Membrane-sensitive conformational states of helix 8 in the metabotropic Glu2 receptor, a class C GPCR

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Bruno, Agostino ^a,b   Costantino, Gabriele ^b   de Fabritiis, Gianni ^a   Pastor, Manuel ^a   Selent, Jana ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; METABOTROPIC RECEPTOR 2;

ARTICLE; CONFORMATIONAL TRANSITION; DEPLETION; HELIX 8; LIPID MEMBRANE; MEMBRANE; MEMBRANE COMPONENT; MOLECULAR DYNAMICS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE;

CELL MEMBRANE; CHOLESTEROL; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84864751433     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042023     Document Type: Article

References (69)

1. Deupi X, Kobilka BK, (2010) Energy landscapes as a tool to integrate GPCR structure, dynamics and function. Physiology (Bethesda) 25: 293-303.
2. Katritch V, Cherezov V, Stevens RC, (2011) Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci. 33: 17-27.
3. Monnier C, Tu H, Bourrier E, Vol C, Lamarque L, et al. (2010) Trans-activation between 7TM domains: implication in heterodimeric GABAB receptor activation. Embo J. 30: 32-42.
4. Kniazeff J, Prézeau L, Rondard P, Pin J-P, Goudet C, (2011) Dimers and beyond: The functional puzzles of class C GPCRs. Pharmacol. Ther. 130: 9-25.
5. Rondard P, Goudet C, Kniazeff J, Pin J-P, Prézeau L, (2011) The complexity of their activation mechanism opens new possibilities for the modulation of mGlu and GABAB class C G protein-coupled receptors. Neuropharmacol. 60: 82-92.
6. Binet V, Duthey B, Lecaillon J, Vol C, Quoyer J, et al. (2007) Common Structural Requirements for Heptahelical Domain Function in Class A and Class C G Protein-coupled Receptors. J. Biol. Chem. 282: 12154-12163.
7. Goudet C, Gaven F, Kniazeff J, Vol C, Liu J, et al. (2004) Heptahelical domain of metabotropic glutamate receptor 5 behaves like rhodopsin-like receptors. Proceed. Natl. Acad. Sci. U.S.A. 101: 378-383.
8. Binet V, Brajon C, Le Corre L, Acher F, Pin J-P, et al. (2004) The Heptahelical Domain of GABAB2 Is Activated Directly by CGP7930, a Positive Allosteric Modulator of the GABAB Receptor. J. Biol. Chem. 279: 29085-29091.
9. Miedlich SU, Gama L, Seuwen K, Wolf RM, Breitwieser GE, (2004) Homology Modeling of the Transmembrane Domain of the Human Calcium Sensing Receptor and Localization of an Allosteric Binding Site. J. Biol. Chem. 279: 7254-7263.
10. Lundström L, Bissantz C, Beck J, Wettstein JG, Woltering TJ, et al. (2011) Structural determinants of allosteric antagonism at metabotropic glutamate receptor 2: mechanistic studies with new potent negative allosteric modulators. Br. J. Pharmacol. 164: 521-537.
11. Gonzalez-Maeso J, Ang RL, Yuen T, Chan P, Weisstaub NV, et al. (2008) Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature 452: 93-97.
12. Javitt DC, (2010) Glutamatergic theories of schizophrenia. Isr J. Psychiatry Relat. Sci. 47: 4-16.
13. Spooren W, Lesage A, Lavreysen H, Gasparini F, Steckler T, (2010) Metabotropic glutamate receptors: their therapeutic potential in anxiety. Curr. Top. Behav. Neurosci. 2: 391-413.
14. Fribourg M, Moreno JL, Holloway T, Provasi D, Baki L, et al. (2011) Decoding the Signaling of a GPCR Heteromeric Complex Reveals a Unifying Mechanism of Action of Antipsychotic Drugs. Cell 147: 1011-1023.
15. Moreno JL, Holloway T, Albizu L, Sealfon SC, González-Maeso J, (2011) Metabotropic glutamate mGlu2 receptor is necessary for the pharmacological and behavioral effects induced by hallucinogenic 5-HT2A receptor agonists. Neurosci. Lett. 493: 76-79.
16. Bruno A, Guadix AE, Costantino G, (2009) Molecular Dynamics Simulation of the Heterodimeric mGluR2/5HT2A Complex. An Atomistic Resolution Study of a Potential New Target in Psychiatric Conditions. J. Chem. Inf. Model. 49: 1602-1616.
17. Bruno A, Beato C, Costantino G, (2011) Molecular dynamics simulations and docking studies on 3D models of the heterodimeric and homodimeric 5-HT(2A) receptor subtype. Future Med Chem 3: 665-681.
18. Wess J, Han S-J, Kim S-K, Jacobson KA, Li JH, (2008) Conformational changes involved in G-protein-coupled-receptor activation. Trends Pharmacol. Sci. 29: 616-625.
19. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SGF, Thian FS, et al. (2007) High-Resolution Crystal Structure of an Engineered Human β2-Adrenergic G Protein-Coupled Receptor. Science 318: 1258-1265.
20. Jaakola V-P, Griffith MT, Hanson MA, Cherezov V, Chien EYT, et al. (2008) The 2.6 Angstrom Crystal Structure of a Human A2A Adenosine Receptor Bound to an Antagonist. Science 322: 1211-1217.
21. Warne T, Serrano-Vega MJ, Baker JG, Moukhametzianov R, Edwards PC, et al. (2008) Structure of a [bgr]1-adrenergic G-protein-coupled receptor. Nature 454: 486-491.
22. Chien EYT, Liu W, Zhao Q, Katritch V, Won Han G, et al. (2010) Structure of the Human Dopamine D3 Receptor in Complex with a D2/D3 Selective Antagonist. Science 330: 1091-1095.
23. Wu B, Chien EYT, Mol CD, Fenalti G, Liu W, et al. (2010) Structures of the CXCR4 Chemokine GPCR with Small-Molecule and Cyclic Peptide Antagonists. Science 330: 1066-1071.
24. Rasmussen SGF, Choi H-J, Fung JJ, Pardon E, Casarosa P, et al. (2011) Structure of a nanobody-stabilized active state of the [bgr]2 adrenoceptor. Nature 469: 175-180.
25. Rasmussen SGF, DeVree BT, Zou Y, Kruse AC, Chung KY, et al. (2011) Crystal structure of the [bgr]2 adrenergic receptor-Gs protein complex. Nature 477: 549-555.
26. Shimamura T, Shiroishi M, Weyand S, Tsujimoto H, Winter G, et al. (2011) Structure of the human histamine H1 receptor complex with doxepin. Nature 475: 65-70.
27. Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M, et al. (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482: 547-551.
28. Kaye RG, Saldanha JW, Lu Z-L, Hulme EC, (2011) Helix 8 of the M1 Muscarinic Acetylcholine Receptor: Scanning Mutagenesis Delineates a G Protein Recognition Site. Mol. Pharmacol. 79: 701-709.
29. Tiburu EK, Tyukhtenko S, Zhou H, Janero DR, Struppe J, et al. (2011) Human Cannabinoid 1 GPCR C-Terminal Domain Interacts with Bilayer Phospholipids to Modulate the Structure of its Membrane Environment. AAPS J 13: 92-98.
30. Kuwasako K, Kitamura K, Nagata S, Hikosaka T, Kato J, (2011) Structure-function analysis of helix 8 of human calcitonin receptor-like receptor within the adrenomedullin 1 receptor. Peptides 32: 144-149.
31. Fotiadis D, Liang Y, Filipek S, Saperstein DA, Engel A, et al. (2003) Atomic-force microscopy: Rhodopsin dimers in native disc membranes. Nature 421: 127-128.
32. Liang Y, Fotiadis D, Filipek S, Saperstein DA, Palczewski K, et al. (2003) Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278: 21655-21662.
33. Guo W, Urizar E, Kralikova M, Mobarec JC, Shi L, et al. (2008) Dopamine D2 receptors form higher order oligomers at physiological expression levels. Embo J. 27: 2293-2304.
34. Ahn KH, Nishiyama A, Mierke DF, Kendall DA, (2010) Hydrophobic Residues in Helix 8 of Cannabinoid Receptor 1 Are Critical for Structural and Functional Properties. Biochemistry 49: 502-511.
35. Dowal L, Sim DS, Dilks JR, Blair P, Beaudry S, et al. (2011) Identification of an antithrombotic allosteric modulator that acts through helix 8 of PAR1. Proceed. Natl. Acad. Sci. U.S.A. 108: 2951-2956.
36. Kirchberg K, Kim T-Y, Möller M, Skegro D, Dasara Raju G, et al. (2011) Conformational dynamics of helix 8 in the GPCR rhodopsin controls arrestin activation in the desensitization process. Proceed. Natl. Acad. Sci. U.S.A. 108: 18690-18695.
37. Liu JJ, Horst R, Katritch V, Stevens RC, Wüthrich K, (2012) Biased Signaling Pathways in β2-Adrenergic Receptor Characterized by 19F-NMR. Science 235: 1106-1110.
38. Olausson BES, Grossfield A, Pitman MC, Brown MF, Feller SE, et al. (2012) Molecular dynamics simulations reveal specific interactions of post-translational palmitoyl modifications with rhodopsin in membranes. J. Am. Chem. Soc. 134: 4324-4331.
39. Pin JP, Joly C, Heinemann SF, Bockaert J, (1994) Domains involved in the specificity of G protein activation in phospholipase C-coupled metabotropic glutamate receptors. Embo J 13: 342-348.
40. El Far O, Bofill-Cardona E, Airas JM, O'Connor V, Boehm S, et al. (2001) Mapping of calmodulin and Gbetagamma binding domains within the C-terminal region of the metabotropic glutamate receptor 7A. J. Biol. Chem. 276: 30662-30669.
41. Pin J-P, Kniazeff J, Goudet C, Bessis A-S, Liu J, et al. (2004) The activation mechanism of class-C G-protein coupled receptors. Biol. Cell 96: 335-342.
42. Parker MS, Parker SL, (2010) The fourth intracellular domain of G-protein coupling receptors: helicity, basicity and similarity to opsins. Amino Acids 38: 1-13.
43. Vanejevs M, Jatzke C, Renner S, Müller S, Hechenberger M, et al. (2008) Positive and negative modulation of group I metabotropic glutamate receptors. J. Med. Chem. 51: 634-647.
44. Michino M, Abola E, Brooks CL 3rd, Dixon JS, Moult J, et al (2009) Community-wide assessment of GPCR structure modelling and ligand docking: GPCR Dock 2008. Nat. Rev. Drug Discov. 8: 455-463.
45. Mobarec JC, Sanchez R, Filizola M, (2009) Modern Homology Modeling of G-Protein Coupled Receptors: Which Structural Template to Use? J. Med. Chem. 52: 5207-5216.
46. Costanzi S, (2010) Modeling G Protein-Coupled Receptors: a Concrete Possibility. Chim. Oggi 28: 26-31.
47. Kufareva I, Rueda M, Katritch V, Stevens RC, Abagyan R, (2011) Status of GPCR modeling and docking as reflected by community-wide GPCR Dock 2010 assessment. Structure 19: 1108-1126.
48. Obiol-Pardo C, López L, Pastor M, Selent J, (2011) Progress in the structural prediction of G protein-coupled receptors: D3 receptor in complex with eticlopride. Proteins 79: 1695-1703.
49. Harvey MJ, Giupponi G, Fabritiis GD, (2009) ACEMD: Accelerating Biomolecular Dynamics in the Microsecond Time Scale. J. Chem. Theory Comput. 5: 1632-1639.
50. Khelashvili G, Grossfield A, Feller SE, Pitman MC, Weinstein H, (2009) Structural and dynamic effects of cholesterol at preferred sites of interaction with rhodopsin identified from microsecond length molecular dynamics simulations. Proteins 76: 403-417.
51. Lyman E, Higgs C, Kim B, Lupyan D, Shelley JC, et al. (2009) A Role for a Specific Cholesterol Interaction in Stabilizing the Apo Configuration of the Human A2A Adenosine Receptor. Structure 17: 1660-1668.
52. Binder H, Gawrisch K, (2001) Effect of Unsaturated Lipid Chains on Dimensions, Molecular Order and Hydration of Membranes. J. Phys. Chem. B 105: 12378-12390.
53. Gamba Z, (2008) Effective potentials and electrostatic interactions in self-assembled molecular bilayers II: The case of biological membranes. J. Chem. Phys. 129: 215104.
54. Saiz L, Klein ML, (2001) Structural Properties of a Highly Polyunsaturated Lipid Bilayer from Molecular Dynamics Simulations. Biophys. J. 81: 204-216.
55. Mihailescu M, Soubias O, Worcester D, White SH, Gawrisch K, (2010) Structure and Dynamics of Cholesterol-Containing Polyunsaturated Lipid Membranes Studied by Neutron Diffraction and NMR. J. Membr. Biol. 239: 63-71.
56. Hanson MA, Cherezov V, Griffith MT, Roth CB, Jaakola V-P, et al. (2008) A Specific Cholesterol Binding Site Is Established by the 2.8 Å Structure of the Human [beta]2-Adrenergic Receptor. Structure 16: 897-905.
57. Ikonen E, (2008) Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9: 125-138.
58. Simons K, Ikonen E, (2000) How cells handle cholesterol. Science 290: 1721-1726.
59. Horváth I, Multhoff G, Sonnleitner A, Vígh L, (2008) Membrane-associated stress proteins: More than simply chaperones. Biochim. et Biophys. Acta, Biomembr. 1778: 1653-1664.
60. Eroglu C, Barres BA, (2010) Regulation of synaptic connectivity by glia. Nature 468: 223-231.
61. Kenakin T, (2002) Efficacy at G-protein-coupled receptors. Nat. Rev. Drug Discov. 1: 103-.
62. Stern CM, Mermelstein PG, (2010) Caveolin regulation of neuronal intracellular signaling. Cell Mol. Life Sci. 67: 3785-3795.
63. Eroglu Ç, Brügger B, Wieland F, Sinning I, (2003) Glutamate-binding affinity of Drosophila metabotropic glutamate receptor is modulated by association with lipid rafts. Proc. Natl. Acad. Sci. 100: 10219-10224.
64. Francesconi A, Kumari R, Zukin RS, (2009) Regulation of Group I Metabotropic Glutamate Receptor Trafficking and Signaling by the Caveolar/Lipid Raft Pathway. J. Neurosci. 29: 3590-3602.
65. Fredericks WJ, McGarvey T, Wang H, Lal P, Puthiyaveettil R, et al. (2011) The Bladder Tumor Suppressor Protein TERE1 (UBIAD1)Modulates Cell Cholesterol: Implications for Tumor Progression. DNA and Cell Biol. 30: 851-864.
66. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J. Mol. Graph. 14: 33-38, 27-28.
67. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: An N{dot operator}log(N) method for Ewald sums in large systems. J. Chem. Phys. 98: 10089.
68. Topiol S, Sabio M, (2009) X-ray structure breakthroughs in the GPCR transmembrane region. Biochem. Pharmacol. 78: 11-20.
69. Park PS-H, Sapra KT, Jastrzebska B, Maeda T, Maeda A, et al. (2009) Modulation of Molecular Interactions and Function by Rhodopsin Palmitylation. Biochemistry 48: 4294-4304.