Electron crystallography reveals the structure of metarhodopsin I

EMBO Journal

Volumn 23, Issue 18, 2004, Pages 3609-3620

  Ruprecht, Jonathan J ^a   Mielke, Thorsten ^a,c   Vogel, Reiner ^b   Villa, Claudio ^a   Schertler, Gebhard F X ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Electron crystallography; G protein coupled receptor; Membrane protein; Metarhodopsin I; Visual pigment

Indexed keywords

BETA IONONE; CHOLESTEROL; G PROTEIN COUPLED RECEPTOR; RHODOPSIN; TRYPTOPHAN;

ARTICLE; BLEACHING; CHROMATOPHORE; CONFORMATIONAL TRANSITION; LIGHT ABSORPTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; RETINA; VISION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CATTLE; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION; RHODOPSIN; ROD OUTER SEGMENTS;

EID: 5044235587     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600374     Document Type: Article

References (61)

1. Altenbach C, Yang K, Farrens DL, Farahbakhsh ZT, Khorana HG, Hubbell WL (1996) Structural features and light-dependent changes in the cytoplasmic interhelical E-F loop region of rhodopsin: a site-directed spin-labeling study. Biochemistry 35: 12470-12478
2. Arnis S, Hofmann KP (1993) Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proc Natl Acad Sci USA 90: 7849-7853
3. Baldwin JM, Schertler GF, Unger VM (1997) An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J Mol Biol 272: 144-164
4. Baldwin PA, Hubbell WL (1985) Effects of lipid environment on the light-induced conformational changes of rhodopsin. 1. Absence of metarhodopsin II production in dimyristoylphosphatidylcholine recombinant membranes. Biochemistry 24: 2624-2632
5. Beck M, Sakmar TP, Siebert F (1998) Spectroscopic evidence for interaction between transmembrane helices 3 and 5 in rhodopsin. Biochemistry 37: 7630-7639
6. Bockaert J, Pin JP (1999) Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18: 1723-1729
7. Borhan B, Souto ML, Imai H, Shichida Y, Nakanishi K (2000) Movement of retinal along the visual transduction path. Science 288: 2209-2212
8. Bullough PA, Henderson R (1987) Use of spot scan procedure for recording low-dose micrographs of beam sensitive specimens. Ultramicroscopy 21: 223-230
9. Butt HJ, Wang DN, Hansma PK, Kühlbrandt W (1991) Effect of surface roughness of carbon support films on high-resolution electron diffraction of two-dimensional protein crystals. Ultramicroscopy 36: 307-318
10. Cai K, Langen R, Hubbell WL, Khorana HG (1997) Structure and function in rhodopsin: topology of the C-terminal polypeptide chain in relation to the cytoplasmic loops. Proc Natl Acad Sci USA 94: 14267-14272
11. Caspar DLD, Kirschner DA (1971) Myelin membrane structure at 10 Å resolution. Nat New Biol 231: 46-52
12. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763
13. Crowther RA, Henderson R, Smith JM (1996) MRC image processing programs. J Struct Biol 116: 9-16
14. Ernst OP, Meyer CK, Marin EP, Henklein P, Fu WY, Sakmar TP, Hofmann KP (2000) Mutation of the fourth cytoplasmic loop of rhodopsin affects binding of transducin and peptides derived from the carboxyl-terminal sequences of transducin alpha and gamma subunits. J Biol Chem 275: 1937-1943
15. Franke RR, Konig B, Sakmar TP, Khorana HG, Hofmann KP (1990) Rhodopsin mutants that bind but fail to activate transducin. Science 250: 123-125
16. Franke RR, Sakmar TP, Graham RM, Khorana HG (1992) Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin. J Biol Chem 267: 14767-14774
17. Franks NP, Lieb WR (1979) The structure of lipid bilayers and the effects of general anaesthetics. An X-ray and neutron diffraction study. J Mol Biol 133: 469-500
18. 5,6F motif in the rhodopsin ground state and during activation. Proc Natl Acad Sci USA 100: 2290-2295
19. Fujiyoshi Y (1998) The structural study of membrane proteins by electron crystallography. Adv Biophys 35: 25-80
20. Havelka WA, Henderson R, Oesterhelt D (1995) Three-dimensional structure of halorhodopsin at 7 Å resolution. J Mol Biol 247: 726-738
21. Henderson R, Baldwin JM, Ceska TA, Zemlin F, Beckmann E, Downing KH (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213: 899-929
22. Henderson R, Baldwin JM, Downing KH, Lepault J, Zemlin F (1986) Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5 Å resolution. Ultramicroscopy 19: 147-178
23. Hubbell WL, Altenbach C, Hubbel CM, Khorana HG (2003) Rhodopsin structure, dynamics, and activation: a perspective from crystallography, site-directed spin labeling, sulfhydryl reactivity, and disulfide cross-linking. Adv Protien Chem 63 243-290
24. Imai H, Mizukami T, Imamoto Y, Shicida Y (1994) Direct observation of the thermal equilibria among lumirhodopsin, metarhodopsin I, and metarhodopsin II in chicken rhodopsin. Biochemistry 33: 14351-14358
25. Jones TA, Zou JY, Cowan SW, Kjeldgaard (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47 (Part 2): 110-119
26. Kim JE, Pan D, Mathies RA (2003) Picosecond dynamics of G-protein coupled receptor activation in rhodopsin from time-resolved UV resonance Raman spectroscopy. Biochemistry 42: 5169-5175
27. Kito Y, Suzuki T, Azuma M, Sekoguti Y (1968) Absorption spectrum of rhodopsin denatured with acid. Nature 218: 955-957
28. Kochendoerfer GG, Kaminaka S, Mathies RA (1997) Ultraviolet resonance Raman examination of the light-induced protein structural changes in rhodopsin activation. Biochemistry 36: 13153-13159
29. Krebs A, Edwards PC, Villa C, Li J, Schertler GF (2003) The three-dimensional structure of bovine rhodopsin determined by electron cryomicroscopy. J Biol Chem 278: 50217-50225
30. Krebs A, Villa C, Edwards PC, Schertler GF (1998) Characterisation of an improved two-dimensional p22121 crystal from bovine rhodopsin. J Mol Biol 282: 991-1003
31. Kühn H, Mommertz O, Hargrave PA (1982) Light-dependent conformational change at rhodopsin's cytoplasmic surface detected by increased susceptibility to proteolysis. Biochim Biophys Acta 679: 95-100
32. Lamola AA, Yamane T, Zipp A (1974) Effects of detergents and high pressures upon the metarhodopsin I-metarhodopsin II equilibrium. Biochemistry 13: 738-745
33. Lewis JW, Kliger DS (1992) Photointermediates of visual pigments. J Bioenerg Biomembr 24: 201-210
34. Lewis JW, van Kuijk FJ, Carruthers JA, Kliger DS (1997) Metarhodopsin III formation and decay kinetics: comparison of bovine and human rhodopsin. Vis Res 37: 1-8
35. Lin SW, Sakmar TP (1996) Specific tryptophan UV-absorbance changes are probes of the transition of rhodopsin to its active state. Biochemistry 35: 11149-11159
36. Marin EP, Krishna AG, Zvyaga TA, Isele J, Siebert F, Sakmar TP (2000) The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. J Biol Chem 275: 1930-1936
37. Marr K, Peters KS (1991) Photoacoustic calorimetric study of the conversion of rhodopsin and isorhodopsin to lumirhodopsin. Biochemistry 30: 1254-1258
38. Matthews RG, Hubbard R, Brown PK, Wald G (1963) Tautomeric forms of metarhodopsin. J Gen Physiol 47: 215-240
39. Menon ST, Han M, Sakmar TP (2001) Rhodopsin: structural basis of molecular physiology. Physiol Rev 81: 1659-1688
40. Mielke T, Alexiev U, Glasel M, Otto H, Heyn MP (2002a) Light-induced changes in the structure and accessibility of the cytoplasmic loops of rhodopsin in the activated MII state. Biochemistry 41: 7875-7884
41. Mielke T, Villa C, Edwards PC, Schertler GF, Heyn MP (2002b) X-ray diffraction of heavy-atom labelled two-dimensional crystals of rhodopsin identifies the position of cysteine 140 in helix 3 and cysteine 316 in helix 8. J Mol Biol 316: 693-709
42. Mitchell DC, Straume M, Litman BJ (1992) Role of sn-1-saturated,sn-2- polyunsaturated phospholipids in control of membrane receptor conformational equilibrium: effects of cholesterol and acyl chain unsaturation on the metarhodopsin I metarhodopsin II equilibrium. Biochemistry 31: 662-670
43. Mitchell DC, Straume M, Miller JL, Litman BJ (1990) Modulation of metarhodopsin formation by cholesterol-induced ordering of bilayer lipids. Biochemistry 29: 9143-9149
44. Okada T, Fujiyoshi Y, Silow M, Navarro J, Landau EM, Shichida Y (2002) Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography. Proc Natl Acad Sci USA 99: 5982-5987
45. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure, of rhodopsin: a G protein-coupled receptor. Science 289: 739-745
46. Resek JF, Farahbakhsh ZT, Hubbell WL, Khorana HG (1993) Formation of the meta II photointermediate is accompanied by conformational changes in the cytoplasmic surface of rhodopsin. Biochemistry 32: 12025-12032
47. Scherter GF, Hargrave PA (1995) Projection structure of frog rhodopsin in two crystal forms. Proc Natl Acad Sci USA 92: 11578-11582
48. Schertler GF, Villa C, Henderson R (1993) Projection structure of rhodopsin. Nature 362: 770-772
49. Shaw PJ, Hills GJ (1981) Tilted specimen in the electron microscope-a simple specimen holder and the calculation of tilt angles for crystalline specimens. Micron 12: 279-282
50. Spooner PJ, Sharples JM, Goodall SC, Seedorf H, Verhoeven MA, Lugtenburg J, Bovee-Geurts PH, DeGrip WJ, Watts A (2003) Conformational similarities in the beta-ionone ring region of the rhodopsin chromophore in its ground state and after photoactivation to the metarhodopsin-I intermediate. Biochemistry 42: 13371-13378
51. Teller DC, Okada T, Behnke CA, Palczewski K, Stenkamp RE (2001) Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry 40: 7761-7772
52. Thorgeirsson TE, Lewis JW, Wallace-Williams SE, Kliger DS (1992) Photolysis of rhodopsin results in deprotonation of its retinal Schiffs base prior to formation of metarhodopsin II. Photochem Photobiol 56: 1135-1144
53. Unger VM, Hargrave PA, Baldwin JM, Schertler GF (1997) Arrangement of rhodopsin transmembrane alpha-helices. Nature 389: 203-206
54. Unger VM, Schertler GF (1995) Low resolution structure of bovine rhodopsin determined by electron cryo-microscopy. Biophys J 68: 1776-1786
55. Vogel R, Ruprecht J, Villa C, Mielke T, Schertler GF, Siebert F (2004) Rhodopsin photoproducts in 2D crystals. J Mol Biol 338: 597-609
56. Vogel R, Siebert F (2002) Conformation and stability of alpha-helical membrane proteins. 2. Influence of pH and salts on stability and unfolding of rhodopsin. Biochemistry 41: 3536-3545
57. Vogel R, Siebert F, Mathias G, Tavan P, Fan G, Sheves M (2003) Deactivation of rhodopsin in the transition from the signaling state meta II to meta III involves a thermal isomerization of the retinal chromophore C = N double bond. Biochemistry 42: 9863-9874
58. Vonck J (2000) Parameters affecting specimen flatness of two-dimensional crystals for electron crystallography. Ultramicroscopy 85: 123-129
59. Wald G (1968) Molecular basis of visual excitation. Science 162: 230-239
60. Yan EC, Kazmi MA, Ganim Z, Hou JM, Pan D, Chang BS, Sakmar TP, Mathies RA (2003) Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc Natl Acad Sci USA 100: 9262-9267
61. Yoshizawa T, Wald G (1963) Pre-lumirhodopsin and the bleaching of visual pigments. Nature 197: 1279-1286