Mechanistic insights into the allosteric modulation of opioid receptors by sodium ions

Biochemistry

Volumn 53, Issue 31, 2014, Pages 5140-5149

  Shang, Yi ^a   Lerouzic, Valerie ^b   Schneider, Sebastian ^a   Bisignano, Paola ^a   Pasternak, Gavril W ^b   Filizola, Marta ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; COMPUTER SIMULATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; EXPERIMENTS; LIGANDS; METAL IONS; MOLECULAR DYNAMICS;

ALLOSTERIC MODULATION; BINDING AFFINITIES; G-PROTEIN COUPLED RECEPTORS; INTRACELLULAR SIDE; MOLECULAR DYNAMICS SIMULATIONS; NON-CONSERVED RESIDUES; SEQUENCE SIMILARITY; TRANSFECTED CELLS;

SODIUM;

G PROTEIN COUPLED RECEPTOR; OPIATE RECEPTOR; RECEPTOR SUBTYPE; SODIUM; SODIUM ION;

ALLOSTERISM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ATOM; BINDING SITE; BRAIN HOMOGENATE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FEMALE; LIGAND BINDING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIMULATION;

ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HUMANS; LIGANDS; MICE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; RADIOLIGAND ASSAY; RECEPTORS, OPIOID; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU; SODIUM;

EID: 84905975806     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5006915     Document Type: Article

References (50)

1. Pasternak, G. W. and Snyder, S. H. (1975) Identification of novel high affinity opiate receptor binding in rat brain Nature 253, 563-565
2. Pert, C. B., Pasternak, G., and Snyder, S. H. (1973) Opiate agonists and antagonists discriminated by receptor binding in brain Science 182, 1359-1361
3. Preininger, A. M., Meiler, J., and Hamm, H. E. (2013) Conformational flexibility and structural dynamics in GPCR-mediated G protein activation: A perspective J. Mol. Biol. 425, 2288-2298
4. Pasternak, G. W. and Pan, Y. X. (2013) Mu opioids and their receptors: Evolution of a concept Pharmacol. Rev. 65, 1257-1317
5. + Ion that Stabilises the Ligand-Free Receptor PLoS One 9, e92727
6. Katritch, V., Fenalti, G., Abola, E. E., Roth, B. L., Cherezov, V., and Stevens, R. C. (2014) Allosteric sodium: A key co-factor in class A GPCR signaling Trends Biol. Sci. 39, 233-244
7. Werling, L. L., Brown, S. R., Puttfarcken, P., and Cox, B. M. (1986) Sodium regulation of agonist binding at opioid receptors. II. Effects of sodium replacement on opioid binding in guinea pig cortical membranes Mol. Pharmacol. 30, 90-95
8. Vosahlikova, M., Jurkiewicz, P., Roubalova, L., Hof, M., and Svoboda, P. (2014) High- and low-affinity sites for sodium in δ-OR-Gi1α (Cys (351)-Ile (351)) fusion protein stably expressed in HEK293 cells; functional significance and correlation with biophysical state of plasma membrane Naunyn-Schmiedeberg's Arch. Pharmacol. 387, 487-502
9. Pasternak, G. W., Wilson, H. A., and Snyder, S. H. (1975) Differential effects of protein-modifying reagents on receptor binding of opiate agonists and antagonists Mol. Pharmacol. 11, 340-351
10. 3H]opiate agonist binding by divalent cations Mol. Pharmacol. 11, 735-744
11. Christopoulos, A. (2002) Allosteric binding sites on cell-surface receptors: Novel targets for drug discovery Nat. Rev. Drug Discovery 1, 198-210
12. Horstman, D. A., Brandon, S., Wilson, A. L., Guyer, C. A., Cragoe, E. J., Jr., and Limbird, L. E. (1990) An aspartate conserved among G-protein receptors confers allosteric regulation of α2-adrenergic receptors by sodium J. Biol. Chem. 265, 21590-21595
13. Neve, K. A., Cumbay, M. G., Thompson, K. R., Yang, R., Buck, D. C., Watts, V. J., DuRand, C. J., and Teeter, M. M. (2001) Modeling and mutational analysis of a putative sodium-binding pocket on the dopamine D2 receptor Mol. Pharmacol. 60, 373-381
14. Barbhaiya, H., McClain, R., Ijzerman, A., and Rivkees, S. A. (1996) Site-directed mutagenesis of the human A1 adenosine receptor: Influences of acidic and hydroxy residues in the first four transmembrane domains on ligand binding Mol. Pharmacol. 50, 1635-1642
15. 3 adenosine receptor Mol. Pharmacol. 63, 1021-1031
16. Nie, J. and Lewis, D. L. (2001) Structural domains of the CB1 cannabinoid receptor that contribute to constitutive activity and G-protein sequestration J. Neurosci. 21, 8758-8764
17. Proulx, C. D., Holleran, B. J., Boucard, A. A., Escher, E., Guillemette, G., and Leduc, R. (2008) Mutational analysis of the conserved Asp2.50 and ERY motif reveals signaling bias of the urotensin II receptor Mol. Pharmacol. 74, 552-561
18. Martin, S., Botto, J. M., Vincent, J. P., and Mazella, J. (1999) Pivotal role of an aspartate residue in sodium sensitivity and coupling to G proteins of neurotensin receptors Mol. Pharmacol. 55, 210-215
19. Ballesteros, J. and Weinstein, H. (1995) Integrated methods for the construction of three-dimensional models and computational probing of structure-function relations in G protein-coupled receptors Methods Neurosci. 25, 366-428
20. Selent, J., Sanz, F., Pastor, M., and De Fabritiis, G. (2010) Induced effects of sodium ions on dopaminergic G-protein coupled receptors PLoS Comput. Biol. 6, e1000884
21. Yuan, S., Vogel, H., and Filipek, S. (2013) The role of water and sodium ions in the activation of the μ-opioid receptor Angew. Chem. 52, 10112-10115
22. Liu, W., Chun, E., Thompson, A. A., Chubukov, P., Xu, F., Katritch, V., Han, G. W., Roth, C. B., Heitman, L. H., IJzerman, A. P., Cherezov, V., and Stevens, R. C. (2012) Structural basis for allosteric regulation of GPCRs by sodium ions Science 337, 232-236
23. Zhang, C., Srinivasan, Y., Arlow, D. H., Fung, J. J., Palmer, D., Zheng, Y., Green, H. F., Pandey, A., Dror, R. O., Shaw, D. E., Weis, W. I., Coughlin, S. R., and Kobilka, B. K. (2012) High-resolution crystal structure of human protease-activated receptor 1 Nature 492, 387-392
24. Fenalti, G., Giguere, P. M., Katritch, V., Huang, X. P., Thompson, A. A., Cherezov, V., Roth, B. L., and Stevens, R. C. (2014) Molecular control of δ-opioid receptor signalling Nature 506, 191-196
25. 2A Adenosine G Protein-Coupled Receptor Structure 21, 2175-2185
26. White, J. F., Noinaj, N., Shibata, Y., Love, J., Kloss, B., Xu, F., Gvozdenovic-Jeremic, J., Shah, P., Shiloach, J., Tate, C. G., and Grisshammer, R. (2012) Structure of the agonist-bound neurotensin receptor Nature 490, 508-513
27. Manglik, A., Kruse, A. C., Kobilka, T. S., Thian, F. S., Mathiesen, J. M., Sunahara, R. K., Pardo, L., Weis, W. I., Kobilka, B. K., and Granier, S. (2012) Crystal structure of the μ-opioid receptor bound to a morphinan antagonist Nature 485, 321-326
28. Wu, H., Wacker, D., Mileni, M., Katritch, V., Han, G. W., Vardy, E., Liu, W., Thompson, A. A., Huang, X. P., Carroll, F. I., Mascarella, S. W., Westkaemper, R. B., Mosier, P. D., Roth, B. L., Cherezov, V., and Stevens, R. C. (2012) Structure of the human κ-opioid receptor in complex with JDTic Nature 485, 327-332
29. Kaufmann, K. W., Lemmon, G. H., DeLuca, S. L., Sheehan, J. H., and Meiler, J. (2010) Practically Useful: What the Rosetta Protein Modeling Suite Can Do for You Biochemistry 49, 2987-2998
30. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling Electrophoresis 18, 2714-2723
31. Marchi, M. and Ballone, P. (1999) Adiabatic bias molecular dynamics: A method to navigate the conformational space of complex molecular systems J. Chem. Phys. 110, 3697-3702
32. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the β2 adrenergic receptor-Gs protein complex Nature 477, 549-555
33. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., and Mackerell, A. D., Jr. (2010) CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 31, 671-690
34. Maestro, version 9.7 (2014) Schrödinger Release 2014-1, Schrödinger, LLC, New York.
35. a prediction and protonation state generation for drug-like molecules J. Comput.-Aided Mol. Des. 21, 681-691
36. Mićović, V. I., Ivanović, M. D., and Došen-Mićović, L. J. (2009) Structural requirements for ligands of the δ-opioid receptor J. Serb. Chem. Soc. 74, 1207-1217
37. Friesner, R. A., Murphy, R. B., Repasky, M. P., Frye, L. L., Greenwood, J. R., Halgren, T. A., Sanschagrin, P. C., and Mainz, D. T. (2006) Extra precision glide: Docking and scoring incorporating a model of hydrophobic enclosure for protein-ligand complexes J. Med. Chem. 49, 6177-6196
38. Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. (2005) GROMACS: Fast, flexible, and free J. Comput. Chem. 26, 1701-1718
39. Nosé, S. and Klein, M. L. (1983) Constant pressure molecular dynamics for molecular systems Mol. Phys. 50, 1055-1076
40. Parrinello, M. and Rahman, A. (1980) Crystal Structure and Pair Potentials: A Molecular-Dynamics Study Phys. Rev. Lett. 45, 1196-1199
41. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18, 1463-1472
42. Bonomi, M., Branduardi, D., Bussi, G., Camilloni, C., Provasi, D., Raiteri, P., Donadio, D., Marinelli, F., Pietrucci, F., Broglia, R. A., and Parrinello, M. (2009) PLUMED: A portable plugin for free-energy calculations with molecular dynamics Comput. Phys. Commun. 180, 1961-1972
43. Ludemann, S. K., Lounnas, V., and Wade, R. C. (2000) How do substrates enter and products exit the buried active site of cytochrome P450cam? 1. Random expulsion molecular dynamics investigation of ligand access channels and mechanisms J. Mol. Biol. 303, 797-811
44. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kale, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD J. Comput. Chem. 26, 1781-1802
45. Brooks, B. R., Brooks, C. L., III, Mackerell, A. D., Jr., Nilsson, L., Petrella, R. J., Roux, B., Won, Y., Archontis, G., Bartels, C., Boresch, S., Caflisch, A., Caves, L., Cui, Q., Dinner, A. R., Feig, M., Fischer, S., Gao, J., Hodoscek, M., Im, W., Kuczera, K., Lazaridis, T., Ma, J., Ovchinnikov, V., Paci, E., Pastor, R. W., Post, C. B., Pu, J. Z., Schaefer, M., Tidor, B., Venable, R. M., Woodcock, H. L., Wu, X., Yang, W., York, D. M., and Karplus, M. (2009) CHARMM: The biomolecular simulation program J. Comput. Chem. 30, 1545-1614
46. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14, 33-38
47. The PyMOL Molecular Graphics System, version 1.3r1 (2010) Schrödinger, LLC, New York.
48. Hunter, J. D. (2007) Matplotlib: A 2D graphics environment Comput. Sci. Eng. 9, 90-95
49. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent J. Biol. Chem. 193, 265-275
50. Deupi, X. and Standfuss, J. (2011) Structural insights into agonist-induced activation of G-protein-coupled receptors Curr. Opin. Struct. Biol. 21, 541-551