Highly conserved tyrosine stabilizes the active state of rhodopsin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 46, 2010, Pages 19861-19866

  Goncalves, Joseph A ^a   South, Kieron ^b   Ahuja, Shivani ^a   Zaitseva, Ekaterina ^c   Opefi, Chikwado A ^b   Eilers, Markus ^a   Vogel, Reiner ^c   Reeves, Philip J ^b   Smith, Steven O ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF ESSEX   (United Kingdom)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

ERY motif; G protein coupled receptor; Solid state NMR spectroscopy

Indexed keywords

11 CIS RETINAL; ALANINE; ARGININE; G PROTEIN COUPLED RECEPTOR; GLUTAMINE; HISTONE H5; HISTONE H6; HISTONE H7; LEUCINE; METHIONINE; OPSIN; RHODOPSIN; TRANSDUCIN; TYROSINE; UNCLASSIFIED DRUG; VISUAL PIGMENT;

CARBON NUCLEAR MAGNETIC RESONANCE; CHROMATOPHORE; CONFERENCE PAPER; CRYSTAL STRUCTURE; GENE MUTATION; ISOMERIZATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON TRANSPORT; SOLID STATE;

EID: 78650526380     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1009405107     Document Type: Article

References (40)

1. Ballesteros JA, 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.
2. Palczewski K, et al. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289:739-745.
3. Altenbach C, Kusnetzow AK, Ernst OP, Hofmann KP, Hubbell WL (2008) High-resolution distance mapping in rhodopsin reveals the pattern of helix movement due to activation. Proc Natl Acad Sci USA 105:7439-7444.
4. Farrens DL, Altenbach C, Yang K, Hubbell WL, Khorana HG (1996) Requirement of rigid-bodymotion of transmembrane helices for light activation ofrhodopsin. Science 274:768-770.
5. Lamola AA, Yamane T, Zipp A (1974) Effects of detergents and high-pressures upon metarhodopsin I ↔ metarhodopsin II equilibrium. Biochemistry 13:738-745.
6. Okada T, Palczewski K(2001)Crystal structure of rhodopsin:Implications for vision and beyond. Curr Opin Struct Biol 11:420-426.
7. Salom D, et al. (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc Natl Acad Sci USA 103:16123-16128.
8. Knierim B, Hofmann KP, Ernst OP, Hubbell WL (2007) Sequence of late molecular events in the activation of rhodopsin. Proc Natl Acad Sci USA 104:20290-20295.
9. Park JH, Scheerer P, Hofmann KP, Choe HW, Ernst OP (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454:183-187.
10. Jäger S, Palczewski K, Hofmann KP (1996) Opsin/all-trans-retinal complex activates transducin by different mechanisms than photolyzed rhodopsin. Biochemistry 35:2901-2908.
11. Vogel R, Siebert F (2001) Conformations of the active and inactive states of opsin. J Biol Chem 276:38487-38493.
12. Scheerer P, et al. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455:497-502.
13. Kisselev OG, et al. (1998) Light-activated rhodopsin induces a structural binding motif in G protein α subunit. Proc Natl Acad Sci USA 95:4270-4275.
14. Koenig BW, et al. (2002) Structure and orientation of a G protein fragment in the receptor bound state from residual dipolar couplings. J Mol Biol 322:441-461.
15. Fritze O, et al. (2003) Role of the conserved NPxxY(x)(5,6)F motif in the rhodopsin ground state and during activation. Proc Natl Acad Sci USA 100:2290-2295.
16. Ahuja S, et al. (2009) Location of the retinal chromophore in the activated state of rhodopsin. J Biol Chem 284:10190-10201.
17. Ahuja S, et al. (2009) Helix movement is coupled to displacement of the second extracellular loop in rhodopsin activation. Nat Struct Mol Biol 16:168-175.
18. Petkova AT, et al. (1999) Arginine activity in the proton-motive photocycle of bacteriorhodopsin: Solid-state NMR studies of the wild-type and D85N proteins. Biochemistry 38:1562-1572.
19. Farrens DL, Khorana HG (1995) Structure and function in rhodopsin. Measurement of the rate of metarhodopsin II decay by fluorescence spectroscopy. J Biol Chem 270:5073-5076.
20. Andres A, Garriga P, Manyosa J (2003) Altered functionality in rhodopsin point mutants associated with retinitis pigmentosa. Biochem Biophys Res Commun 303:294-301.
21. Hawtin SR(2005) Charged residues of the conserved DRY triplet of the vasopressin V1a receptor provide molecular determinants for cell surface delivery and internalization. Mol Pharmacol 68:1172-1182.
22. Auger GA, Pease JE, Shen XY, Xanthou G, Barker MD (2002) Alanine scanning mutagenesis of CCR3 reveals that the three intracellular loops are essential for functional receptor expression. Eur J Immunol 32:1052-1058.
23. Eilers M, Patel AB, Liu W, Smith SO (2002) Comparison of helix interactions in membrane and soluble α-bundle proteins. Biophys J 82:2720-2736.
24. Smith SO (2010) Structure and activation of the visual pigment rhodopsin. Annu Rev Biophys 39:309-328.
25. Imai H, et al. (1997) Single amino acid residue as a functional determinant of rod and cone visual pigments. Proc Natl Acad Sci USA 94:2322-2326.
26. Patel AB, et al. (2005) Changes in interhelical hydrogen bonding upon rhodopsin activation. J Mol Biol 347:803-812.
27. Janz JM, Farrens DL (2004) Role of the retinal hydrogen bond network in rhodopsin Schiff base stability and hydrolysis. J Biol Chem 279:55886-55894.
28. Sakmar TP, Franke RR, Khorana HG (1989) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci USA 86:8309-8313.
29. Ballesteros J, et al. (1998) Functional microdomains in G-protein-coupled receptors- the conserved arginine-cage motif in the gonadotropin-releasing hormone receptor. J Biol Chem 273:10445-10453.
30. Ballesteros JA, et al. (2001) 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 276:29171-29177.
31. 2a adenosine receptor bound to an antagonist. Science 322:1211-1217.
32. 1, -adrenergic G-protein-coupled receptor. Nature 454:486-491.
33. 2-adrenergic receptor function. Science 318:1266-1273.
34. 2-adrenergic receptor reconciles structural and biochemical observations. Proc Natl Acad Sci USA 106:4689-4694.
35. Baltensperger K, et al. (1996) The β-adrenergic receptor is a substrate for the insulin receptor tyrosine kinase. J Biol Chem 271:1061-1064.
36. Vogel R, et al. (2008) Functional role of the "ionic lock"-an interhelical hydrogen- bond network in family a heptahelical receptors. J Mol Biol 380:648-655.
37. Han M, Smith SO, Sakmar TP (1998) Constitutive activation of opsin by mutation of methionine 257 on transmembrane helix 6. Biochemistry 37:8253-8261.
38. 2-adrenergic receptor. Proc Natl Acad Sci USA 104:7027-7032.
39. Davidson FF, Loewen PC, Khorana HG (1994) Structure and function in rhodopsin: Replacement by alanine of cysteine residues 110 and 187, components of a conserved disulfide bond in rhodopsin, affects the light-activated metarhodopsin II state. Proc Natl Acad Sci USA 91:4029-4033.
40. Cohen GB, Oprian DD, Robinson PR (1992) Mechanism of activation and inactivation of opsin: Role of Glu113 and Lys296. Biochemistry 31:12592-12601.