Coupling efficiency of rhodopsin and transducin in bicelles

Biochemistry

Volumn 50, Issue 15, 2011, Pages 3193-3203

  Kaya, Ali I ^a   Thaker, Tarjani M ^b   Preininger, Anita M ^a   Iverson, T M ^a,b   Hamm, Heidi E ^a  

^a Department of Pharmacology ^*  (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BICELLES; COMPLEX FORMATIONS; COUPLING EFFICIENCY; EXTRACELLULAR STIMULI; FUNCTIONAL RECEPTORS; G PROTEIN; G PROTEIN ACTIVATION; G PROTEIN COUPLED RECEPTORS; GTP BINDING; HETEROTRIMERIC G PROTEINS; HIGH AFFINITY; IN-VIVO; MEMBRANE COMPOSITION; RATE-LIMITING STEPS; STRUCTURAL CHARACTERISTICS; TRANSDUCIN;

NUCLEOTIDES; PHOSPHOLIPIDS;

PROTEINS;

G PROTEIN COUPLED RECEPTOR; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPID; RHODOPSIN; TRANSDUCIN;

ARTICLE; BICELLE; BILAYER MEMBRANE; BINDING AFFINITY; CHEMICAL COMPOSITION; COMPLEX FORMATION; CONTROLLED STUDY; HALF LIFE TIME; IN VIVO STUDY; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MICELLE; MOLECULAR STABILITY; PRIORITY JOURNAL; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

BIOCATALYSIS; CELL MEMBRANE; DETERGENTS; HALF-LIFE; HYDROGEN-ION CONCENTRATION; LIGHT; MICELLES; NUCLEOTIDES; PROTEIN BINDING; RHODOPSIN; SCATTERING, RADIATION; TEMPERATURE; TRANSDUCIN;

EID: 79953906182     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200037j     Document Type: Article

References (71)

1. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies Trends Biochem. Sci. 26, 318-324 (Pubitemid 32436382)
2. Palczewski, K. (2006) G protein-coupled receptor rhodopsin Annu. Rev. Biochem. 75, 743-767 (Pubitemid 44118051)
3. Emeis, D., Kuhn, H., Reichert, J., and Hofmann, K. P. (1982) Complex formation between metarhodopsin II and GTP-binding protein in bovine photoreceptor membranes leads to a shift of the photoproduct equilibrium FEBS Lett. 143, 29-34
4. Parkes, J. H., Gibson, S. K., and Liebman, P. A. (1999) Temperature and pH dependence of the metarhodopsin I-metarhodopsin II equilibrium and the binding of metarhodopsin II to G protein in rod disk membranes Biochemistry 38, 6862-6878
5. Parkes, J. H. and Liebman, P. A. (1984) Temperature and pH dependence of the metarhodopsin I-metarhodopsin II kinetics and equilibria in bovine rod disk membrane suspensions Biochemistry 23, 5054-5061
6. Fung, J. J., Deupi, X., Pardo, L., Yao, X. J., Velez-Ruiz, G. A., Devree, B. T., Sunahara, R. K., and Kobilka, B. K. (2009) Ligand-regulated oligomerization of beta(2)-adrenoceptors in a model lipid bilayer EMBO J. 28, 3315-3328
7. Alves, I. D., Salgado, G. F., Salamon, Z., Brown, M. F., Tollin, G., and Hruby, V. J. (2005) Phosphatidylethanolamine enhances rhodopsin photoactivation and transducin binding in a solid supported lipid bilayer as determined using plasmon-waveguide resonance spectroscopy Biophys. J. 88, 198-210 (Pubitemid 40070669)
8. Litman, B. J., Niu, S. L., Polozova, A., and Mitchell, D. C. (2001) The role of docosahexaenoic acid containing phospholipids in modulating G protein-coupled signaling pathways: visual transduction J. Mol. Neurosci. 16, 237-242 (Pubitemid 32664785)
9. Jastrzebska, B., Goc, A., Golczak, M., and Palczewski, K. (2009) Phospholipids are needed for the proper formation, stability, and function of the photoactivated rhodopsin-transducin complex Biochemistry 48, 5159-5170
10. Mitchell, D. C., Niu, S. L., and Litman, B. J. (2001) Optimization of receptor-G protein coupling by bilayer lipid composition I: kinetics of rhodopsin-transducin binding J. Biol. Chem. 276, 42801-42806
11. Gawrisch, K., Soubias, O., and Mihailescu, M. (2008) Insights from biophysical studies on the role of polyunsaturated fatty acids for function of G-protein coupled membrane receptors Prostaglandins Leukotrienes Essent. Fatty Acids 79, 131-134
12. Bennett, M. P. and Mitchell, D. C. (2008) Regulation of membrane proteins by dietary lipids: effects of cholesterol and docosahexaenoic acid acyl chain-containing phospholipids on rhodopsin stability and function Biophys. J. 95, 1206-1216
13. McKibbin, C., Farmer, N. A., Jeans, C., Reeves, P. J., Khorana, H. G., Wallace, B. A., Edwards, P. C., Villa, C., and Booth, P. J. (2007) Opsin stability and folding: modulation by phospholipid bicelles J. Mol. Biol. 374, 1319-1332 (Pubitemid 350122546)
14. Faham, S., Boulting, G. L., Massey, E. A., Yohannan, S., Yang, D., and Bowie, J. U. (2005) Crystallization of bacteriorhodopsin from bicelle formulations at room temperature Protein Sci. 14, 836-840 (Pubitemid 40283923)
15. Rasmussen, S. G., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I., and Kobilka, B. K. (2007) Crystal structure of the human beta2 adrenergic G-protein-coupled receptor Nature 450, 383-387 (Pubitemid 350126755)
16. Luecke, H., Schobert, B., Stagno, J., Imasheva, E. S., Wang, J. M., Balashov, S. P., and Lanyi, J. K. (2008) Crystallographic structure of xanthorhodopsin, the light-driven proton pump with a dual chromophore Proc. Natl. Acad. Sci. U. S. A. 105, 16561-16565
17. Ujwal, R., Cascio, D., Colletier, J. P., Faham, S., Zhang, J., Toro, L., Ping, P., and Abramson, J. (2008) The crystal structure of mouse VDAC1 at 2.3 Å resolution reveals mechanistic insights into metabolite gating Proc. Natl. Acad. Sci. U. S. A. 105, 17742-17747
18. Bayburt, T. H., Vishnivetskiy, S. A., McLean, M. A., Morizumi, T., Huang, C. C., Tesmer, J. J., Ernst, O. P., Sligar, S. G., and Gurevich, V. V. (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding J. Biol. Chem. 286, 1420-1428
19. Sanders, C. R. and Prosser, R. S. (1998) Bicelles: a model membrane system for all seasons? Structure 6, 1227-1234 (Pubitemid 28485955)
20. Wu, H., Su, K., Guan, X., Sublette, M. E., and Stark, R. E. (2010) Assessing the size, stability, and utility of isotropically tumbling bicelle systems for structural biology Biochim. Biophys. Acta 1798, 482-488
21. Glover, K. J., Whiles, J. A., Wu, G., Yu, N., Deems, R., Struppe, J. O., Stark, R. E., Komives, E. A., and Vold, R. R. (2001) Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules Biophys. J. 81, 2163-2171 (Pubitemid 32917165)
22. Struppe, J., Whiles, J. A., and Vold, R. R. (2000) Acidic phospholipid bicelles: A versatile model membrane system Biophys. J. 78, 281-289 (Pubitemid 30207137)
23. Struppe, J., Komives, E. A., Taylor, S. S., and Vold, R. R. (1998) 2H NMR studies of a myristoylated peptide in neutral and acidic phospholipid bicelles Biochemistry 37, 15523-15527 (Pubitemid 28516015)
24. Marcotte, I. and Auger, M. (2005) Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins Concepts Magn. Reson., Part A 24A, 17-37
25. Prosser, R. S., Hwang, J. S., and Vold, R. R. (1998) Magnetically aligned phospholipid bilayers with positive ordering: a new model membrane system Biophys. J. 74, 2405-2418 (Pubitemid 28225237)
26. t with four proteases defines monoclonal antibody epitope J. Biol. Chem. 266, 14072-14081 (Pubitemid 21907462)
27. Litman, B. J. (1982) Purification of rhodopsin by concanavalin A affinity chromatography Methods Enzymol. 81, 150-153
28. Aris, L., Gilchrist, A., Rens-Domiano, S., Meyer, C., Schatz, P. J., Dratz, E. A., and Hamm, H. E. (2001) Structural requirements for the stabilization of metarhodopsin II by the C terminus of the α subunit of transducin J. Biol. Chem. 276, 2333-2339
29. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
30. Preininger, A., Funk, M., Meier, S., Oldham, W., Johnston, C., Adhikary, S., Kimple, A., Siderovski, D., Hamm, H., and Iverson, T. (2009) Helix dipole movement and conformational variability contribute to allosteric GDP release in Gi subunits Biochemistry 48, 2630-2642
31. Schleicher, A., Kuhn, H., and Hofmann, K. P. (1989) Kinetics, binding constant, and activation energy of the 48-kDa protein-rhodopsin complex by extra-metarhodopsin II Biochemistry 28, 1770-1775 (Pubitemid 19072052)
32. Hoffmann, W., Siebert, F., Hofmann, K. P., and Kreutz, W. (1978) Two distinct rhodopsin molecules within the disc membrane of vertebrate rod outer segments Biochim. Biophys. Acta 503, 450-461 (Pubitemid 9007252)
33. Emeis, D. and Hofmann, K. P. (1981) Shift in the relation between flash-induced metarhodopsin I and metarhodpsin II within the first 10% rhodopsin bleaching in bovine disc membranes FEBS Lett. 136, 201-207 (Pubitemid 12142382)
34. Kisselev, O. G., Meyer, C. K., Heck, M., Ernst, O. P., and Hofmann, K. P. (1999) Signal transfer from rhodopsin to the G-protein: evidence for a two-site sequential fit mechanism Proc. Natl. Acad. Sci. U. S. A. 96, 4898-4903 (Pubitemid 29214507)
35. Chen, Y., Herrmann, R., Fishkin, N., Henklein, P., Nakanishi, K., and Ernst, O. P. (2008) Synthesis and spectroscopic characterization of photo-affinity peptide ligands to study rhodopsin-G protein interaction Photochem. Photobiol. 84, 831-838
36. Faham, S. and Bowie, J. U. (2002) Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure J. Mol. Biol. 316, 1-6 (Pubitemid 34729261)
37. Bayburt, T. H., Leitz, A. J., Xie, G., Oprian, D. D., and Sligar, S. G. (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins J. Biol. Chem. 282, 14875-14881 (Pubitemid 47093370)
38. Sanders, C. R. and Schwonek, J. P. (1992) Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR Biochemistry 31, 8898-8905
39. Sanders, C. R., Kuhn Hoffmann, A., Gray, D. N., Keyes, M. H., and Ellis, C. D. (2004) French swimwear for membrane proteins ChemBiochem 5, 423-426 (Pubitemid 39257097)
40. Whiles, J. A., Deems, R., Vold, R. R., and Dennis, E. A. (2002) Bicelles in structure-function studies of membrane-associated proteins Bioorg. Chem. 30, 431-442 (Pubitemid 36294219)
41. Boesze-Battaglia, K. and Schimmel, R. (1997) Cell membrane lipid composition and distribution: implications for cell function and lessons learned from photoreceptors and platelets J. Exp. Biol. 200, 2927-2936 (Pubitemid 28029161)
42. Eichberg, J. and Hess, H. H. (1967) The lipid composition of frog retinal rod outer segments Experientia 23, 993-994
43. Wiegand, R. D., Naash, M. I., Penn, J. S., Maude, M. B., and Anderson, R. E. (1986) Effect of Constant Light on Rat Retinas Deficient in Glutathione-Reductase Fed. Proc. 45, 1728-1728
44. Kosloff, M., Alexov, E., Arshavsky, V. Y., and Honig, B. (2008) Electrostatic and lipid anchor contributions to the interaction of transducin with membranes: mechanistic implications for activation and translocation J. Biol. Chem. 283, 31197-31207
45. Lambright, D. G., Sondek, J., Bohm, A., Skiba, N. P., Hamm, H. E., and Sigler, P. B. (1996) The 2.0 A crystal structure of a heterotrimeric G protein Nature 379, 311-319
46. Bohm, A., Gaudet, R., and Sigler, P. B. (1997) Structural aspects of heterotrimeric G-protein signaling Curr. Opin. Biotechnol. 8, 480-487 (Pubitemid 27351287)
47. Saari, J. C., Nawrot, M., Stenkamp, R. E., Teller, D. C., and Garwin, G. G. (2009) Release of 11-cis-retinal from cellular retinaldehyde-binding protein by acidic lipids Mol. Vis. 15, 844-854
48. Ilincheta de Boschero, M. G. and Giusto, N. M. (1992) Phosphatidic acid and polyphosphoinositide metabolism in rod outer segments. Differential role of soluble and peripheral proteins Biochim. Biophys. Acta 1127, 105-115
49. LaLonde, M. M., Janssens, H., Rosenbaum, E., Choi, S. Y., Gergen, J. P., Colley, N. J., Stark, W. S., and Frohman, M. A. (2005) Regulation of phototransduction responsiveness and retinal degeneration by a phospholipase D-generated signaling lipid J. Cell Biol. 169, 471-479 (Pubitemid 40686697)
50. Calvert, P. D., Govardovskii, V. I., Krasnoperova, N., Anderson, R. E., Lem, J., and Makino, C. L. (2001) Membrane protein diffusion sets the speed of rod phototransduction Nature 411, 90-94 (Pubitemid 32428195)
51. Aveldano, M. I. (1995) Phospholipid solubilization during detergent extraction of rhodopsin from photoreceptor disk membranes Arch. Biochem. Biophys. 324, 331-343 (Pubitemid 26006416)
52. Nickell, S., Park, P. S., Baumeister, W., and Palczewski, K. (2007) Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography J. Cell Biol. 177, 917-925 (Pubitemid 46873096)
53. Andersson, A. and Maler, L. (2006) Size and shape of fast-tumbling bicelles as determined by translational diffusion Langmuir 22, 2447-2449
54. Dupuy, C., Auvray, X., and Petipas, C. (1997) Anomeric effects on the structure of micelles of alkyl maltosides in water Langmuir 13, 3965-3967 (Pubitemid 127591808)
55. Kozak, M., Kempka, M., Szpotkowski, K., and Jurga, S. (2007) NMR in soft materials: A study of DMPC/DHPC bicellar system J. Non-Cryst. Solids 353, 4246-4251 (Pubitemid 350016028)
56. Botelho, A. V., Huber, T., Sakmar, T. P., and Brown, M. F. (2006) Curvature and hydrophobic forces drive oligomerization and modulate activity of rhodopsin in membranes Biophys. J. 91, 4464-4477 (Pubitemid 44911035)
57. Botelho, A. V., Gibson, N. J., Thurmond, R. L., Wang, Y., and Brown, M. F. (2002) Conformational energetics of rhodopsin modulated by nonlamellar-forming lipids Biochemistry 41, 6354-6368 (Pubitemid 34526000)
58. Sato, K., Morizumi, T., Yamashita, T., and Shichida, Y. (2010) Direct observation of the pH-dependent equilibrium between metarhodopsins I and II and the pH-independent interaction of metarhodopsin II with transducin C-terminal peptide Biochemistry 49, 736-741
59. Jager, S., Palczewski, K., and Hofmann, K. P. (1996) Opsin/all-trans- retinal complex activates transducin by different mechanisms than photolyzed rhodopsin Biochemistry 35, 2901-2908 (Pubitemid 26086799)
60. Jastrzebska, B., Golczak, M., Fotiadis, D., Engel, A., and Palczewski, K. (2009) Isolation and functional characterization of a stable complex between photoactivated rhodopsin and the G protein, transducin FASEB J. 23, 371-381
61. Lee, A. G. (2003) Lipid-protein interactions in biological membranes: a structural perspective Biochim. Biophys. Acta 1612, 1-40 (Pubitemid 36555684)
62. Shogomori, H. and Brown, D. A. (2003) Use of detergents to study membrane rafts: the good, the bad, and the ugly Biol. Chem. 384, 1259-1263 (Pubitemid 37168692)
63. Simons, K. and Ikonen, E. (1997) Functional rafts in cell membranes Nature 387, 569-572 (Pubitemid 27248754)
64. Gibson, N. J. and Brown, M. F. (1991) Role of phosphatidylserine in the MI-MII equilibrium of rhodopsin Biochem. Biophys. Res. Commun. 176, 915-921
65. Gibson, N. J. and Brown, M. F. (1993) Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes Biochemistry 32, 2438-2454 (Pubitemid 23094909)
66. Bayburt, T. H., Vishnivetskiy, S. A., McLean, M. A., Morizumi, T., Huang, C. C., Tesmer, J. J., Ernst, O. P., Sligar, S. G., and Gurevich, V. V. (2011) Monomeric rhodopsin is sufficient for normal rhodopsin kinase (GRK1) phosphorylation and arrestin-1 binding J. Biol. Chem. 1420
67. Tsukamoto, H., Sinha, A., DeWitt, M., and Farrens, D. L. (2010) Monomeric rhodopsin is the minimal functional unit required for arrestin binding J. Mol. Biol. 399, 501-511
68. Kohl, B. and Hofmann, K. P. (1987) Temperature dependence of G-protein activation in photoreceptor membranes. Transient extra metarhodopsin II on bovine disk membranes Biophys. J. 52, 271-277
69. Knierim, B., Hofmann, K. P., Ernst, O. P., and Hubbell, W. L. (2007) Sequence of late molecular events in the activation of rhodopsin Proc. Natl. Acad. Sci. U. S. A. 104, 20290-20295
70. Feller, S. E. (2008) Acyl chain conformations in phospholipid bilayers: a comparative study of docosahexaenoic acid and saturated fatty acids Chem. Phys. Lipids 153, 76-80
71. Niu, S. L., Mitchell, D. C., and Litman, B. J. (2001) Optimization of receptor-G protein coupling by bilayer lipid composition II: formation of metarhodopsin II-transducin complex J. Biol. Chem. 276, 42807-42811