Photoactivation of rhodopsin causes an increased hydrogen-deuterium exchange of buried peptide groups

Biophysical Journal

Volumn 74, Issue 1, 1998, Pages 192-198

  Rath, Parshuram ^a,c   DeGrip, Willem J ^b   Rothschild, Kenneth J ^a  

^a Boston University   (United States)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Emisphere Technologies Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROGEN; PEPTIDE; RHODOPSIN; TRANSDUCIN;

ARTICLE; FOURIER TRANSFORMATION; INFRARED RADIATION; INFRARED SPECTROMETRY; ION EXCHANGE; PHOTOACTIVATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE;

EID: 0031972563     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(98)77779-3     Document Type: Article

References (59)

1. Arkin, I. T., K. R. MacKenzie, L. Fisher, S. Aimoto, D. M. Engelman, and S. O. Smith. 1996. Mapping the lipid-exposed surfaces of membrane proteins. Nat. Struct. Biol. 3:240-243.
2. Baenziger, J. E., K. W. Miller, M. P. McCarthy, and K. J. Rothschild. 1992. Probing conformational changes in the nicotinic acetylcholine receptor by Fourier transform infrared difference spectroscopy. Biophys. J. 62: 64-66.
3. Bagley, K. A., V. Balogh-Nair, A. A. Croteau, G. Dollinger, T. G. Ebrey, L. Eisenstein, M. K. Hong, K. Nakanishi, and J. Vittitow. 1985. Fourier-transform infrared difference spectroscopy of rhodopsin and its photoproducts at low temperature. Biochemistry. 24:6055-6071.
4. Blout, E. R., C. de Lozé, and A. Asadourian. 1961. The deuterium exchange of water-soluble polypeptides and proteins as measured by infrared spectroscopy. J. Am. Chem. Soc. 83:1895-1900.
5. Braiman, M. S., and K. J. Rothschild. 1988. Fourier transform infrared techniques for probing membrane protein structure. Annu. Rev. Biophys. Biophys. Chem. 17:541-570.
6. Clark, N. A., K. J. Rothschild, D. A. Luippold, and A. Simon. 1980. Surface-induced lamellar orientation of multilayer membrane arrays: theoretical analysis and a new method with application to purple membrane fragments. Biophys. J. 31:65-96.
7. DeCaluwé, G. L. J., P. H. M. Bovee-Geurts, P. Rath, K. J. Rothschild, and W. J. DeGrip. 1995. Effect of carboxyl mutations on functional properties of bovine rhodopsin. Biophys. Chem. 56:79-87.
8. DeGrip, W. J., and F. J. M. Daemen. 1982. Sulfhydryl chemistry of rhodopsin. Methods Enzymol. 81:223-236.
9. DeGrip, W. J., F. J. M. Daemen, and S. L. Bonting. 1980. Isolation and purification of bovine rhodopsin. Methods Enzymol. 67:301-320.
10. DeGrip, W. J., J. Gillespie, and K. J. Rothschild. 1985. Carboxyl group involvement in the meta I and meta II stages in rhodopsin bleaching. A Fourier transform infrared spectroscopic study. Biochim. Biophys. Acta. 809:97-106.
11. DeGrip, W. J., D. Gray, J. Gillespie, P. H. M. Bovee, E. M. M. Van den Berg, J. Lugtenburg, and K. J. Rothschild. 1988. Photoexcitation of rhodopsin: conformation changes in the chromophore, protein and associated lipids as determined by FTIR difference spectroscopy. Photochem. Photobiol. 48:497-504.
12. Downer, N. W., T. J. Bruchman, and J. H. Hazzard. 1986. Infrared spectroscopic study of photoreceptor membrane and purple membrane. Protein secondary structure and hydrogen deuterium exchange. J. Biol. Chem. 261:3640-3647.
13. Downer, N. W., and J. J. Englander. 1982. Tritium-hydrogen exchange kinetics. Methods Enzymol. (Biomembranes, Pt. I), 88:673-676.
14. Downer, N. W., and S. W. Englander. 1977. Hydrogen exchange study of membrane-bound rhodopsin. II. Light-induced protein structure change. J. Biol. Chem. 252:8101-8104.
15. Earnest, T. N., P. Roepe, M. S. Braiman, J. Gillespie, and K. J. Rothschild. 1986. Orientation of the bacteriorhodopsin chromophore probed by polarized Fourier transform infrared difference spectroscopy. Biochemistry. 25:7793-7798.
16. Englander, J. J., N. W. Downer, and S. W. Englander. 1982. Reexamination of rhodopsin structure by hydrogen exchange. J. Biol. Chem. 257: 7982-7986.
17. Englander, J. J., and S. W. Englander. 1977. Comparison of bacterial and animal rhodopsins by hydrogen exchange studies. Nature (Lond.). 265: 658-659.
18. Englander, S. W., and L. Mayne. 1992. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21:243-265.
19. Fahmy, K., F. Siebert, and T. P. Sakmar. 1994. A mutant rhodopsin photoproduct with a protonated Schiff base displays an active-state conformation: a Fourier-transform infrared spectroscopy study. J. Biochem. 33:13700-13705.
20. Farahbakhsh, Z. T., K. Hideg, and W. L. Hubbell. 1993. Photoactivated conformational changes in rhodopsin: a time-resolved spin label study. Science. 262:1416-1419.
21. Green, B. H., T. G. Monger, R. R. Alfano, B. Aton, and R. H. Callender. 1977. Cis-trans isomerization in rhodopsin occurs in picoseconds. Nature (Lond.). 269:179-180.
22. Hargrave, P. A., and J. H. McDowell. 1992. Rhodopsin and phototransduction: a model system for G protein-linked receptors. FASEB J. 6:2323-2331.
23. Haris, P. I., M. Coke, and D. Chapman. 1989. Fourier transform infrared spectroscopic investigation of rhodopsin structure and its comparison with bacteriorhodopsin. Biochim. Biophys. Acta. 995:160-167.
24. Harrick, N. J. 1967. Internal Reflection Spectroscopy. Interscience Publishers, New York.
25. Khorana, H. G. 1992. Rhodopsin, photoreceptor of the rod cell. An emerging pattern for structure and function. J. Biol. Chem. 267:1-4.
26. Kibelbek, J., D. C. Mitchell, J. M. Beach, and B. J. Litman. 1991. Functional equivalence of metarhodopsin II and the G{-t}-activating form of photolyzed bovine rhodopsin. Biochemistry. 30:6761-6768.
27. Klinger, A. L., and M. S. Braiman. 1992. Structural comparison of metarhodopsin II, metarhodopsin III, and opsin based on kinetic analysis of Fourier transform infrared difference spectra. Biophys. J. 63:1244-1255.
28. Kuehn, H., and P. A. Hargrave. 1981. Light-induced binding of guanosinetriphosphatase to bovine photoreceptor membranes: effect of limited proteolysis of the membranes. Biochemistry. 20:2410-2417.
29. Ludlam, C. F. C., I. T. Arkin, X.-M. Liu, M. S. Rothman, P. Rath, S. Aimoto, S. O. Smith, D. M. Engelman, and K. J. Rothschild. 1996. Fourier transform infrared spectroscopy and site-directed isotope labeling as a probe of local secondary structure in the transmembrane domain of phospholamban. Biophys. J. 70:1728-1736.
30. Ludlam, C. F. C., S. Sonar, C.-P. Lee, M. Coleman, J. Herzfeld, U. L. RajBhandary, and K. J. Rothschild. 1995. Site-directed isotope labeling and ATR-FTIR difference spectroscopy of bacteriorhodopsin: the peptide carbonyl group of Tyr 185 is structurally active during the bR→N transition. Biochemistry. 34:2-6.
31. Marrero, H., and K. J. Rothschild. 1987. Conformational changes in bacteriorhodopsin studied by infrared attenuated total reflection. Biophys. J. 52:629-635.
32. Miyazawa, T., T. Shimanouchi, and S. Mizushima. 1958. Normal vibrations of N-methylacetamide. J. Chem. Phys. 29:611-616.
33. Nishimura, S., J. Sasaki, H. Kandori, T. Matsuda, Y. Fukada, and A. Maeda. 1996. Structural changes in the peptide backbone in complex formation between activated rhodopsin and transducin studied by FTIR spectroscopy. Biochemistry. 35:13267-13271.
34. Osborne, H. B., and E. Nabedryk-Viala. 1977. The hydrophobic heart of rhodopsin revealed by an infrared proton-deuterium exchange study. FEBS Lett. 84:217-220.
35. Osborne, H. B., and E. Nabedryk-Viala. 1978. The conformation of membrane-bound and detergent-solubilised bovine rhodopsin: a comparative hydrogen-isotope exchange study. Eur. J. Biochem. 89:81-88.
36. Osborne, H. B., C. Sardet, M. Michel-Villaz, and M. Chabre. 1978. Structural study of rhodopsin in detergent micelles by small-angle neutron scattering. J. Mol. Biol. 123:177-206.
37. Ostroy, S. E. 1977. Rhodopsin and the visual process. Biochim. Biophys. Acta. 463:91-125.
38. Pistorius, A. M. A., and W. J. DeGrip. 1994. Rhodopsin's secondary structure revisited: assignment of structural elements. Biochem. Biophys. Res. Commun. 198:1040-1045.
39. Rath, P., P. H. M. Bovee-Geurts, W. J. DeGrip, and K. J. Rothschild. 1994. Photoactivation of rhodopsin involves alterations in cysteine side-chains: detection of an S-H band in the Meta I→Meta II FTIR difference spectrum. Biophys. J. 66:2085-2091.
40. Rath, P., L. L. J. DeCaluwé, P. H.-M. Bovee-Geurts, W. J. DeGrip, and K. J. Rothschild. 1993. Fourier-transform infrared difference spectroscopy of rhodopsin mutants: light activation of rhodopsin causes hydrogen bonding change in residue aspartic acid-83 during meta II formation. Biochemistry. 32:10277-10282.
41. Rath, P., E. Spudich, D. D. Neal, J. L. Spudich, and K. J. Rothschild. 1996. Asp-76 is the Schiff base counterion and proton acceptor in the proton-translocating form of sensory rhodopsin I. Biochemistry. 35:6690-6696.
42. Regan, C. M., W. J. DeGrip, F. J. M. Daemen, and S. L. Bonting. 1978. Biochemical aspects of the visual process. XXXIX. Sulfhydryl group reactivity as a probe of transient protein conformational changes during rhodopsin photolysis. Biochim. Biophys. Acta 537:145-152.
43. Rothschild, K. J., J. Andrew, W. J. DeGrip, and H. E. Stanley. 1976. Opsin structure probed by Raman spectroscopy of photoreceptor membranes. Science. 191:1176-1178.
44. Rothschild, K. J., W. A. Cantore, and H. Marrero, 1983. Fourier transform infrared difference spectra of intermediates in rhodopsin bleaching. Science. 219:1333-1335.
45. Rothschild, K. J., and N. A. Clark. 1979. Polarized infrared spectroscopy of oriented purple membrane. Biophys. J. 25:473-488.
46. Rothschild, K. J., W. DeGrip, and R. Sanches. 1980a. Fourier transform infrared absorption of photoreceptor membrane. I. Group assignments based on rhodopsin delipidation and reconstitution. Biochim. Biophys. Acta. 596:338-351.
47. Rothschild, K. J., and W. J. DeGrip. 1986. FTIR studies of the rhodopsin transduction mechanism. Photobiochem. Photobiophys. 13:245-258.
48. Rothschild, K. J., J. Gillespie, and W. J. DeGrip. 1987. Evidence for rhodopsin refolding during the decay of meta II. Biophys. J. 51:345-350.
49. Rothschild, K. J., K. M. Rosen, and N. A. Clark. 1980b. Incorporation of photoreceptor membrane into a multilamellar film. Biophys. J. 31: 45-52.
50. Rothschild, K. J., R. Sanches, T. L. Hsiao, and N. A. Clark. 1980c. A spectroscopic study of rhodopsin alpha-helix orientation. Biophys. J. 31:53-64.
51. Rothschild, K. J., M. Zagaeski, and W. A. Cantore. 1981. Conformational changes of bacteriorhodopsin detected by Fourier transform infrared difference spectroscopy. Biochem. Biophys. Res. Commun. 103: 483-489.
52. Schoenlein, R. W., L. A. Peteanu, R. A. Mathies, and C. V. Shank. 1991. The first step in vision: femtosecond isomerization of rhodopsin. Science. 254:412-415.
53. Siebert, F., W. Maentele, and K. Gerwert. 1983. Fourier-transform infrared spectroscopy applied to rhodopsin. The problem of the protonation state of the retinylidene Schiff base reinvestigated. Eur. J. Biochem. 136: 119-127.
54. 2O solutions. J. Biol. Chem. 242:5460-5466.
55. Van Breugel, P. J. G. M., P. H. M. Bovee-Geurts, S. L. Bonting, and F. J. M. Daemen. 1979. Biochemical aspects of the visual process. XL. Spectral and chemical analysis of metarhodopsin III in photoreceptor membrane suspensions. Biochim. Biophys. Acta. 557:188-198.
56. van Rhee, A. M., and K. A. Jacobson. 1996. Molecular architecture of G-protein-coupled receptors. Drug Dev. Res. 37:1-38.
57. Vuong, T. M., M. Chabre, and L. Stryer. 1984. Millisecond activation of transducin in the cyclic nucleotide cascade of vision. Nature (Lond.). 311:659-661.
58. Wald, G. 1968. Molecular basis of visual excitation. Science. 162: 230-239.
59. Yoshizawa, T., and G. Wald. 1963. Pre-lumirhodopsin and the bleaching of visual pigments. Nature. 197:1279-1286.