Identification of a new hormone-binding site on the surface of thyroid hormone receptor

Molecular Endocrinology

Volumn 28, Issue 4, 2014, Pages 534-545

  Souza, P C T ^a   Puhl, A C ^b   Martinez L ^a   Aparicio R ^a   Nascimento, A S ^b   Figueira, A C M ^c   Nguyen, P ^d   Webb, P ^b,e   Skaf, M S ^a   Polikarpov, Igor ^b  

^a UNIVERSITY OF CAMPINAS   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIOTHYRONINE; THYROID HORMONE RECEPTOR; THYROID HORMONE RECEPTOR ALPHA; THYROXINE; AMINO ACID; LIGAND; THYROID HORMONE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DISSOCIATION CONSTANT; ESCHERICHIA COLI; HORMONE BINDING; HUMAN; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; TRANSACTIVATION; TRANSACTIVATION ASSAY; X RAY CRYSTALLOGRAPHY; CELL LINE; CHEMISTRY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION;

AMINO ACIDS; BINDING SITES; CELL LINE; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIGANDS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, THYROID HORMONE; STRUCTURE-ACTIVITY RELATIONSHIP; THYROID HORMONES; TRANSCRIPTIONAL ACTIVATION;

EID: 84897940546     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1359     Document Type: Article

References (78)

1. Yen P. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001; 81: 1097-10142.
2. Ribeiro RC, Kushner PJ, Baxter JD. The nuclear hormone receptor gene superfamily. Annu Rev Med. 1995; 46: 443-453.
3. Lazar MA, Chin WW. Nuclear thyroid hormone receptors. J Clin Invest. 1990; 86: 1777-1782.
4. Wagner R, Huber B, Shiau A, et al. Hormone selectivity in thyroid hormone receptors. Mol Endocrinol. 2001; 15: 398-410.
5. Sandler B, Webb P, Apriletti J, et al. Thyroxine-thyroid hormone receptor interactions. J Biol Chem. 2004; 279: 55801-55808.
6. Blange I, Drvota V, Yen PM, Sylven C. Species differences in cardiac thyroid hormone receptor isoforms protein abundance. Biol Pharm Bull. 1997; 20: 1123-1126.
7. Schwartz HL, Strait KA, Ling NC, Oppenheimer JH. Quantitation of rat tissue thyroid hormone binding receptor isoforms by immunoprecipitation of nuclear triiodothyronine binding capacity. J Biol Chem. 1992; 267: 11794-11799.
8. Martínez L, Nascimento AS, Nunes FM, et al. Gaining ligand selectivity in thyroid hormone receptors via entropy. Proc Natl Acad Sci USA. 2009; 106: 20717-20722.
9. Bleicher L, Aparicio R, Nunes F, et al. Structural basis of GC-1 selectivity for thyroid hormone receptor isoforms. BMCStruct Biol. 2008; 8: 8.
10. Gauthier K, Chassande O, Plateroti M, et al. Different functions for the thyroid hormone receptors TRα and TRα in the control of thyroid hormone production and post-natal development. EMBO J. 1999; 18: 623-631.
11. Johansson C, Vennström B, Thorén P. Evidence that decreased heart rate in thyroid hormone receptor-α1-deficient mice is an intrinsic defect. Am J Physiol. 1998; 275: R640-R646.
12. Weatherman RV, Fletterick RJ, Scanlan TS. Nuclear-receptor ligands and ligand-binding domains. Annu Rev Biochem. 1999; 68: 559-5581.
13. Webb P, Nguyen NH, Chiellini G, et al. Design of thyroid hormone receptor antagonists from first principles. J Steroid Biochem Mol Biol. 2002; 83: 59-73.
14. Cunha Lima ST, Nguyen NH, Togashi M, et al. Differential effects of TR ligands on hormone dissociation rates: Evidence for multiple ligand entry/exit pathways. J Steroid Biochem Mol Biol. 2009; 117: 125-131.
15. Perakyla M. Ligand unbinding pathways from the vitamin D receptor studied by molecular dynamics simulations. Eur Biophys J. 2009; 38: 185-198.
16. Sonoda MT, Martínez L, Webb P, Skaf MS, Polikarpov I. Ligand dissociation from estrogen receptor is mediated by receptor dimerization: Evidence from molecular dynamics simulations. Mol Endocrinol. 2008; 22: 1565-1578.
17. Martínez L, Polikarpov I, Skaf MS. Only subtle protein conformational adaptations are required for ligand binding to thyroid hormone receptors: Simulations using a novel multipoint steered mo lecular dynamics approach. J Phys Chem B. 2008; 112: 10741-10751.
18. Genest D, Garnier N, Arrault A, Marot C, Morin-Allory L, Genest M. Ligand-escape pathways from the ligand-binding domain of PPARγ receptor as probed by molecular dynamics simulations. Eur Biophys J. 2008; 37: 369-379.
19. Carlsson P, Burendahl S, Nilsson L. Unbinding of retinoic acid from the retinoic acid receptor by random expulsion molecular dynamics. Biophys J. 2006; 91: 3151-3161.
20. Martínez L, Webb P, Polikarpov I, Skaf MS. 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. 2006; 49: 23-26.
21. Martínez L, Sonoda MT, Webb P, Baxter JD, Skaf MS, Polikarpov I. Molecular dynamics simulations reveal multiple pathways of ligand dissociation from thyroid hormone receptors. Biophys J. 2005; 89: 2011-2023.
22. Moras D, Gronemeyer H. The nuclear receptor ligand-binding domain: structure and function. Curr Opin Cell Biol. 1998; 10: 384-391.
23. Glass CK, Rosenfeld MG. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 2000; 14: 121-141.
24. Nichols M, Rientjes JM, Stewart AF. Different positioning of the ligand-binding domain helix 12 and the F domain of the estrogen receptor accounts for functional differences between agonists and antagonists. EMBO J. 1998; 17: 765-773.
25. Brzozowski AM, Pike AC, Dauter Z, et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature. 1997; 389: 753-758.
26. Figueira AC, Saidemberg DM, Souza PC, et al. Analysis of agonist and antagonist effects on thyroid hormone receptor conformation by hydrogen/deuterium exchange. Mol Endocrinol. 2011; 25: 15-31.
27. Wang Y, Chirgadze NY, Briggs SL, Khan S, Jensen EV, Burris TP. A second binding site for hydroxytamoxifen within the coactivatorbinding groove of estrogen receptor beta. Proc Natl Acad Sci U S A. 2006; 103: 9908-9911.
28. Hedden A, Müller V, Jensen E. A new interpretation of antiestrogen action. Ann NY Acad Sci. 1995; 761: 109-120.
29. Jensen EV, Khan SA. A two-site model for antiestrogen action. Mech Ageing Dev. 2004; 125: 679-682.
30. Estébanez-Perpiñá E, Arnold LA, Nguyen P, et al. A surface on the androgen receptor that allosterically regulates coactivator binding. Proc Natl Acad Sci USA. 2007; 104: 16074-16079.
31. Lack NA, Axerio-Cilies P, Tavassoli P, et al. Targeting the binding function 3 (BF3) site of the human androgen receptor through virtual screening. J Med Chem. 2011; 54: 8563-8573.
32. Munuganti RS, Leblanc E, Axerio-Cilies P, et al. Targeting the binding function 3 (BF3) site of the androgen receptor through virtual screening. 2. Development of 2-(2-phenoxyethyl) thio)-1Hbenzimidazole derivatives. J Med Chem. 2013; 56: 1136-1148.
33. Mizwicki MT, Keidel D, Bula CM, et al. Identification of an alternative ligand-binding pocket in the nuclear vitamin D receptor and its functional importance in 1alpha, 25(OH)2-vitamin D3 signaling. Proc Natl Acad Sci U S A. 2004; 101: 12876-12881.
34. Bernardes A, Souza PC, Muniz JR, et al. Molecular mechanism of peroxisome proliferator-activated receptor α activation by WY14643: a new mode of ligand recognition and receptor stabilization. J Mol Biol. 2013; 425: 2878-2893.
35. Puhl AC, Bernardes A, Silveira RL, et al. Mode of peroxisome proliferator-activated receptor γ activation by luteolin. Mol Pharmacol. 2012; 81: 788-799.
36. Liberato MV, Nascimento AS, Ayers SD, et al. Medium chain fatty acids are selective peroxisome proliferator activated receptor (PPAR) activators and Pan-PPAR partial agonists. Plos One. 2012; 7: e36297.
37. Itoh T, Fairall L, Amin K, et al. Structural basis for the activation of PPAR by oxidized fatty acids. Nat Struct Mol Biol. 2008; 15: 924-931.
38. Ambrosio AL, Dias SM, Polikarpov I, Zurier RB, Burstein SH, Garratt RC. Ajulemic acid, a synthetic nonpsychoactive cannabinoid acid, bound to the ligand binding domain of the human peroxisome proliferator-activated receptor γ. J Biol Chem. 2007; 282: 18625-18633.
39. Estébanez-Perpiñá E, Arnold LA, Jouravel N, et al. Structural insight into the mode of action of a direct inhibitor of coregulator binding to the thyroid hormone receptor. Mol Endocrinol. 2007; 21: 2919-2928.
40. Hwang JY, Arnold LA, Zhu F, et al. Improvement of pharmacological properties of irreversible thyroid receptor coactivator binding inhibitors. J Med Chem. 2009; 52: 3892-3901.
41. Hwang JY, Attia RR., Carrillo AK, Connelly MC, Guy RK. Synthesis and evaluation of methylsulfonylnitrobenzamides (MSNBAs) as inhibitors of the thyroid hormone receptor-coactivator interaction. Bioorg Med Chem Lett. 2013; 23: 1891-1895.
42. Nunes FM, Aparício R, Santos MA, et al. Crystallization and preliminary X-ray diffraction studies of isoform α1 of the human thyroid hormone receptor ligand-binding domain. Acta Crystallogr D Biol Crystallogr. 2004; 60: 1867-1870.
43. Otwinowski Z, Minor W. Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997; 276: 307-326.
44. Navaza J. Implementation of molecular replacement in AMoRe. Acta Crystallogr D Biol Crystallogr. 2001; 57: 1367-1372.
45. Adams PD, Afonine PV, Bunkóczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D. 2010; 66: 213-221.
46. Murshudov G, Vagin A, Dodson E. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol. Crystallogr. 1997; 53: 240-255.
47. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004; 60: 2126-2132.
48. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009; 25: 1189-1191.
49. Lockless SW, Ranganathan R. Evolutionarily conserved pathways of energetic connectivity in protein families. Science. 1999; 286: 295-299.
50. Süel GM, Lockless SW, Wall MA, Ranganathan R. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nature Struct Biol. 2003; 10: 59-69.
51. Feng W, Ribeiro RC, Wagner RL, et al. Hormone-dependent coactivator binding to a hydrophobic cleft on nuclear receptors. Science. 1998; 280: 1747-1749.
52. Martínez L, Andrade R, Birgin EG, Martínez JM. PACKMOL: A package for building initial configurations for molecular dynamics simulations. J Comput Chem. 2009; 30: 2157-2164.
53. Martínez JM, Martínez L. Packing optimization for automated generation of complex system's initial configurations for molecular dynamics and docking. J Comput Chem. 2003; 24: 819-825.
54. Verlet L. Computer experiments on classical fluids. I Thermodinamical properties of Lennard-Jones molecules. Phys Rev. 1967; 159: 98-103.
55. Darden T, York D, Pedersen L. Particle Mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys. 1993; 98: 10089-10092.
56. Phillips JC, Braun R, Wang W, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005; 26: 1781-1802.
57. MacKerell AD Jr, Bashford D, Bellott M, et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B. 1998; 102: 3586-3616.
58. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 1983; 79: 926-935.
59. Duggan BM, Craik DJ. Conformational dynamics of thyroid hormones by variable temperature nuclear magnetic resonance: the role of side chain rotations and cisoid/transoid interconversions. J Med Chem. 1997; 40: 2259-2265.
60. 13C NMR relaxation studies of molecular dynamics of the thyroid hormones thyroxine, 3, 5, 3-triiodothyronine, and 3, 5-diiodothyronine. J Med Chem. 1996; 39: 4007-4016.
61. Hansson AO, Souza PCT, Silveira RL, Martínez L, Skaf MS. CHARMM force field parameterization of rosiglitazone. Int J Quantum Chem. 2011; 111: 1346-1354.
62. Prates ET, Souza PCT, Pickholz M, Skaf MS. CHARMM based parameterization of neutral articaine-a widely used local anesthesic. Intern J Quantum Chem. 2011; 111: 1339-1345.
63. Hénin J, Fiorin J, Chipot C, Klein ML. Exploring multidimensional free energy landscapes using time-dependent biases on collective variables. J Chem Theory Comput. 2010; 6: 35-47.
64. Hénin J, Chipot C. Overcoming free energy barriers using unconstrained molecular dynamics simulations. J Chem Phys. 2004; 121: 2904-2914.
65. Chipot C, Hénin J. Exploring the free-energy landscape of a short peptide using an average force. J Chem Phys. 2005; 123: 244906.
66. Nascimento AS, Dias SM, Nunes FM, et al. Structural rearrangements in the thyroid hormone receptor hinge domain and their putative role in the receptor function. J Mol Biol. 2006; 360: 586-598.
67. Wagner RL, Apriletti JW, McGrath ME, West BL, Baxter JD, Fletterick RJ. A structural role for hormone in the thyroid hormone receptor. Nature. 1995; 378: 690-697.
68. Borngraeber S, Budny MJ, Chiellini G, et al. Ligand selectivity by seeking hydrophobicity in thyroid hormone receptor. Proc Natl Acad Sci USA. 2003; 100: 15358-15363.
69. Escobar-Morreale HF, Obregón MJ, Escobar del Rey F, Morreale de Escobar G. Replacement therapy for hypothyroidism with thyroxine alone does not ensure euthyroidism in all tissues, as studied in thyroidectomized rats. J Clin Invest. 1995; 96: 2828-2838.
70. Trost SU, Swanson E, Gloss B, et al. The thyroid hormone receptor-β-selective agonist GC-1 differentially affects plasma lipids and cardiac activity. Endocrinology. 2000; 141: 3057-3064.
71. Oppenheimer JH, Schwartz HL. Stereospecific transport of triiodothyronine from plasma to cytosol and from cytosol to nucleus in rat liver, kidney, brain, and heart. J Clin Invest. 1985; 75: 147-154.
72. Shahrara S, Drvota V, Sylvén C. Organ specific expression of thyroid hormone receptor mRNA and protein in different human tissues. Biol Pharm Bull. 1999; 22: 1027-1033.
73. Souza PC, Barra GB, Velasco LF, et al. Helix 12 dynamics and thyroid hormone receptor activity: experimental and molecular dynamics studies of Ile280 mutants. J Mol Biol. 2011; 412: 882-893.
74. Marimuthu A, Feng W, Tagami T, et al. TR surfaces and conformations required to bind nuclear receptor corepressor. Mol Endocrinol. 2002; 16: 271-286.
75. Togashi M, Nguyen P, Fletterick R, Baxter JD, Webb P. Rearrangements in thyroid hormone receptor charge clusters that stabilize bound 3, 5, 5-triiodo-L-thyronine and inhibit homodimer formation. J Biol Chem. 2005; 280: 25665-25673.
76. Ribeiro RC, Feng W, Wagner RL, et al. 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. 2001; 276: 14987-14995.
77. de Araujo AS, Martínez L, de Paula Nicoluci R, Skaf MS, Polikarpov I. Structural modeling of high-affinity thyroid receptor-ligand complexes. Eur Biophys J. 2010; 39: 1523-1536.
78. Takayama S, Hostick U, Haendel M, Eisen J, Darimont B. An F-domain introduced by alternative splicing regulates activity of the zebrafish thyroid hormone receptor α. Gen Comp Endocrinol. 2008; 155: 176-189.