Structural dynamics and thermostabilization of neurotensin receptor 1

Journal of Physical Chemistry B

Volumn 119, Issue 15, 2015, Pages 4917-4928

  Lee, Sangbae ^a   Bhattacharya, Supriyo ^a   Tate, Christopher G ^b   Grisshammer, Reinhard ^c   Vaidehi, Nagarajan ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYSTAL STRUCTURE; LIPID BILAYERS; MOLECULAR DYNAMICS; PEPTIDES; PROTEINS; STABILITY; STRUCTURAL DYNAMICS;

BIOPHYSICAL STUDIES; EFFICIENT DESIGNS; ENERGETIC FACTORS; HYDROPHOBIC PACKING; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN PURIFICATION; RECEPTOR INTERACTION; THERMOSTABILIZATION;

HYDROGEN BONDS;

LIPID BILAYER; NEUROTENSIN; NEUROTENSIN RECEPTOR; NEUROTENSIN TYPE 1 RECEPTOR; SOLVENT; WATER;

CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; HYDROGEN BOND; LIPID BILAYER; MOLECULAR DYNAMICS; MOTION; MUTATION; PLIABILITY; PRINCIPAL COMPONENT ANALYSIS; PROTEIN STABILITY; TEMPERATURE;

HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; MOTION; MUTATION; NEUROTENSIN; PLIABILITY; PRINCIPAL COMPONENT ANALYSIS; PROTEIN STABILITY; RECEPTORS, NEUROTENSIN; SOLVENTS; TEMPERATURE; WATER;

EID: 84928034559     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp510735f     Document Type: Article

References (45)

1. Carraway, R.; Leeman, S. E. The Isolation of a New Hypotensive Peptide, Neurotensin, from Bovine Hypothalami J. Biol. Chem. 1973, 248, 6854-6861
2. Bissette, G.; Nemeroff, C. B.; Loosen, P. T.; Prange, A. J., Jr.; Lipton, M. A. Hypothermia and Intolerance to Cold Induced by Intracisternal Administration of the Hypothalamic Peptide Neurotensin Nature 1976, 262, 607-609
3. Schimpff, R. M.; Avard, C.; Fenelon, G.; Lhiaubet, A. M.; Tenneze, L.; Vidailhet, M.; Rostene, W. Increased Plasma Neurotensin Concentrations in Patients with Parkinson's Disease J. Neurol., Neurosurg. Psychiatry 2001, 70, 784-786
4. Alifano, M.; Souaze, F.; Dupouy, S.; Camilleri-Broet, S.; Younes, M.; Ahmed-Zaid, S. M.; Takahashi, T.; Cancellieri, A.; Damiani, S.; Boaron, M. Neurotensin Receptor 1 Determines the Outcome of Non-Small Cell Lung Cancer Clin. Cancer. Res. 2010, 16, 4401-4410
5. Griebel, G.; Holsboer, F. Neuropeptide Receptor Ligands as Drugs for Psychiatric Diseases: The End of the Beginning? Nat. Rev. Drug Discovery 2012, 11, 462-478
6. Kitabgi, P. Targeting Neurotensin Receptors with Agonists and Antagonists for Therapeutic Purposes Curr. Opin. Drug Discovery Dev. 2002, 5, 764-776
7. Venkatakrishnan, A. J.; Deupi, X.; Lebon, G.; Tate, C. G.; Schertler, G. F.; Babu, M. M. Molecular Signatures of G-Protein-Coupled Receptors Nature 2013, 494, 185-194
8. Rasmussen, S. G. F.; DeVree, B. T.; Zou, Y. Z.; Kruse, A. C.; Chung, K. Y.; Kobilka, T. S.; Thian, F. S.; Chae, P. S.; Pardon, E.; Calinski, D. Crystal Structure of the Beta(2) Adrenergic Receptor-Gs Protein Complex Nature 2011, 477, 549-555
9. Haga, K.; Kruse, A. C.; Asada, H.; Yurugi-Kobayashi, T.; Shiroishi, M.; Zhang, C.; Weis, W. I.; Okada, T.; Kobilka, B. K.; Haga, T. Structure of the Human M2Muscarinic Acetylcholine Receptor Bound to an Antagonist Nature 2012, 482, 547-551
10. Cherezov, V.; Rosenbaum, D. M.; Hanson, M. A.; Rasmussen, S. G.; Thian, F. S.; Kobilka, T. S.; Choi, H. J.; Kuhn, P.; Weis, W. I.; Kobilka, B. K. High-Resolution Crystal Structure of an Engineered Human Beta2-Adrenergic G Protein-Coupled Receptor Science 2007, 318, 1258-1265
11. Tehan, B. G.; Bortolato, A.; Blaney, F. E.; Weir, M. P.; Mason, J. S. Unifying Family a GPCR Theories of Activation Pharmacol. Ther. 2014, 143, 51-60
12. Dror, R. O.; Jensen, M. O.; Borhani, D. W.; Shaw, D. E. Exploring Atomic Resolution Physiology on a Femtosecond to Millisecond Timescale Using Molecular Dynamics Simulations J. Gen. Physiol. 2010, 135, 555-562
13. Ballesteros, J. A.; Weinstein, H. Integrated Methods for the Construction of Three-Dimensional Models and Computational Probing of Structure-Function Relations in G Protein-Coupled Receptors. In Methods in Neurosciences; Stuart, C. S., Ed.; Academic Press: 1995; Vol. 25, pp 366-428.
14. Rasmussen, S. G.; Choi, H. J.; Fung, J. J.; Pardon, E.; Casarosa, P.; Chae, P. S.; Devree, B. T.; Rosenbaum, D. M.; Thian, F. S.; Kobilka, T. S. Structure of a Nanobody-Stabilized Active State of the Beta(2) Adrenoceptor Nature 2011, 469, 175-180
15. Rose, A. S.; Elgeti, M.; Zachariae, U.; Grubmuller, H.; Hofmann, K. P.; Scheerer, P.; Hildebrand, P. W. Position of Transmembrane Helix 6 Determines Receptor G Protein Coupling Specificity J. Am. Chem. Soc. 2014, 136, 11244-11247
16. White, J. F.; Noinaj, N.; Shibata, Y.; Love, J.; Kloss, B.; Xu, F.; Gvozdenovic-Jeremic, J.; Shah, P.; Shiloach, J.; Tate, C. G. Structure of the Agonist-Bound Neurotensin Receptor Nature 2012, 490, 508-513
17. Egloff, P.; Hillenbrand, M.; Klenk, C.; Batyuk, A.; Heine, P.; Balada, S.; Schlinkmann, K. M.; Scott, D. J.; Schutz, M.; Pluckthun, A. Structure of Signaling-Competent Neurotensin Receptor 1 Obtained by Directed Evolution in Escherichia Coli Proc. Natl. Acad. Sci. U.S.A. 2014, 111, E655-E662
18. Park, J. H.; Scheerer, P.; Hofmann, K. P.; Choe, H. W.; Ernst, O. P. Crystal Structure of the Ligand-Free G-Protein-Coupled Receptor Opsin Nature 2008, 454, 183-187
19. Choe, H. W.; Kim, Y. J.; Park, J. H.; Morizumi, T.; Pai, E. F.; Krauss, N.; Hofmann, K. P.; Scheerer, P.; Ernst, O. P. Crystal Structure of Metarhodopsin Ii Nature 2011, 471, 651-655
20. Shibata, Y.; White, J. F.; Serrano-Vega, M. J.; Magnani, F.; Aloia, A. L.; Grisshammer, R.; Tate, C. G. Thermostabilization of the Neurotensin Receptor NTS1 J. Mol. Biol. 2009, 390, 262-277
21. Shaw, D. E.; Dror, R. O.; Salmon, J. K.; Grossman, J. P.; Mackenzie, K. M.; Bank, J. A.; Young, C.; Deneroff, M. M.; Batson, B.; Bowers, K. J.; Millisecond-Scale Molecular Dynamics Simulations on Anton. In Proceedings of the Conference on High Performance Computing Networking, Storage and Analysis; ACM: Portland, OR, 2009; pp 1-11.
22. Eswar, N.; Webb, B.; Marti-Renom, M. A.; Madhusudhan, M. S.; Eramian, D.; Shen, M. Y.; Pieper, U.; Sali, A. Comparative Protein Structure Modeling Using Modeller. Curr. Protoc. Bioinf. 2006, Chapter 5, Unit 5-6.
23. Marti-Renom, M. A.; Stuart, A. C.; Fiser, A.; Sanchez, R.; Melo, F.; Sali, A. Comparative Protein Structure Modeling of Genes and Genomes Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325
24. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
25. Mackerell, A. D., Jr.; Feig, M.; Brooks, C. L., III. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
26. Beglov, D.; Roux, B. Finite Representation of an Infinite Bulk System-Solvent Boundary Potential for Computer-Simulations J. Chem. Phys. 1994, 100, 9050-9063
27. Klauda, J. B.; Venable, R. M.; Freites, J. A.; O'Connor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerell, A. D., Jr.; Pastor, R. W. Update of the Charmm All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types J. Phys. Chem. B 2010, 114, 7830-7843
28. Shaw, D. E.; Maragakis, P.; Lindorff-Larsen, K.; Piana, S.; Dror, R. O.; Eastwood, M. P.; Bank, J. A.; Jumper, J. M.; Salmon, J. K.; Shan, Y. Atomic-Level Characterization of the Structural Dynamics of Proteins Science 2010, 330, 341-346
29. Krautler, V.; Van Gunsteren, W. F.; Hunenberger, P. H. A Fast Shake: Algorithm to Solve Distance Constraint Equations for Small Molecules in Molecular Dynamics Simulations J. Comput. Chem. 2001, 22, 501-508
30. Shan, Y.; Klepeis, J. L.; Eastwood, M. P.; Dror, R. O.; Shaw, D. E. Gaussian Split Ewald: A Fast Ewald Mesh Method for Molecular Simulation J. Chem. Phys. 2005, 122, 54101-54113
31. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. Gromacs: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718
32. Niesen, M. J.; Bhattacharya, S.; Vaidehi, N. The Role of Conformational Ensembles in Ligand Recognition in G-Protein Coupled Receptors J. Am. Chem. Soc. 2011, 133, 13197-13204
33. Hildebrand, P. W.; Gunther, S.; Goede, A.; Forrest, L.; Frommel, C.; Preissner, R. Hydrogen-Bonding and Packing Features of Membrane Proteins: Functional Implications Biophys. J. 2008, 94, 1945-1953
34. Zhou, F. X.; Cocco, M. J.; Russ, W. P.; Brunger, A. T.; Engelman, D. M. Interhelical Hydrogen Bonding Drives Strong Interactions in Membrane Proteins Nat. Struct. Biol. 2000, 7, 154-160
35. Shibata, Y.; Gvozdenovic-Jeremic, J.; Love, J.; Kloss, B.; White, J. F.; Grisshammer, R.; Tate, C. G. Optimising the Combination of Thermostabilising Mutations in the Neurotensin Receptor for Structure Determination Biochim. Biophys. Acta 2013, 1828, 1293-1301
36. Pardo, L.; Deupi, X.; Dolker, N.; Lopez-Rodriguez, M. L.; Campillo, M. The Role of Internal Water Molecules in the Structure and Function of the Rhodopsin Family of G Protein-Coupled Receptors ChemBioChem 2007, 8, 19-24
37. Gutierrez-de-Teran, H.; Massink, A.; Rodriguez, D.; Liu, W.; Han, G. W.; Joseph, J. S.; Katritch, I.; Heitman, L. H.; Xia, L.; Ijzerman, A. P. The Role of a Sodium Ion Binding Site in the Allosteric Modulation of the a(2a) Adenosine G Protein-Coupled Receptor Structure 2013, 21, 2175-2185
38. 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. Structural Basis for Allosteric Regulation of GPCRs by Sodium Ions Science 2012, 337, 232-236
39. Miller-Gallacher, J. L.; Nehme, R.; Warne, T.; Edwards, P. C.; Schertler, G. F.; Leslie, A. G.; Tate, C. G. The 2.1 A Resolution Structure of Cyanopindolol-Bound Beta1-Adrenoceptor Identifies an Intramembrane Na+ Ion That Stabilises the Ligand-Free Receptor PLoS One 2014, 9, e92727
40. 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. High-Resolution Crystal Structure of Human Protease-Activated Receptor 1 Nature 2012, 492, 387-392
41. Fenalti, G.; Giguere, P. M.; Katritch, V.; Huang, X. P.; Thompson, A. A.; Cherezov, V.; Roth, B. L.; Stevens, R. C. Molecular Control of Delta-Opioid Receptor Signalling Nature 2014, 506, 191-196
42. Wu, B.; Chien, E. Y.; Mol, C. D.; Fenalti, G.; Liu, W.; Katritch, V.; Abagyan, R.; Brooun, A.; Wells, P.; Bi, F. C. Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists Science 2010, 330, 1066-1071
43. Niesen, M. J.; Bhattacharya, S.; Grisshammer, R.; Tate, C. G.; Vaidehi, N. Thermostabilization of the Beta1-Adrenergic Receptor Correlates with Increased Entropy of the Inactive State J. Phys. Chem. B 2013, 117, 7283-7291
44. Lee, S.; Bhattacharya, S.; Grisshammer, R.; Tate, C.; Vaidehi, N. Dynamic Behavior of the Active and Inactive States of the Adenosine a(2a) Receptor J. Phys. Chem. B 2014, 118, 3355-3365
45. Magnani, F.; Shibata, Y.; Serrano-Vega, M. J.; Tate, C. G. Co-Evolving Stability and Conformational Homogeneity of the Human Adenosine A2a Receptor Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 10744-10749