Structural prerequisites for G-protein activation by the neurotensin receptor

Nature Communications

Volumn 6, Issue , 2015, Pages

  Krumm, Brian E ^a   White, Jim F ^a   Shah, Priyanka ^a   Grisshammer, Reinhard ^a  

^a U S DEPARTMENT OF HEALTH AND HUMAN SERVICES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROTENSIN RECEPTOR;

CHEMICAL BINDING; ENZYME ACTIVITY; MUTATION; NEUROLOGY; PEPTIDE; PROTEIN;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; CRYSTALLIZATION; GENE MUTATION; HYDROGEN BOND; INSECT CELL; INSECT CELL CULTURE; LIGAND BINDING; LIPID BILAYER; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; TRICHOPLUSIA NI; ANIMAL; CELL CULTURE; CHEMICAL STRUCTURE; GENETICS; HUMAN; METABOLISM; MOTH; MUTATION;

ANIMALS; CELLS, CULTURED; GTP-BINDING PROTEINS; HUMANS; MOLECULAR STRUCTURE; MOTHS; MUTATION; RECEPTORS, NEUROTENSIN;

EID: 84937958846     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8895     Document Type: Article

References (55)

1. Deupi, X. & Kobilka, B. K. Energy landscapes as a tool to integrate GPCR structure, dynamics, and function. Physiology (Bethesda) 25, 293-303 (2010).
2. Manglik, A. et al. Crystal structure of the mu-opioid receptor bound to a morphinan antagonist. Nature 485, 321-326 (2012).
3. White, J. F. et al. Structure of the agonist-bound neurotensin receptor. Nature 490, 508-513 (2012).
4. Choe, H. W. et al. Crystal structure of metarhodopsin II. Nature 471, 651-655 (2011).
5. Kruse, A. C. et al. Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 504, 101-106 (2013).
6. Rasmussen, S. G. et al. Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 469, 175-180 (2011).
7. Rasmussen, S. G. et al. Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477, 549-555 (2011).
8. Tanaka, K., Masu, M. & Nakanishi, S. Structure and functional expression of the cloned rat neurotensin receptor. Neuron 4, 847-854 (1990).
9. Carraway, R. & Leeman, S. E. The isolation of a new hypotensive peptide, neurotensin, from bovine hypothalami. J. Biol. Chem. 248, 6854-6861 (1973).
10. Griebel, G. & Holsboer, F. Neuropeptide receptor ligands as drugs for psychiatric diseases: the end of the beginning? Nat. Rev. Drug Discov. 11, 462-478 (2012).
11. Kitabgi, P. Targeting neurotensin receptors with agonists and antagonists for therapeutic purposes. Curr. Opin. Drug Discov. Devel. 5, 764-776 (2002).
12. Shibata, Y. et al. Optimising the combination of thermostabilising mutations in the neurotensin receptor for structure determination. Biochim. Biophys. Acta 1828, 1293-1301 (2013).
13. Ballesteros, J. A. & Weinstein, H. Integrated methods for the construction of three-dimensional models and computationla probing of structure-function relations in G protein-coupled receptors. Methods Neurosci. 25, 366-428 (1995).
14. Gully, D. et al. Biochemical and pharmacological profile of a potent and selective nonpeptide antagonist of the neurotensin receptor. Proc. Natl Acad. Sci. USA 90, 65-69 (1993).
15. Rovati, G. E., Capra, V. & Neubig, R. R. The highly conserved DRY motif of class A G protein-coupled receptors: beyond the ground state. Mol. Pharmacol. 71, 959-964 (2007).
16. Warne, T. et al. Structure of a beta1-adrenergic G-protein-coupled receptor. Nature 454, 486-491 (2008).
17. Cherezov, V. et al. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258-1265 (2007).
18. Egloff, P. et al. Structure of signaling-competent neurotensin receptor 1 obtained by directed evolution in Escherichia coli. Proc. Natl Acad. Sci. USA 111, E655-E662 (2014).
19. Lee, S., Bhattacharya, S., Tate, C. G., Grisshammer, R. & Vaidehi, N. Structural dynamics and thermostabilization of neurotensin receptor 1. J. Phys. Chem. B 119, 4917-4928 (2015).
20. Lin, S. W. & Sakmar, T. P. Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state. Biochemistry 35, 11149-11159 (1996).
21. Pope, A., Eilers, M., Reeves, P. J. & Smith, S. O. Amino acid conservation and interactions in rhodopsin: probing receptor activation by NMR spectroscopy. Biochim. Biophys. Acta 1837, 683-693 (2014).
22. Standfuss, J. et al. The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660 (2011).
23. Tehan, B. G., Bortolato, A., Blaney, F. E., Weir, M. P. & Mason, J. S. Unifying family A GPCR theories of activation. Pharmacol. Ther. 143, 51-60 (2014).
24. Martin, S., Botto, J. M., Vincent, J. P. & Mazella, J. Pivotal role of an aspartate residue in sodium sensitivity and coupling to G proteins of neurotensin receptors. Mol. Pharmacol. 55, 210-215 (1999).
25. Fenalti, G. et al. Molecular control of delta-opioid receptor signalling. Nature 506, 191-196 (2014).
26. Liu, W. et al. Structural basis for allosteric regulation of GPCRs by sodium ions. Science 337, 232-236 (2012).
27. Miller-Gallacher, J. L. et al. The 2.1A resolution structure of cyanopindololbound beta1-adrenoceptor identifies an intramembrane Na? ion that stabilises the ligand-free receptor. PLoS ONE 9, e92727 (2014).
28. Zhang, C. et al. High-resolution crystal structure of human protease-activated receptor 1. Nature 492, 387-392 (2012).
29. Scheerer, P. et al. Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497-502 (2008).
30. Shibata, Y. et al. Thermostabilization of the neurotensin receptor NTS1. J. Mol. Biol. 390, 262-277 (2009).
31. Tate, C. G. A crystal clear solution for determining G-protein-coupled receptor structures. Trends Biochem. Sci. 37, 343-352 (2012).
32. Sarkar, C. A. et al. Directed evolution of a G protein-coupled receptor for expression, stability, and binding selectivity. Proc. Natl Acad. Sci. USA 105, 14808-14813 (2008).
33. Schlinkmann, K. M. et al. Maximizing detergent stability and functional expression of a GPCR by exhaustive recombination and evolution. J. Mol. Biol. 422, 414-428 (2012).
34. Schlinkmann, K. M. et al. Critical features for biosynthesis, stability, and functionality of a G protein-coupled receptor uncovered by all-versus-all mutations. Proc. Natl Acad. Sci. USA 109, 9810-9815 (2012).
35. Franke, R. R., Konig, B., Sakmar, T. P., Khorana, H. G. & Hofmann, K. P. Rhodopsin mutants that bind but fail to activate transducin. Science 250, 123-125 (1990).
36. Kobilka, B. K. Amino and carboxyl terminal modifications to facilitate the production and purification of a G protein-coupled receptor. Anal. Biochem. 231, 269-271 (1995).
37. Hellmich, M. R., Battey, J. F. & Northup, J. K. Selective reconstitution of gastrin-releasing peptide receptor with G alpha q. Proc. Natl Acad. Sci. USA 94, 751-756 (1997).
38. Hartman, J. L. & Northup, J. K. Functional reconstitution in situ of 5-hydroxytryptamine 2c (5HT2c) receptors with alphaq and inverse agonism of 5HT2c receptor antagonists. J. Biol. Chem. 271, 22591-22597 (1996).
39. Jian, X. et al. The bombesin receptor subtypes have distinct G protein specificities. J. Biol. Chem. 274, 11573-11581 (1999).
40. Cheng, Y. & Prusoff, W. H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108 (1973).
41. Inagaki, S. et al. Modulation of the interaction between neurotensin receptor NTS1 and Gq protein by lipid. J. Mol. Biol. 417, 95-111 (2012).
42. Chattopadhyay, A. & Harikumar, K. G. Dependence of critical micelle concentration of a zwitterionic detergent on ionic strength: implications in receptor solubilization. FEBS Lett. 391, 199-202 (1996).
43. Chae, P. S. et al. Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins. Nat. Methods 7, 1003-1008 (2010).
44. Caffrey, M. & Cherezov, V. Crystallizing membrane proteins using lipidic mesophases. Nat. Protoc. 4, 706-731 (2009).
45. Landau, E. M. & Rosenbusch, J. P. Lipidic cubic phases: a novel concept for the crystallization of membrane proteins. Proc. Natl Acad. Sci. USA 93, 14532-14535 (1996).
46. Cherezov, V. et al. Rastering strategy for screening and centring of microcrystal samples of human membrane proteins with a sub-10 microm size X-ray synchrotron beam. J. R. Soc. Interface 6(Suppl 5): S587-S597 (2009).
47. Hilgart, M. C. et al. Automated sample-scanning methods for radiation damage mitigation and diffraction-based centering of macromolecular crystals. J. Synchrotron Radiat. 18, 717-722 (2011).
48. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
49. Evans, P. R. & Murshudov, G. N. How good are my data and what is the resolution? Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013).
50. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
51. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
52. Winn, M. D., Isupov, M. N. & Murshudov, G. N. Use of TLS parameters to model anisotropic displacements in macromolecular refinement. Acta Crystallogr. D Biol. Crystallogr. 57, 122-133 (2001).
53. Painter, J. & Merritt, E. A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450 (2006).
54. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
55. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).