Intramolecular interactions that induce helical rearrangement upon rhodopsin activation: Light-induced structural changes in metarhodopsin II a probed by cysteine S-H stretching vibrations

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 13792-13800

  Yamazaki, Yoichi ^a,b   Nagata, Tomoko ^a   Terakita, Akihisa ^a,c   Kandori, Hideki ^a,d   Shichida, Yoshinori ^a   Imamoto, Yasushi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^c Osaka Prefecture University   (Japan)

^d NAGOYA INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; CHROMOPHORES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; HYDROGEN BONDS; PROTEINS; STRETCHING;

ENVIRONMENTAL CHANGE; G-PROTEIN TRANSDUCIN; HYDROPHOBIC PACKING; INTRAMOLECULAR INTERACTIONS; STRETCHING FREQUENCY; STRETCHING VIBRATIONS; TRANSMEMBRANE HELICES; TRANSMEMBRANE REGIONS;

AMINO ACIDS;

ALANINE; ARGININE; CYSTEINE; GLUTAMIC ACID; GLYCINE; HISTIDINE; LEUCINE; METARHODOPSIN 2A; PHENYLALANINE; RHODOPSIN; TRYPTOPHAN; UNCLASSIFIED DRUG; LIPOSOME; METARHODOPSINS; PHOSPHATIDYLCHOLINE; PROTEIN BINDING;

AMINO ACID COMPOSITION; ARTICLE; CHROMATOPHORE; HYDROGEN BOND; HYDROPHOBICITY; INFRARED SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HEK293 CELL LINE; HUMAN; LIGHT; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN SECONDARY STRUCTURE; RADIATION RESPONSE; VIBRATION;

AMINO ACID SEQUENCE; CYSTEINE; HEK293 CELLS; HUMANS; LIGHT; LIPOSOMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHATIDYLCHOLINES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RHODOPSIN; VIBRATION;

EID: 84901024015     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.527606     Document Type: Article

References (47)

1. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: a G proteincoupled receptor. Science 289, 739-745
2. 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 humanβ2 adrenergic G-protein-coupled receptor. Nature 450, 383-387
3. Cherezov, V., Rosenbaum, D. M., Hanson, M.A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human β2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
4. Farrens, D. L., Altenbach, C., Yang, K., Hubbell, W. L., and Khorana, H. G. (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274, 768-770
5. Sheikh, S. P., Zvyaga, T. A., Lichtarge, O., Sakmar, T. P., and Bourne, H. R. (1996) Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F. Nature 383, 347-350
6. Dunham, T. D., and Farrens, D. L. (1999) Conformational changes in rhodopsin. Movement of helix F detected by site-specific chemical labeling and fluorescence spectroscopy. J. Biol. Chem. 274, 1683-1690
7. Deupi, X., and Standfuss, J. (2011) Structural insights into agonist-induced activation of G-protein-coupled receptors. Curr. Opin. Struct. Biol. 21, 541-551
8. Choe, H. W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauss, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II. Nature 471, 651-655
9. Standfuss, J., Edwards, P. C., D'Antona, A., Fransen, M., Xie, G., Oprian, D. D., and Schertler, G. F. (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471, 656-660
10. Deupi, X., Edwards, P., Singhal, A., Nickle, B., Oprian, D., Schertler, G., and Standfuss, J. (2012) StabilizedGprotein binding site in the structure of constitutively active metarhodopsin-II. Proc. Natl. Acad. Sci. U.S.A. 109, 119-124
11. Matthews, R. G., Hubbard, R., Brown, P. K., and Wald, G. (1963) Tautomeric forms of metarhodopsin. J. Gen. Physiol. 47, 215-240
12. 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
13. Imai, H., Mizukami, T., Imamoto, Y., and Shichida, Y. (1994) Direct observation of the thermal equilibria among lumirhodopsin, metarhodopsin I, and metarhodopsin II in chicken rhodopsin. Biochemistry 33, 14351-14358
14. 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
15. 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
16. Vogel, R., Mahalingam, M., Lüdeke, S., Huber, T., Siebert, F., and Sakmar, T. P. (2008) Functional role of the "ionic lock": an interhelical hydrogenbond network in family A heptahelical receptors. J. Mol. Biol. 380, 648-655
17. Mahalingam, M., Martínez-Mayorga, K., Brown, M. F., and Vogel, R. (2008) Two protonation switches control rhodopsin activation in membranes. Proc. Natl. Acad. Sci. U.S.A. 105, 17795-17800
18. Zaitseva, E., Brown, M. F., and Vogel, R. (2010) Sequential rearrangement of interhelical networks upon rhodopsin activation in membranes: the Meta IIa conformational substate. J. Am. Chem. Soc. 132, 4815-4821
19. Vogel, R., and Siebert, F. (2003) Fourier transform IR spectroscopy study for new insights into molecular properties and activation mechanisms of visual pigment rhodopsin. Biopolymers 72, 133-148
20. Li, H., and Thomas, G. J., Jr. (1991) Cysteine conformation and sulfhydryl interactions in proteins and viruses. 1. Correlation of the Raman S-H band with hydrogen bonding and intramolecular geometry in model compounds. J. Am. Chem. Soc. 113 456-462
21. Rath, P., Bovee-Geurts, P. H., DeGrip, W. J., and Rothschild, K. J. (1994) Photoactivation of rhodopsin involves alterations in cysteine side chains: detection of an S-H band in the Meta I 3 Meta II FTIR difference spectrum. Biophys. J. 66, 2085-2091
22. Kandori, H., Kinoshita, N., Shichida, Y., Maeda, A., Needleman, R., and Lanyi, J. K. (1998) Cysteine S-H as a hydrogen-bonding probe in proteins. J. Am. Chem. Soc. 120, 5828-5829
23. Yamazaki, Y., Nagata, T., Terakita, A., Kandori, H., Shichida, Y., and Imamoto, Y. (2014) Mapping of the local environmental changes in proteins by cysteine scanning. Biophysics 10, 1-7
24. Ye, S., Zaitseva, E., Caltabiano, G., Schertler, G. F., Sakmar, T. P., Deupi, X., and Vogel, R. (2010) Tracking G-protein-coupled receptor activation using genetically encoded infrared probes. Nature 464, 1386-1389
25. Nathans, J. (1990) Determinants of visual pigment absorbance: identification of the retinylidene Schiff's base counterion in bovine rhodopsin. Biochemistry 29, 9746-9752
26. Fahmy, K., and Sakmar, T. P. (1993) Regulation of the rhodopsin-transducin interaction by a highly conserved carboxylic acid group. Biochemistry 32, 7229-7236
27. 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
28. Zhukovsky, E. A., and Oprian, D. D. (1989) Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246, 928-930
29. Imai, H., Kefalov, V., Sakurai, K., Chisaka, O., Ueda, Y., Onishi, A., Morizumi, T., Fu, Y., Ichikawa, K., Nakatani, K., Honda, Y., Chen, J., Yau, K. W., and Shichida, Y. (2007) Molecular properties of rhodopsin and rod function. J. Biol. Chem. 282, 6677-6684
30. Nathans, J., Weitz, C. J., Agarwal, N., Nir, I., and Papermaster, D. S. (1989) Production of bovine rhodopsin by mammalian cell lines expressing cloned cDNA: spectrophotometry and subcellular localization. Vision Res. 29, 907-914
31. Nagata, T., Terakita, A., Kandori, H., Shichida, Y., and Maeda, A. (1998) The hydrogen-bonding network of water molecules and the peptide backbone in the region connecting Asp83, Gly120, and Glu113 in bovine rhodopsin. Biochemistry 37, 17216-17222
32. Arnis, S., and Hofmann, K. P. (1993) Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proc. Natl. Acad. Sci. U.S.A. 90, 7849-7853
33. Ohkita, Y. J., Sasaki, J., Maeda, A., Yoshizawa, T., Groesbeek, M., Verdegem, P., and Lugtenburg, J. (1995) Changes in structure of the chromophore in the photochemical process of bovine rhodopsin as revealed by FTIR spectroscopy for hydrogen out-of-plane vibrations. Biophys. Chem. 56, 71-78
34. Nishimura, S., Sasaki, J., Kandori, H., Lugtenburg, J., and Maeda, A. (1995) Structural changes in the lumirhodopsin-to-metarhodopsin I conversion of air-dried bovine rhodopsin. Biochemistry 34, 16758-16763
35. Jäger, F., Fahmy, K., Sakmar, T. P., and Siebert, F. (1994) Identification of glutamic acid 113 as the Schiff base proton acceptor in the metarhodopsin II photointermediate of rhodopsin. Biochemistry 33, 10878-10882
36. Fahmy, K., Jäger, F., Beck, M., Zvyaga, T. A., Sakmar, T. P., and Siebert, F. (1993) Protonation states of membrane-embedded carboxylic acid groups in rhodopsin and metarhodopsin II: a Fourier-transform infrared spectroscopy study of site-directed mutants. Proc. Natl. Acad. Sci. U.S.A. 90, 10206-10210
37. Scheerer, P., Park, J. H., Hildebrand, P. W., Kim, Y. J., Krauss, N., Choe, H. W., Hofmann, K. P., and Ernst, O. P. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497-502
38. Park, J. H., Scheerer, P., Hofmann, K. P., Choe, H. W., and Ernst, O. P. (2008) Crystal structure of the ligand-free G-protein-coupled receptor opsin. Nature 454, 183-187
39. Imamoto, Y., Kataoka, M., Tokunaga, F., and Palczewski, K. (2000) Lightinduced conformational changes of rhodopsin probed by fluorescent Alexa594 immobilized on the cytoplasmic surface. Biochemistry 39, 15225-15233
40. Salom, D., Lodowski, D. T., Stenkamp, R. E., Le Trong, I., Golczak, M., Jastrzebska, B., Harris, T., Ballesteros, J. A., and Palczewski, K. (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 103, 16123-16128
41. Weitz, C. J., and Nathans, J. (1992) Histidine residues regulate the transition of photoexcited rhodopsin to its active conformation, metarhodopsin II. Neuron 8, 465-472
42. Imai, H., Kojima, D., Oura, T., Tachibanaki, S., Terakita, A., and Shichida, Y. (1997) Single amino acid residue as a functional determinant of rod and cone visual pigments. Proc. Natl. Acad. Sci. U.S.A. 94, 2322-2326
43. Imamoto, Y., Seki, I., Yamashita, T., and Shichida, Y. (2013) Efficiencies of activation of transducin by cone and rod visual pigments. Biochemistry 52, 3010-3018
44. Nakayama, T. A., and Khorana, H. G. (1991) Mapping of the amino acids in membrane-embedded helices that interact with the retinal chromophore in bovine rhodopsin. J. Biol. Chem. 266, 4269-4275
45. Han, M., Lin, S. W., Smith, S. O., and Sakmar, T. P. (1996) The effects of amino acid replacements of glycine 121 on transmembrane helix 3 of rhodopsin. J. Biol. Chem. 271, 32330-32336
46. Hwa, J., Garriga, P., Liu, X., and Khorana, H. G. (1997) Structure and function in rhodopsin: packing of the helices in the transmembrane domain and folding to a tertiary structure in the intradiscal domain are coupled. Proc. Natl. Acad. Sci. U.S.A. 94, 10571-10576
47. Han, M., Lin, S. W., Minkova, M., Smith, S. O., and Sakmar, T. P. (1996) Functional interaction of transmembrane helices 3 and 6 in rhodopsin. Replacement of phenylalanine 261 by alanine causes reversion of phenotype of a glycine 121 replacement mutant. J. Biol. Chem. 271, 32337-32342