The Molecular Switching Mechanism at the Conserved D(E)RY Motif in Class-A GPCRs

Biophysical Journal

Volumn 111, Issue 1, 2016, Pages 79-89

  Sandoval, Angelica ^a   Eichler, Stefanie ^b   Madathil, Sineej ^c   Reeves, Philip J ^d   Fahmy, Karim ^b   Böckmann, Rainer A ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^d UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LIPID BILAYER; PROTON;

AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; CONSERVED SEQUENCE; HYDROGEN BOND; LIPID BILAYER; LIPID METABOLISM; METABOLISM; MOLECULAR DYNAMICS; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL MEMBRANE; CONSERVED SEQUENCE; HYDROGEN BONDING; LIPID BILAYERS; LIPID METABOLISM; MOLECULAR DYNAMICS SIMULATION; PROTONS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84993945227     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2016.06.004     Document Type: Article

References (56)

1. 1 Lagerström, M.C., Schiöth, H.B., Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7 (2008), 339–357.
2. 2 Hofmann, K.P., Scheerer, P., et al., Ernst, O.P., A G protein-coupled receptor at work: the rhodopsin model. Trends Biochem. Sci. 34 (2009), 540–552.
3. 3 Palczewski, K., G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75 (2006), 743–767.
4. 4 Ballesteros, J.A., Jensen, A.D., et al., Javitch, J.A., Activation of the β2-adrenergic receptor involves disruption of an ionic lock between the cytoplasmic ends of transmembrane segments 3 and 6. J. Biol. Chem. 276 (2001), 29171–29177.
5. 5 Shi, L., Liapakis, G., et al., Javitch, J.A., β2 adrenergic receptor activation. Modulation of the proline kink in transmembrane 6 by a rotamer toggle switch. J. Biol. Chem. 277 (2002), 40989–40996.
6. 6 Dror, R.O., Arlow, D.H., et al., Shaw, D.E., Identification of two distinct inactive conformations of the β2-adrenergic receptor reconciles structural and biochemical observations. Proc. Natl. Acad. Sci. USA 106 (2009), 4689–4694.
7. 7 Sheikh, S.P., Zvyaga, T.A., et al., Bourne, H.R., Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F. Nature 383 (1996), 347–350.
8. 8 Arnis, S., Fahmy, K., et al., Sakmar, T.P., A conserved carboxylic acid group mediates light-dependent proton uptake and signaling by rhodopsin. J. Biol. Chem. 269 (1994), 23879–23881.
9. 9 Mahalingam, M., Martínez-Mayorga, K., et al., Vogel, R., Two protonation switches control rhodopsin activation in membranes. Proc. Natl. Acad. Sci. USA 105 (2008), 17795–17800.
10. 10 Vogel, R., Mahalingam, M., et al., Sakmar, T.P., Functional role of the “ionic lock”—an interhelical hydrogen-bond network in family A heptahelical receptors. J. Mol. Biol. 380 (2008), 648–655.
11. 11 Vogel, R., Sakmar, T.P., et al., Siebert, F., Coupling of protonation switches during rhodopsin activation. Photochem. Photobiol. 83 (2007), 286–292.
12. 12 Yan, E.C., Kazmi, M.A., et al., Mathies, R.A., Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. USA 100 (2003), 9262–9267.
13. 13 Jäger, F., Fahmy, K., et al., Siebert, F., Identification of glutamic acid 113 as the Schiff base proton acceptor in the metarhodopsin II photointermediate of rhodopsin. Biochemistry 33 (1994), 10878–10882.
14. 14 Standfuss, J., Edwards, P.C., et al., Schertler, G.F., The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471 (2011), 656–660.
15. 15 Farrens, D.L., Altenbach, C., et al., Khorana, H.G., Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274 (1996), 768–770.
16. 16 Herrmann, R., Heck, M., et al., Ernst, O.P., Sequence of interactions in receptor-G protein coupling. J. Biol. Chem. 279 (2004), 24283–24290.
17. 17 Knierim, B., Hofmann, K.P., et al., Hubbell, W.L., Sequence of late molecular events in the activation of rhodopsin. Proc. Natl. Acad. Sci. USA 104 (2007), 20290–20295.
18. 18 Fahmy, K., Siebert, F., Sakmar, T.P., Photoactivated state of rhodopsin and how it can form. Biophys. Chem. 56 (1995), 171–181.
19. 19 Dizhoor, A.M., Woodruff, M.L., et al., Fain, G.L., Night blindness and the mechanism of constitutive signaling of mutant G90D rhodopsin. J. Neurosci. 28 (2008), 11662–11672.
20. 20 Cohen, G.B., Yang, T., et al., Oprian, D.D., Constitutive activation of opsin: influence of charge at position 134 and size at position 296. Biochemistry 32 (1993), 6111–6115.
21. 21 Kim, J.-M., Altenbach, C., et al., Hubbell, W.L., Structure and function in rhodopsin: rhodopsin mutants with a neutral amino acid at E134 have a partially activated conformation in the dark state. Proc. Natl. Acad. Sci. USA 94 (1997), 14273–14278.
22. 22 Nygaard, R., Frimurer, T.M., et al., Schwartz, T.W., Ligand binding and micro-switches in 7TM receptor structures. Trends in Pharm. Sci. 30 (2009), 249–259.
23. 23 Madathil, S., Fahmy, K., Lipid protein interactions couple protonation to conformation in a conserved cytosolic domain of G protein-coupled receptors. J. Biol. Chem. 284 (2009), 28801–28809.
24. 24 Wolf, M.G., Hoefling, M., et al., Groenhof, G., g_membed: efficient insertion of a membrane protein into an equilibrated lipid bilayer with minimal perturbation. J. Comput. Chem. 31 (2010), 2169–2174.
25. 25 Jorgensen, W.L., Chandrasekhar, J., et al., Klein, M.L., Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983), 926–935.
26. 26 Pronk, S., Páll, S., et al., Lindahl, E., GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29 (2013), 845–854.
27. 27 Nosé, S., A unified formulation of the constant temperature molecular dynamics methods. J. Chem. Phys. 81 (1984), 511–519.
28. 28 Hoover, W.G., Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A Gen. Phys. 31 (1985), 1695–1697.
29. 29 Parrinello, M., Rahman, A., Polymorphic transitions in single crystals: a new molecular dynamics method. J. Appl. Phys. 52 (1981), 7182–7190.
30. 30 Hess, B., Bekker, H., et al., Fraaije, J.G.E.M., LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18 (1997), 1463–1472.
31. 31 Miyamoto, S., Kollman, P.A., SETTLE: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13 (1992), 952–962.
32. 32 Jämbeck, J.P.M., Lyubartsev, A.P., An extension and further validation of an all-atomistic force field for biological membranes. J. Chem. Theory Comput. 8 (2012), 2938–2948.
33. 33 Hornak, V., Abel, R., et al., Simmerling, C., Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins Struc. Func. Bioinf. 65 (2006), 712–725.
34. 34 Dickson, C.J., Madej, B.D., et al., Walker, R.C., Lipid14: the amber lipid force field. J. Chem. Theory Comput. 10 (2014), 865–879.
35. 35 Maier, J.A., Martinez, C., et al., Simmerling, C., ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput. 11 (2015), 3696–3713.
36. 36 Georgescu, R.E., Alexov, E.G., Gunner, M.R., Combining conformational flexibility and continuum electrostatics for calculating pK(a)s in proteins. Biophys. J. 83 (2002), 1731–1748.
37. 37 Alexov, E.G., Gunner, M.R., Incorporating protein conformational flexibility into the calculation of pH-dependent protein properties. Biophys. J. 72 (1997), 2075–2093.
38. a calculations with extensive side chain rotamer sampling. J. Comput. Chem. 30 (2009), 2231–2247.
39. 39 Krishnakumar, S.S., London, E., The control of transmembrane helix transverse position in membranes by hydrophilic residues. J. Mol. Biol. 374 (2007), 1251–1269.
40. 40 Castile, J.D., Taylor, K.M., Factors affecting the size distribution of liposomes produced by freeze-thaw extrusion. Int. J. Pharm. 188 (1999), 87–95.
41. 41 Standfuss, J., Xie, G., et al., Schertler, G.F., Crystal structure of a thermally stable rhodopsin mutant. J. Mol. Biol. 372 (2007), 1179–1188.
42. 42 Opefi, C.A., South, K., et al., Reeves, P.J., Retinitis pigmentosa mutants provide insight into the role of the N-terminal cap in rhodopsin folding, structure, and function. J. Biol. Chem. 288 (2013), 33912–33926.
43. 43 Rockland, L.B., Saturated salt solutions for static control of relative humidity between 5° and 40°C. Anal. Chem. 32 (1960), 1375–1376.
44. 44 Abusharkh, S.E., Erkut, C., et al., Fahmy, K., The role of phospholipid headgroup composition and trehalose in the desiccation tolerance of Caenorhabditis elegans. Langmuir 30 (2014), 12897–12906.
45. 45 Khesbak, H., Savchuk, O., et al., Fahmy, K., The role of water H-bond imbalances in B-DNA substate transitions and peptide recognition revealed by time-resolved FTIR spectroscopy. J. Am. Chem. Soc. 133 (2011), 5834–5842.
46. 46 Vivian, J.T., Callis, P.R., Mechanisms of tryptophan fluorescence shifts in proteins. Biophys. J. 80 (2001), 2093–2109.
47. 47 Choe, H.W., Kim, Y.J., et al., Ernst, O.P., Crystal structure of metarhodopsin II. Nature 471 (2011), 651–655.
48. 48 Park, J.H., Scheerer, P., et al., Ernst, O.P., Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454 (2008), 183–187.
49. 49 Scheerer, P., Park, J.H., et al., Ernst, O.P., Crystal structure of opsin in its G-protein-interacting conformation. Nature 455 (2008), 497–502.
50. 50 Palczewski, K., Kumasaka, T., et al., Miyano, M., Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 (2000), 739–745.
51. 51 Gleason, N.J., Vostrikov, V.V., et al., Koeppe, R.E. 2nd, Tyrosine replacing tryptophan as an anchor in GWALP peptides. Biochemistry 51 (2012), 2044–2053.
52. 52 Shahidullah, K., Krishnakumar, S.S., London, E., The effect of hydrophilic substitutions and anionic lipids upon the transverse positioning of the transmembrane helix of the ErbB2 (neu) protein incorporated into model membrane vesicles. J. Mol. Biol. 396 (2010), 209–220.
53. 53 Lew, S., Ren, J., London, E., The effects of polar and/or ionizable residues in the core and flanking regions of hydrophobic helices on transmembrane conformation and oligomerization. Biochemistry 39 (2000), 9632–9640.
54. 54 Borisovska, M., Schwarz, Y.N., et al., Bruns, D., Membrane-proximal tryptophans of synaptobrevin II stabilize priming of secretory vesicles. J. Neurosci. 32 (2012), 15983–15997.
55. 55 Fahmy, K., Sakmar, T.P., Siebert, F., Transducin-dependent protonation of glutamic acid 134 in rhodopsin. Biochemistry 39 (2000), 10607–10612.
56. 56 Lüdeke, S., Mahalingam, M., Vogel, R., Rhodopsin activation switches in a native membrane environment. Photochem. Photobiol. 85 (2009), 437–441.