Ligand dissociation from estrogen receptor is mediated by receptor dimerization: Evidence from molecular dynamics simulations

Molecular Endocrinology

Volumn 22, Issue 7, 2008, Pages 1565-1578

  Sonoda, Milton T ^a   Martínez, Leandro ^b   Webb, Paul ^c   Skaf, Munir S ^b   Polikarpov, Igor ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR; RALOXIFENE;

ARTICLE; COMPUTER SYSTEM; DIMERIZATION; DISSOCIATION; HORMONE RECEPTOR INTERACTION; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE;

CELL NUCLEUS; COMPUTER SIMULATION; DIMERIZATION; HUMANS; KINETICS; LIGANDS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RALOXIFENE; RECEPTORS, ESTROGEN; SOFTWARE;

EID: 46349088224     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0501     Document Type: Article

References (54)

1. Aranda A, Pascual A 2001 Nuclear hormone receptors and gene expression. Physiol Rev 81:1269-1304
2. Jordan VC 2003 Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 1. Receptor interactions. J Med Chem 46:883-908
3. Jordan VC 2003 Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 2. Clinical considerations and new agents. J Med Chem 46:1081-1111
4. Nilsson S, Gustafsson JA 2000 Estrogen receptor transcription and transactivation: basic aspects of estrogen action. Breast Cancer Res 2:360-366
5. Nilsson S, Koehler KF 2005 Oestrogen receptors and selective oestrogen receptor modulators: molecular and cellular pharmacology. Basic Clin Pharm Toxicol 96:15-25
6. Muramatsu M, Inoue S 2000 Estrogen receptors: how do they control reproductive and nonreproductive functions? Biochem Biophys Res Commun 270:1-10
7. Gee AC, Katzenellenbogen JA 2001 Probing conformational changes in the estrogen receptor: evidence for a partially unfolded intermediate facilitating ligand binding and release. Mol Endocrinol 15:421-428
8. Tamrazi A, Carlson KE, Katzenellenbogen JA 2003 Molecular sensors of estrogen receptor conformations and dynamics. Mol Endocrinol 17:2593-2602
9. Gronemeyer H, Gustafsson JA, Laudet V 2004 Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discovery 3:950-964
10. Nettles KW, Greene GL 2005 Ligand control of coregulator recruitment to nuclear receptors. Annu Rev Physiol 67:309-333
11. Moras D, Gronemeyer H 1998 The nuclear receptor ligand-binding domain: structure and function. Curr Opin Cell Biol 10:384-391
12. Nolte RT, Wisely GB, Westin S, Cobb JE, Lambert MH, Kurokawa R, Rosenfeld MG, Willson TM, Glass CK, Milburn MV 1998 Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-γ. Nature 395:137-143
13. Wang L, Zuercher WJ, Consler TG, Lambert MH, Miller AB, Orband-Miller LA, McKee DD, Willson TM, Nolte RT 2006 X-ray crystal structures of the estrogen-related receptor-γ ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J Biol Chem 281:37773-37781
14. Kallen J, Schlaeppi JM, Bitsch F, Filipuzzi I, Schilb A, Riou V, Graham A, Strauss A, Geiser M, Fournier B 2004 Evidence for ligand-independent transcriptional activation of the human estrogen-related receptor α (ERR α) - Crystal structure of ERR α ligand binding domain in complex with peroxisome proliferator-activated receptor coactivator-1 α. J Biol Chem 279:49330-49337
15. Flaig R, Greschik H, Peluso-Iltis C, Moras D 2005 Structural basis for the cell-specific activities of the NGFI-B and the Nurr1 ligand-binding domain. J Biol Chem 280:19250-19258
16. Baker KD, Shewchuk LM, Kozlova T, Makishima M, Hassell A, Wisely B, Caravella JA, Lambert MH, Reinking JL, Krause H, Thummel CS, Willson TM, Mangelsdorf DJ 2003 The Drosophila orphan nuclear receptor DHR38 mediates an atypical ecdysteroid signaling pathway. Cell 113:731-742
17. Wagner RL, Apriletti JW, Mcgrath ME, West BL, Baxter JD, Fletterick RJ 1995 A structural role for hormone in the thyroid-hormone receptor. Nature 378:690-697
18. Blondel A, Renaud JP, Fischer S, Moras D, Karplus M 1999 Retinoic acid receptor: a simulation analysis of retinoic acid binding and the resulting conformational changes. J Mol Biol 291:101-115
19. Kosztin D, Izrailev S, Schulten K 1999 Unbinding of retinoic acid from its receptor studied by steered molecular dynamics. Biophys J 76:188-197
20. Carlsson P, Burendahl S, Nilsson L 2006 Unbinding of retinoic acid from the retinoic acid receptor by random expulsion molecular dynamics. Biophys J 91:3151-3161
21. Martinez L, Sonoda MT, Webb P, Baxter JD, Skaf MS, Polikarpov I 2005 Molecular dynamics simulations reveal multiple pathways of ligand dissociation from thyroid hormone receptors. Biophys J 89:2011-2023
22. Martinez L, Webb P, Polikarpov I, Skaf MS 2006 Molecular dynamics simulations of ligand dissociation from thyroid hormone receptors: evidence of the likeliest escape pathway and its implications for the design of novel ligands. J Med Chem 49:23-26
23. Tamrazi A, Carlson KE, Rodriguez AL, Katzenellenbogen JA 2005 Coactivator proteins as determinants of estrogen receptor structure and function: spectroscopic evidence for a novel coactivator-stabilized receptor conformation. Mol Endocrinol 19:1516-1528
24. Ribeiro RCJ, Feng WJ, Wagner RL, Costa CHRM, Pereira AC, Apriletti JW, Fletterick RJ, Baxter JD 2001 Definition of the surface in the thyroid hormone receptor ligand binding domain for association as homodimers and heterodimers with retinoid X receptor. J Biol Chem 276:14987-14995
25. Zhong L, Skafar DF 2002 Mutations of tyrosine 537 in the human estrogen receptor-α selectively alter the receptor's affinity for estradiol and the kinetics of the interaction. Biochemistry 41:4209-4217
26. Weichman BM, Notides AC 1977 Estradiol-binding kinetics of activated and non-activated estrogen-receptor. J Biol Chem 252:8856-8862
27. Tamrazi A, Carlson KE, Daniels JR, Hurth KM, Katzenellenbogen JA 2002 Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Mol Endocrinol 16:2706-2719
28. Gee AC, Carlson KE, Martini PGV, Katzenellenbogen BS, Katzenellenbogen JA 1999 Coactivator peptides have a differential stabilizing effect on the binding of estrogens and antiestrogens with the estrogen receptor. Mol Endocrinol 13:1912-1923
29. Carlson KE, Choi I, Gee A, Katzenellenbogen BS, Katzenellenbogen JA 1997 Altered ligand binding properties and enhanced stability of a constitutively active estrogen receptor: evidence that an open pocket conformation is required for ligand interaction. Biochemistry 36:14897-14905
30. Ekena K, Weis KE, Katzenellenbogen JA, Katzenellenbogen BS 1996 Identification of amino acids in the hormone binding domain of the human estrogen receptor important in estrogen binding. J Biol Chem 271:20053-20059
31. Kubli-Garfias C 1998 Comparative study of the electronic structure of estradiol, epiestradiol and estrone by ab initio theory. Theochem J Mol Struct 452:175-183
32. Skafar DF, Koide S 2006 Understanding the human estrogen receptor-α using targeted mutagenesis. Mol Cell Endocrinol 246:83-90
33. Bledsoe RK, Madauss KP, Holt JA, Apolito CJ, Lambert MH, Pearce KH, Stanley TB, Stewart EL, Trump RP, Willson TM, Williams SP 2005 A ligand-mediated hydrogen bond network required for the activation of the mineralocorticoid receptor. J Biol Chem 280:31283-31293
34. Sack JS, Kish KF, Wang CH, Attar RM, Kiefer SE, An YM, Wu GY, Scheffler JE, Salvati ME, Krystek SR, Weinmann R, Einspahr HM 2001 Crystallographic structures of the ligand-binding domains of the androgen receptor and its T877A mutant complexed with the natural agonist dihydrotestosterone. Proc Natl Acad Sci USA 98:4904-4909
35. Kauppi B, Jakob C, Farnegardh M, Yang J, Ahola H, Alarcon M, Calles K, Engstrom O, Harlan J, Muchmore S, Ramqvist AK, Thorell S, Ohman L, Greer J, Gustafsson JA, Carlstedt-Duke J, Carlquist M 2003 The three-dimensional structures of antagonistic and agonistic forms of the glucocorticoid receptor ligand-binding domain: RU-486 induces a transconformation that leads to active antagonism. J Biol Chem 278:22748-22754
36. Williams SP, Sigler PB 1998 Atomic structure of progesterone complexed with its receptor. Nature 393:392-396
37. Koide A, Zhao CQ, Naganuma M, Abrams J, Deighton-Collins S, Skafar DF, Koide S 2007 Identification of regions within the F domain of the human estrogen receptor α that are important for modulating transactivation and protein-protein interactions. Mol Endocrinol 21:829-842
38. Montano MM, Muller V, Trobaugh A, Katzenellenbogen BS 1995 The carboxy-terminal F-domain of the human estrogen-receptor: role in the transcriptional activity of the receptor and the effectiveness of antiestrogens as estrogen antagonists. Mol Endocrinol 9:814-825
39. Peters GA, Khan SA 1999 Estrogen receptor domains E and F: role in dimerization and interaction with coactivator RIP-140. Mol Endocrinol 13:286-296
40. Elber R, Karplus M 1990 Enhanced sampling in molecular-dynamics - use of the time-dependent Hartree approximation for a simulation of carbon-monoxide diffusion through myoglobin. J Am Chem Soc 112:9161-9175
41. Ulitsky A, Elber R 1993 The thermal-equilibrium aspects of the time-dependent Hartree and the locally enhanced sampling approximations - formal properties, a correction, and computational examples for rare-gas clusters. J Chem Phys 98:3380-3388
42. Straub JE, Karplus M 1991 Energy equipartitioning in the classical time-dependent Hartree approximation. J Chem Phys 94:6737-6739
43. Ulitsky A, Elber R 1994 Application of the locally enhanced sampling (LES) and a mean-field with a binary collision correction (Cles) to the simulation of Ar diffusion and no recombination in myoglobin. J Phys Chem 98:1034-1043
44. Gibson QH, Regan R, Elber R, Olson JS, Carver TE 1992 Distal pocket residues affect picosecond ligand recombination in myoglobin - an experimental and molecular-dynamics study of position 29 mutants. J Biol Chem 267:22022-22034
45. Scott EE, Gibson QH, Olson JS 2001 Mapping the pathways for O-2 entry into and exit from myoglobin. J Biol Chem 276:5177-5188
46. Brunori M, Gibson QH 2001 Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep 2:674-679
47. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL 2001 Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J Phys Chem B 105:6474-6487
48. Jorgensen WL, Maxwell DS, TiradoRives J 1996 Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225-11236
49. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery Jr JA, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, et al. 2004 Gaussian 03, revision C.02, Gaussian, Inc., Wallingford CT
50. Ponder JW 2004 TINKER Software Tools for Molecular Design, version 4.2
51. Sali A, Blundell TL 1993 Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234:779-815
52. Liu DC, Nocedal J 1989 On the limited memory Bfgs method for large-scale optimization. Math Program 45:503-528
53. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K 2005 Scalable molecular dynamics with NAMD. J Comput Chem 26:1781-1802
54. Sonoda MT, Moreira NH, Martinez L, Favero FW, Vechi SM, Martins LR, Skaf MS 2004 A review on the dynamics of water. Braz J Physics 34:3-16