The "phantom effect" of the rexinoid LG100754: Structural and functional insights

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Sato, Yoshiteru ^a,c   Ramalanjaona, Nick ^a   Huet, Tiphaine ^a   Potier, Noelle ^b   Osz, Judit ^a   Antony, Pierre ^a   Peluso Iltis, Carole ^a   Poussin Courmontagne, Pierre ^a   Ennifar, Eric ^a   Mély, Yves ^a   Dejaegere, Annick ^a   Moras, Dino ^a   Rochel, Natacha ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ LOUIS PASTEUR   (France)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYL 7 (5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 3 PROPOXY 2 NAPHTHYL) 2,4,6 OCTATRIENOIC ACID; 4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; BMS 614; BMS 649; HETERODIMER; HX 531; OLEIC ACID; PROTEIN INHIBITOR; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID DERIVATIVE; RETINOID X RECEPTOR; RETINOID X RECEPTOR ALPHA; SOLVENT; UNCLASSIFIED DRUG; UV 3002; UV 3003; LIGAND; RECOMBINANT PROTEIN; RETINOIC ACID RECEPTOR ALPHA; RETINOID; TETRALIN DERIVATIVE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; LIGAND BINDING; MOLECULAR MECHANICS; PHANTOM; PROTEIN CONFORMATION; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION; ANIMAL; BINDING COMPETITION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE POLARIZATION; GENETICS; HUMAN; METABOLISM; MOUSE; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; SIGNAL TRANSDUCTION; SMALL ANGLE SCATTERING; X RAY DIFFRACTION;

ATRA;

ANIMALS; BINDING SITES; BINDING, COMPETITIVE; FLUORESCENCE POLARIZATION; HUMANS; LIGANDS; MICE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR CROSS-TALK; RECEPTORS, RETINOIC ACID; RECOMBINANT PROTEINS; RETINOID X RECEPTORS; RETINOIDS; SCATTERING, SMALL ANGLE; TETRAHYDRONAPHTHALENES; TRETINOIN; X-RAY DIFFRACTION;

EID: 78649771898     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015119     Document Type: Article

References (58)

1. Mark M, Ghyselinck NB, Chambon P (2009) Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 7: e002.
2. Mark M, Ghyselinck NB, Chambon P (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu Rev Pharmacol Toxicol 46: 451-480.
3. Perissi V, Rosenfeld MG (2005) Controlling nuclear receptors: the circular logic of cofactor cycles. Nat Rev Mol Cell Biol 6: 542-554.
4. Rosenfeld MG, Lunyak VV, Glass CK (2006) Sensors and signals: a coactivator/ corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20: 1405-1428.
5. Rochette-Egly C, Germain P (2009) Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl Recept Signal 7: e005.
6. Germain P, Iyer J, Zechel C, Gronemeyer H (2002) Co-regulator recruitment and the mechanism of retinoic acid receptor synergy. Nature 415: 187-192.
7. Minucci S, Leid M, Toyama R, Saint-Jeannet JP, Peterson VJ, et al. (1997) Retinoid X receptor (RXR) within the RXR-retinoic acid receptor heterodimer binds its ligand and enhances retinoid-dependent gene expression. Mol Cell Biol 17: 644-655.
8. Kersten S, Dawson MI, Lewis BA, Noy N (1996) Individual subunits of heterodimers comprised of retinoic acid and retinoid X receptors interact with their ligands independently. Biochemistry 35: 3816-3824.
9. Chen JY, Clifford J, Zusi C, Starrett J, Tortolani D, et al. (1996) Two distinct actions of retinoid-receptor ligands. Nature 382: 819-822.
10. DiRenzo J, Söderstrom M, Kurokawa R, Ogliastro MH, Ricote M, et al. (1997) Peroxisome proliferator-activated receptors and retinoic acid receptors differentially control the interactions of retinoid X receptor heterodimers with ligands, coactivators, and corepressors. Mol Cell Biol 17: 2166-2176.
11. Aarnisalo P, Kim CH, Lee JW, Perlmann T (2002) Defining requirements for heterodimerization between the retinoid X receptor and the orphan nuclear receptor Nurr1. J Biol Chem 277: 35118-35123.
12. Bourguet W, Vivat V, Wurtz JM, Chambon P, Gronemeyer H, et al. (2000) Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol Cell 5: 289-298.
13. Pogenberg V, Guichou JF, Vivat-Hannah V, Kammerer S, Pérez E, et al. (2005) Characterization of the interaction between retinoic acid receptor/retinoid X receptor (RAR/RXR) heterodimers and transcriptional coactivators through structural and fluorescence anisotropy studies. J Biol Chem 280: 1625-1633.
14. Lala DS, Mukherjee R, Schulman IG, Koch SS, Dardashti LJ, et al. (1996) Activation of specific RXR heterodimers by an antagonist of RXR homodimers. Nature 383: 450-453.
15. Mukherjee R, Jow L, Croston GE, Paterniti JR Jr. (1997) Identification, characterization, and tissue distribution of human peroxisome proliferatoractivated receptor (PPAR) isoforms PPARgamma2 versus PPARgamma1 and activation with retinoid X receptor agonists and antagonists. J Biol Chem 272: 8071-8076.
16. Schulman IG, Li C, Schwabe JW, Evans RM (1997) The phantom ligand effect: allosteric control of transcription by the retinoid X receptor. Genes Dev 11: 299-308.
17. Lu HC, Revelli JP, Goering L, Thaller C, Eichele G (1997) Retinoid signaling is required for the establishment of a ZPA and for the expression of Hoxb-8, a mediator of ZPA formation. Development 124: 1643-1651.
18. Billas IM, Iwema T, Garnier JM, Mitschler A, Rochel N, et al. (2003) Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature 426: 91-96.
19. Egea PF, Rochel N, Birck C, Vachette P, Timmins PA, et al. (2001) Effects of ligand binding on the association properties and conformation in solution of retinoic acid receptors RXR and RAR. J Mol Biol 307: 557-576.
20. Lafont V, Schaefer M, Stote RH, Altschuh D, Dejaegere A (2007) Proteinprotein recognition and interaction hot spots in an antigen-antibody complex: free energy decomposition identifies "efficient amino acids". Proteins 67:418-434.
21. Brelivet Y, Kammerer S, Rochel N, Poch O, Moras D (2004) Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep 5: 423-429.
22. Vivat-Hannah V, Bourguet W, Gottardis M, Gronemeyer H (2003) Separation of retinoid X receptor homo- and heterodimerization functions. Mol Cell Biol 23: 7678-7688.
23. Renaud JP, Rochel N, Ruff M, Vivat V, Chambon P, et al. (1995) Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid. Nature 378: 681-689.
24. Egea PF, Mitschler A, Rochel N, Ruff M, Chambon P, et al. (2000) Crystal structure of the human RXRalpha ligand-binding domain bound to its natural ligand: 9-cis retinoic acid. EMBO J 19: 2592-2601.
25. Egea PF, Mitschler A, Moras D (2002) Molecular recognition of agonist ligands by RXRs. Mol Endocrinol 16: 987-997.
26. Folkertsma S, van Noort PI, de Heer A, Carati P, Brandt R, et al. (2007) The use of in vitro peptide binding profiles and in silico ligand-receptor interaction profiles to describe ligand-induced conformations of the retinoid X receptor alpha ligand-binding domain. Mol Endocrinol 21: 30-48.
27. Hashimoto Y, Miyachi H (2005) Nuclear receptor antagonists designed based on the helix-folding inhibition hypothesis. Bioorg Med Chem 13: 5080-5093.
28. Pérez Santín E, Germain P, Quillard F, Khanwalkar H, Rodríguez-Barrios F, et al. (2009) Modulating retinoid X receptor with a series of (E)-3-[4-hydroxy-3-(3-alkoxy-5,5,8,8-tetramethyl-5,6,7,8-tetrahydronaphthalen-2-yl)phenyl]acrylic acids and their 4-alkoxy isomers. J Med Chem 52: 3150-3158.
29. Ebisawa M, Umemiya H, Ohta K, Fukasawa H, Kawachi E, et al. (1999) Retinoid X receptor-antagonistic diazepinylbenzoic acids. Chem Pharm Bull 47: 1778-1786.
30. Nahoum V, Pérez E, Germain P, Rodríguez-Barrios F, Manzo F, et al. (2007) Modulators of the structural dynamics of the retinoid X receptor to reveal receptor function. Proc Natl Acad Sci USA 104: 17323-17328.
31. Koch SSC, Dardashti LJ, Hebert JJ, White SK, Croston GE, et al. (1996) Identification of the first retinoid X receptor homodimer antagonist. J Med Chem 39: 3229-3234.
32. Lu J, Dawson MI, Hu QY, Xia Z, Dambacher JD, et al. (2009) The effect of antagonists on the conformational exchange of the retinoid X receptor alpha ligand-binding domain. Magn Reson Chem 47: 1071-1080.
33. Lehmann JM, Jong L, Fanjul A, Cameron JF, Lu XP, et al. (1992) Retinoids selective for retinoid X receptor response pathways. Science 258: 1944-1946.
34. Delescluse C, Cavey MT, Martin B, Bernard BA, Reichert U, et al. (1991) Selective high affinity retinoic acid receptor alpha or beta-gamma ligands. Mol. Pharmacol 40: 556-562.
35. Xu J, Li Q (2003) Review of the in Vivo Functions of the p160 Steroid Receptor Coactivator Family. Molecular Endocrinology 17: 1681-1692.
36. Pike AC, Brzozowski AM, Hubbard RE, Bonn T, Thorsell AG, et al. (1999) Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO J 18: 4608-4618.
37. de Lera AR, Bourguet W, Altucci L, Gronemeyer H (2007) Design of selective nuclear receptor modulators: RAR and RXR as a case study. Nat Rev Drug Discov 6: 811-820.
38. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology 276: 307-326 Academic Press (New York).
39. Navaza J (1994) AMoRe-an automated package for molecular replacement. Acta Crystallogr A50: 157-163.
40. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D54: 905-921.
41. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular Structures by the Maximum-Likelihood Method. Acta Cryst D53: 240-255.
42. Afonine PV, Grosse-Kunstleve RW, Adams PD (2005) CCP4 Newsl 42, contribution 8.
43. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electrondensity maps and the location of errors in these models. Acta Crystallogr A47: 110-119.
44. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D60: 2126-2132.
45. Painter, J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Cryst D62: 439-450.
46. Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283-291.
47. Kleywegt GJ, Jones TA (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Cryst D50: 178-185.
48. Nicholls A Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.
49. DeLano WL (2002) DeLano Scientific, San Carlos, CA, USA. http://www.pymol.org.
50. Potterton E, McNicholas S, Krissinel E, Cowtan K, Noble M (2002) The CCP4 molecular-graphics project. Acta Cryst D58: 1955-1957.
51. Brunger AT, Karplus M (1988) Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison. Proteins 4: 148-156.
52. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, et al. (1983) Charmm: a program for macromolecular energy minimization and dynamics calculations. J Comp Chem 4: 187-217.
53. Roessle MW et al (2007) Upgrade of the Small Angle X-ray scattering Beamline X33 at the European Molecular Biology Laboratory, Hamburg. J Appl Crystallogr 40: S190-S194.
54. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36: 1277-1282.
55. Guinier A (1939) Diffraction of x-rays of very small angles-application to the study of ultramicroscopic phenomena. Ann Phys 12: 161-237.
56. Svergun DI (1992) Determination of the Regularization Parameter in Indirect- Transform Methods Using Perceptual Criteria. J AppL Cryst 25: 495-503.
57. Svergun D, Barberato C, Koch MHJ (1995) CRYSOL - a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates. J Appl Cryst 28: 768-773.
58. Potier N, Rogniaux H, Chevreux G, Van Dorsselaer A (2005) Ligand-metal ion binding to proteins: investigation by ESI mass spectrometry. Methods in Enzymology 402: 361-389.