Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Jan 9;93(1):372–376. doi: 10.1073/pnas.93.1.372

Bathorhodopsin structure in the room-temperature rhodopsin photosequence: picosecond time-resolved coherent anti-Stokes Raman scattering.

A Popp 1, L Ujj 1, G H Atkinson 1
PMCID: PMC40240  PMID: 8552641

Abstract

Structural changes in the retinal chromophore during the formation of the bathorhodopsin intermediate (bathoRT) in the room-temperature rhodopsin (RhRT) photosequence (i.e., vision) are examined using picosecond time-resolved coherent anti-Stokes Raman scattering. Specifically, the retinal structure assignable to bathoRT following 8-ps excitation of RhRT is measured via vibrational Raman spectroscopy at a 200-ps time delay where the only intermediate present is bathoRT. Significant differences are observed between the C=C stretching frequencies of the retinal chromophore at low temperature where bathorhodopsin is stabilized and at room temperature where bathorhodopsin is a transient species in the RhRT photosequence. These vibrational data are discussed in terms of the formation of bathoRT, an important step in the energy storage/transduction mechanism of RhRT.

Full text

PDF
372

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arnis S., Hofmann K. P. Two different forms of metarhodopsin II: Schiff base deprotonation precedes proton uptake and signaling state. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7849–7853. doi: 10.1073/pnas.90.16.7849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bagley K. A., Balogh-Nair V., Croteau A. A., Dollinger G., Ebrey T. G., Eisenstein L., Hong M. K., Nakanishi K., Vittitow J. Fourier-transform infrared difference spectroscopy of rhodopsin and its photoproducts at low temperature. Biochemistry. 1985 Oct 22;24(22):6055–6071. doi: 10.1021/bi00343a006. [DOI] [PubMed] [Google Scholar]
  3. Birge R. R., Einterz C. M., Knapp H. M., Murray L. P. The nature of the primary photochemical events in rhodopsin and isorhodopsin. Biophys J. 1988 Mar;53(3):367–385. doi: 10.1016/S0006-3495(88)83114-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birge R. R. Nature of the primary photochemical events in rhodopsin and bacteriorhodopsin. Biochim Biophys Acta. 1990 Apr 26;1016(3):293–327. doi: 10.1016/0005-2728(90)90163-x. [DOI] [PubMed] [Google Scholar]
  5. Cooper A. Energy uptake in the first step of visual excitation. Nature. 1979 Nov 29;282(5738):531–533. doi: 10.1038/282531a0. [DOI] [PubMed] [Google Scholar]
  6. DeGrip W. J., Gray D., Gillespie J., Bovee P. H., Van den Berg E. M., Lugtenburg J., Rothschild K. J. Photoexcitation of rhodopsin: conformation changes in the chromophore, protein and associated lipids as determined by FTIR difference spectroscopy. Photochem Photobiol. 1988 Oct;48(4):497–504. doi: 10.1111/j.1751-1097.1988.tb02852.x. [DOI] [PubMed] [Google Scholar]
  7. Deng H., Callender R. H. A study of the Schiff base mode in bovine rhodopsin and bathorhodopsin. Biochemistry. 1987 Nov 17;26(23):7418–7426. doi: 10.1021/bi00397a033. [DOI] [PubMed] [Google Scholar]
  8. Deng H., Huang L., Callender R., Ebrey T. Evidence for a bound water molecule next to the retinal Schiff base in bacteriorhodopsin and rhodopsin: a resonance Raman study of the Schiff base hydrogen/deuterium exchange. Biophys J. 1994 Apr;66(4):1129–1136. doi: 10.1016/S0006-3495(94)80893-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Doukas A. G., Aton B., Callender R. H., Ebrey T. G. Resonance Raman studies of bovine metarhodopsin I and metarhodopsin II. Biochemistry. 1978 Jun 13;17(12):2430–2435. doi: 10.1021/bi00605a028. [DOI] [PubMed] [Google Scholar]
  10. Eyring G., Mathies R. Resonance Raman studies of bathorhodopsin: evidence for a protonated Schiff base linkage. Proc Natl Acad Sci U S A. 1979 Jan;76(1):33–37. doi: 10.1073/pnas.76.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ganter U. M., Gärtner W., Siebert F. Rhodopsin-lumirhodopsin phototransition of bovine rhodopsin investigated by Fourier transform infrared difference spectroscopy. Biochemistry. 1988 Sep 20;27(19):7480–7488. doi: 10.1021/bi00419a046. [DOI] [PubMed] [Google Scholar]
  12. Gibson N. J., Brown M. F. Lipid headgroup and acyl chain composition modulate the MI-MII equilibrium of rhodopsin in recombinant membranes. Biochemistry. 1993 Mar 9;32(9):2438–2454. doi: 10.1021/bi00060a040. [DOI] [PubMed] [Google Scholar]
  13. Gilson H. S., Honig B. H., Croteau A., Zarrilli G., Nakanishi K. Analysis of the factors that influence the C=N stretching frequency of polyene Schiff bases. Implications for bacteriorhodopsin and rhodopsin. Biophys J. 1988 Feb;53(2):261–269. doi: 10.1016/S0006-3495(88)83087-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hayward G., Carlsen W., Siegman A., Stryer L. Retinal chromophore of rhodopsin photoisomerizes within picoseconds. Science. 1981 Feb 27;211(4485):942–944. doi: 10.1126/science.7466366. [DOI] [PubMed] [Google Scholar]
  15. Honig B., Ebrey T., Callender R. H., Dinur U., Ottolenghi M. Photoisomerization, energy storage, and charge separation: a model for light energy transduction in visual pigments and bacteriorhodopsin. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2503–2507. doi: 10.1073/pnas.76.6.2503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Horwitz J. S., Lewis J. W., Powers M. A., Kliger D. S. Nanosecond laser photolysis of rhodopsin and isorhodopsin. Photochem Photobiol. 1983 Feb;37(2):181–188. doi: 10.1111/j.1751-1097.1983.tb04456.x. [DOI] [PubMed] [Google Scholar]
  17. Kandori H., Matuoka S., Shichida Y., Yoshizawa T. Dependency of photon density on primary process of cattle rhodopsin. Photochem Photobiol. 1989 Feb;49(2):181–184. doi: 10.1111/j.1751-1097.1989.tb04094.x. [DOI] [PubMed] [Google Scholar]
  18. Kandori H., Shichida Y., Yoshizawa T. Absolute absorption spectra of batho- and photorhodopsins at room temperature. Picosecond laser photolysis of rhodopsin in polyacrylamide. Biophys J. 1989 Sep;56(3):453–457. doi: 10.1016/S0006-3495(89)82692-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lewis J. W., Kliger D. S. Photointermediates of visual pigments. J Bioenerg Biomembr. 1992 Apr;24(2):201–210. doi: 10.1007/BF00762678. [DOI] [PubMed] [Google Scholar]
  20. Marcus M. A., Lewis A. Assigning the resonance Raman spectral features of rhodopsin, isorhodopsin and bathorhodopsin in bovine photostationary state spectra. Photochem Photobiol. 1979 Apr;29(4):699–702. doi: 10.1111/j.1751-1097.1979.tb07752.x. [DOI] [PubMed] [Google Scholar]
  21. Mathies R., Oseroff A. R., Stryer L. Rapid-flow resonance Raman spectroscopy of photolabile molecules: rhodopsin and isorhodopsin. Proc Natl Acad Sci U S A. 1976 Jan;73(1):1–5. doi: 10.1073/pnas.73.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nathans J. Rhodopsin: structure, function, and genetics. Biochemistry. 1992 Jun 2;31(21):4923–4931. doi: 10.1021/bi00136a001. [DOI] [PubMed] [Google Scholar]
  23. Palings I., van den Berg E. M., Lugtenburg J., Mathies R. A. Complete assignment of the hydrogen out-of-plane wagging vibrations of bathorhodopsin: chromophore structure and energy storage in the primary photoproduct of vision. Biochemistry. 1989 Feb 21;28(4):1498–1507. doi: 10.1021/bi00430a012. [DOI] [PubMed] [Google Scholar]
  24. Peteanu L. A., Schoenlein R. W., Wang Q., Mathies R. A., Shank C. V. The first step in vision occurs in femtoseconds: complete blue and red spectral studies. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11762–11766. doi: 10.1073/pnas.90.24.11762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Popp A., Ujj L., Atkinson G. H. Vibrational spectra of room-temperature rhodopsin: concentration dependence in picosecond resonance coherent anti-Stokes Raman scattering. Biophys Chem. 1995 Sep-Oct;56(1-2):129–135. doi: 10.1016/0301-4622(95)00024-r. [DOI] [PubMed] [Google Scholar]
  26. Rath P., DeCaluwé L. L., Bovee-Geurts P. H., DeGrip W. J., Rothschild K. J. 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. 1993 Oct 5;32(39):10277–10282. doi: 10.1021/bi00090a001. [DOI] [PubMed] [Google Scholar]
  27. Sakmar T. P., Franke R. R., Khorana H. G. Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8309–8313. doi: 10.1073/pnas.86.21.8309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Smith S. O., Courtin J., de Groot H., Gebhard R., Lugtenburg J. 13C magic-angle spinning NMR studies of bathorhodopsin, the primary photoproduct of rhodopsin. Biochemistry. 1991 Jul 30;30(30):7409–7415. doi: 10.1021/bi00244a007. [DOI] [PubMed] [Google Scholar]
  29. Yan M., Manor D., Weng G., Chao H., Rothberg L., Jedju T. M., Alfano R. R., Callender R. H. Ultrafast spectroscopy of the visual pigment rhodopsin. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9809–9812. doi: 10.1073/pnas.88.21.9809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zhukovsky E. A., Oprian D. D. Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science. 1989 Nov 17;246(4932):928–930. doi: 10.1126/science.2573154. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES