Nuclear receptor full-length architectures: Confronting myth and illusion with high resolution

Trends in Biochemical Sciences

Volumn 40, Issue 1, 2015, Pages 16-24

  Rastinejad, Fraydoon ^a   Ollendorff, Vincent ^b   Polikarpov, Igor ^c  

^a BURNHAM INSTITUTE   (United States)

^b University of Montpellier   (France)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Allostery; BRET; Electron microscopy; Nuclear receptor; SAXS; Transcription factor; X ray crystallography

Indexed keywords

CELL NUCLEUS RECEPTOR; DNA; LIVER X RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; VITAMIN D RECEPTOR; CELL RECEPTOR; DNA BINDING PROTEIN; LIGAND;

ALLOSTERISM; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; DIMERIZATION; ELECTRON MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE SPECTROSCOPY; GEL MOBILITY SHIFT ASSAY; LIGAND BINDING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STOICHIOMETRY; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING; STRUCTURE ACTIVITY RELATION;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA; DNA-BINDING PROTEINS; LIGANDS; MICROSCOPY, ELECTRON; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SCATTERING, SMALL ANGLE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84926357367     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2014.10.011     Document Type: Review

References (58)

1. Mangelsdorf D.J., et al. The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
2. Rastinejad F., et al. Understanding nuclear receptor form and function using structural biology. J. Mol. Endocrinol. 2013, 51:T1-T21.
3. Cotnoir-White D., et al. Evolution of the repertoire of nuclear receptor binding sites in genomes. Mol. Cell. Endocrinol. 2011, 334:76-82.
4. Khorasanizadeh S., Rastinejad F. Nuclear-receptor interactions on DNA-response elements. Trends Biochem. Sci. 2001, 26:384-390.
5. Nagy L., Schwabe J.W. Mechanism of the nuclear receptor molecular switch. Trends Biochem. Sci. 2004, 29:317-324.
6. Huang P., et al. Structural overview of the nuclear receptor superfamily: insights into physiology and therapeutics. Annu. Rev. Physiol. 2010, 72:247-272.
7. Wagner R.L., et al. A structural role for hormone in the thyroid hormone receptor. Nature 1995, 378:690-697.
8. Renaud J.P., et al. Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid. Nature 1995, 378:681-689.
9. Brzozowski A.M., et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
10. Shiau A.K., et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998, 95:927-937.
11. Darimont B.D., et al. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev. 1998, 12:3343-3356.
12. Webb P., et al. The nuclear receptor corepressor (N-CoR) contains three isoleucine motifs (I/LXXII) that serve as receptor interaction domains (IDs). Mol. Endocrinol. 2000, 14:1976-1985.
13. McKenna N.J., et al. Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 1999, 20:321-344.
14. Nolte R.T., et al. Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 1998, 395:137-143.
15. Chandra V., et al. Structure of the intact PPAR-gamma-RXR- nuclear receptor complex on DNA. Nature 2008, 456:350-356.
16. Chandra V., et al. Multidomain integration in the structure of the HNF-4alpha nuclear receptor complex. Nature 2013, 495:394-398.
17. Lou X., et al. Structure of the retinoid X receptor alpha-liver X receptor beta (RXRalpha-LXRbeta) heterodimer on DNA. Nat. Struct. Mol. Biol. 2014, 21:277-281.
18. Kallenberger B.C., et al. A dynamic mechanism of nuclear receptor activation and its perturbation in a human disease. Nat. Struct. Biol. 2003, 10:136-140.
19. Johnson B.A., et al. Ligand-induced stabilization of PPARgamma monitored by NMR spectroscopy: implications for nuclear receptor activation. J. Mol. Biol. 2000, 298:187-194.
20. Berger J.P., et al. Distinct properties and advantages of a novel peroxisome proliferator-activated protein [gamma] selective modulator. Mol. Endocrinol. 2003, 17:662-676.
21. Lu J., et al. Analysis of ligand binding and protein dynamics of human retinoid X receptor alpha ligand-binding domain by nuclear magnetic resonance. Biochemistry 2006, 45:1629-1639.
22. Hughes T.S., et al. Ligand and receptor dynamics contribute to the mechanism of graded PPARgamma agonism. Structure 2012, 20:139-150.
23. Yan X., et al. Dynamics and ligand-induced solvent accessibility changes in human retinoid X receptor homodimer determined by hydrogen deuterium exchange and mass spectrometry. Biochemistry 2004, 43:909-917.
24. Figueira A.C., et al. Analysis of agonist and antagonist effects on thyroid hormone receptor conformation by hydrogen/deuterium exchange. Mol. Endocrinol. 2011, 25:15-31.
25. Hamuro Y., et al. Hydrogen/deuterium-exchange (H/D-Ex) of PPARgamma LBD in the presence of various modulators. Protein Sci. 2006, 15:1883-1892.
26. Dai S.Y., et al. Unique ligand binding patterns between estrogen receptor alpha and beta revealed by hydrogen-deuterium exchange. Biochemistry 2009, 48:9668-9676.
27. Greschik H., et al. Structural basis for the deactivation of the estrogen-related receptor gamma by diethylstilbestrol or 4-hydroxytamoxifen and determinants of selectivity. J. Biol. Chem. 2004, 279:33639-33646.
28. Blondel A., et al. Retinoic acid receptor: a simulation analysis of retinoic acid binding and the resulting conformational changes. J. Mol. Biol. 1999, 291:101-115.
29. Kosztin D., et al. Unbinding of retinoic acid from its receptor studied by steered molecular dynamics. Biophys. J. 1999, 76:188-197.
30. Martinez L., et al. Molecular dynamics simulations reveal multiple pathways of ligand dissociation from thyroid hormone receptors. Biophys. J. 2005, 89:2011-2023.
31. Martinez L., et al. 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.
32. Martinez L., et al. Only subtle protein conformational adaptations are required for ligand binding to thyroid hormone receptors: simulations using a novel multipoint steered molecular dynamics approach. J. Phys. Chem. B 2008, 112:10741-10751.
33. Zhong L., Skafar D.F. Mutations of tyrosine 537 in the human estrogen receptor-alpha selectively alter the receptor's affinity for estradiol and the kinetics of the interaction. Biochemistry 2002, 41:4209-4217.
34. Sonoda M.T., et al. Ligand dissociation from estrogen receptor is mediated by receptor dimerization: evidence from molecular dynamics simulations. Mol. Endocrinol. 2008, 22:1565-1578.
35. Osz J., et al. Structural basis for a molecular allosteric control mechanism of cofactor binding to nuclear receptors. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E588-E594.
36. Huang P., et al. Retinoic acid actions through mammalian nuclear receptors. Chem. Rev. 2014, 114:233-254.
37. Li X., et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 2013, 10:584-590.
38. Orlov I., et al. Structure of the full human RXR/VDR nuclear receptor heterodimer complex with its DR3 target DNA. EMBO J. 2012, 31:291-300.
39. Rochel N., et al. Common architecture of nuclear receptor heterodimers on DNA direct repeat elements with different spacings. Nat. Struct. Mol. Biol. 2011, 18:564-570.
40. Pogenberg V., et al. 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. 2005, 280:1625-1633.
41. Gampe R.T., et al. Asymmetry in the PPARgamma/RXRalpha crystal structure reveals the molecular basis of heterodimerization among nuclear receptors. Mol. Cell 2000, 5:545-555.
42. Zhang J., et al. DNA binding alters coactivator interaction surfaces of the intact VDR-RXR complex. Nat. Struct. Mol. Biol. 2011, 18:556-563.
43. Osz J., et al. Solution structures of PPARgamma2/RXRalpha complexes. PPAR Res. 2012, 2012:701412.
44. Helsen C., Claessens F. Looking at nuclear receptors from a new angle. Mol. Cell. Endocrinol. 2014, 382:97-106.
45. Hall J.M., et al. Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements. Mol. Endocrinol. 2002, 16:469-486.
46. Meijsing S.H., et al. DNA binding site sequence directs glucocorticoid receptor structure and activity. Science 2009, 324:407-410.
47. Bernardes A., et al. Low-resolution molecular models reveal the oligomeric state of the PPAR and the conformational organization of its domains in solution. PLoS ONE 2012, 7:e31852.
48. Moll J.R., et al. Magnesium is required for specific DNA binding of the CREB B-ZIP domain. Nucleic Acids Res. 2002, 30:1240-1246.
49. Mulero M., et al. Analysis of RXR/THR and RXR/PPARG2 heterodimerization by bioluminescence resonance energy transfer (BRET). PLoS ONE 2013, 8:e84569.
50. van Royen M.E., et al. FRAP and FRET methods to study nuclear receptors in living cells. Methods Mol. Biol. 2009, 505:69-96.
51. van Royen M.E., et al. Compartmentalization of androgen receptor protein-protein interactions in living cells. J. Cell Biol. 2007, 177:63-72.
52. Maruvada P., et al. Dynamic shuttling and intranuclear mobility of nuclear hormone receptors. J. Biol. Chem. 2003, 278:12425-12432.
53. Groeneweg F.L., et al. Quantitation of glucocorticoid receptor DNA-binding dynamics by single-molecule microscopy and FRAP. PLoS ONE 2014, 9:e90532.
54. Evans R.M., Mangelsdorf D.J. Nuclear receptors, RXR, and the big bang. Cell 2014, 157:255-266.
55. Nielsen R., et al. Genome-wide profiling of PPARgamma:RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis. Genes Dev. 2008, 22:2953-2967.
56. Glass C.K., Saijo K. Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells. Nat. Rev. Immunol. 2010, 10:365-376.
57. Bourguet W., et al. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-alpha. Nature 1995, 375:377-382.
58. Wurtz J.M., et al. A canonical structure for the ligand-binding domain of nuclear receptors. Nat. Struct. Biol. 1996, 3:87-94.