader B, Meoli L, Isensee J, Delbeck M, Noppinger PR, Otto C, A critical review of fundamental controversies in the field of GPR30 research. Steroids 2010 75 603 610. doi: 10.1016/j.steroids.2009.12.006
35. Bernelot Moens SJ, Schnitzler GR, Nickerson M, Guo H, Ueda K, Lu Q, Aronovitz MJ, Nickerson H, Baur WE, Hansen U, Iyer LK, Karas RH, Rapid estrogen receptor signaling is essential for the protective effects of estrogen against vascular injury. Circulation 2012 126 1993 2004. doi: 10.1161/CIRCULATIONAHA.112.124529
36. Iafrati MD, Karas RH, Aronovitz M, Kim S, Sullivan TR Jr, Lubahn DB, O'Donnell TF Jr, Korach KS, Mendelsohn ME, Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice. Nat Med 1997 3 545 548
37. Lindner V, Fingerle J, Reidy MA, Mouse model of arterial injury. Circ Res 1993 73 792 796. doi: 10.1161/01.RES.73.5.792
38. Reis ED, Roqué M, Cordon-Cardo C, Drobnjak M, Fuster V, Badimon JJ, Apoptosis, proliferation, and p27 expression during vessel wall healing: time course study in a mouse model of transluminal femoral artery injury. J Vasc Surg 2000 32 1022 1029. doi: 10.1067/mva.2000.109763
39. Roque M, Fallon JT, Badimon JJ, Zhang WX, Taubman MB, Reis ED, Mouse model of femoral artery denudation injury associated with the rapid accumulation of adhesion molecules on the luminal surface and recruitment of neutrophils. Arterioscler Thromb Vasc Biol 2000 20 335 342
40. Manka D, Forlow SB, Sanders JM, Hurwitz D, Bennett DK, Green SA, Ley K, Sarembock IJ, Critical role of platelet P-selectin in the response to arterial injury in apolipoprotein-E-deficient mice. Arterioscler Thromb Vasc Biol 2004 24 1124 1129. doi: 10.1161/01.ATV.0000127619.04687.f4
41. Murphy LC, Seekallu SV, Watson PH, Clinical significance of estrogen receptor phosphorylation. Endocr Relat Cancer 2011 18 R1 14. doi: 10.1677/ERC-10-0070