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. 1991 Nov 1;88(21):9412–9416. doi: 10.1073/pnas.88.21.9412

Mechanism of activation of sensory rhodopsin I: evidence for a steric trigger.

B Yan 1, K Nakanishi 1, J L Spudich 1
PMCID: PMC52727  PMID: 1946353

Abstract

Sensory rhodopsin I (SR-I) and bacteriorhodopsin (BR) from Halobacterium halobium show broad structural and spectroscopic similarities and yet perform distinct functions: photosensory reception and proton pumping, respectively. Probing the photoactive sites of SR-I and BR with 24 retinal analogs reveals differences in the protein environments near the retinal 13-methyl group and near the beta-ionone ring. 13-cis-Retinal does not form a retinylidene pigment with the SR-I apoprotein, although this isomer binds to the BR apoprotein even more rapidly than all-trans-retinal, the functional isomer of both pigments. The activation of both SR-I and BR requires all-trans/13-cis isomerization of retinal;however, a steric interaction between the retinal 13-methyl group and the protein is required for SR-I activation but not for that of BR. These results reveal a key difference between SR-I and BR that is likely to be the initial diverging point in their photoactivation pathways. We propose the 13-methyl group-protein interaction functions as a trigger for SR-I activation--i.e., converts photon absorption by the chromophore into protein conformational changes. A similar steric trigger is essential for activation of mammalian rhodopsin, indicating a common mechanism for receptor activation in archaebacterial and vertebrate retinylidene photosensors.

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Selected References

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  1. Baselt D. R., Fodor S. P., van der Steen R., Lugtenburg J., Bogomolni R. A., Mathies R. A. Halorhodopsin and sensory rhodopsin contain a C6-C7 s-trans retinal chromophore. Biophys J. 1989 Jan;55(1):193–196. doi: 10.1016/S0006-3495(89)82791-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blanck A., Oesterhelt D., Ferrando E., Schegk E. S., Lottspeich F. Primary structure of sensory rhodopsin I, a prokaryotic photoreceptor. EMBO J. 1989 Dec 20;8(13):3963–3971. doi: 10.1002/j.1460-2075.1989.tb08579.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Braiman M., Mathies R. Resonance Raman spectra of bacteriorhodopsin's primary photoproduct: evidence for a distorted 13-cis retinal chromophore. Proc Natl Acad Sci U S A. 1982 Jan;79(2):403–407. doi: 10.1073/pnas.79.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chabre M. Trigger and amplification mechanisms in visual phototransduction. Annu Rev Biophys Biophys Chem. 1985;14:331–360. doi: 10.1146/annurev.bb.14.060185.001555. [DOI] [PubMed] [Google Scholar]
  5. Eyring G., Curry B., Mathies R., Fransen R., Palings I., Lugtenburg J. Interpretation of the resonance Raman spectrum of bathorhodopsin based on visual pigment analogues. Biochemistry. 1980 May 27;19(11):2410–2418. doi: 10.1021/bi00552a020. [DOI] [PubMed] [Google Scholar]
  6. Fodor S. P., Gebhard R., Lugtenburg J., Bogomolni R. A., Mathies R. A. Structure of the retinal chromophore in sensory rhodopsin I from resonance Raman spectroscopy. J Biol Chem. 1989 Nov 5;264(31):18280–18283. [PubMed] [Google Scholar]
  7. Ganter U. M., Schmid E. D., Perez-Sala D., Rando R. R., Siebert F. Removal of the 9-methyl group of retinal inhibits signal transduction in the visual process. A Fourier transform infrared and biochemical investigation. Biochemistry. 1989 Jul 11;28(14):5954–5962. doi: 10.1021/bi00440a036. [DOI] [PubMed] [Google Scholar]
  8. Groenendijk G. W., De Grip W. J., Daemen F. J. Quantitative determination of retinals with complete retention of their geometric configuration. Biochim Biophys Acta. 1980 Mar 21;617(3):430–438. doi: 10.1016/0005-2760(80)90009-0. [DOI] [PubMed] [Google Scholar]
  9. Henderson R., Baldwin J. M., Ceska T. A., Zemlin F., Beckmann E., Downing K. H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol. 1990 Jun 20;213(4):899–929. doi: 10.1016/S0022-2836(05)80271-2. [DOI] [PubMed] [Google Scholar]
  10. Kalisky O., Ottolenghi M., Honig B., Korenstein R. Environmental effects on formation and photoreaction of the M412 photoproduct of bacteriorhodopsin: implications for the mechanism of proton pumping. Biochemistry. 1981 Feb 3;20(3):649–655. doi: 10.1021/bi00506a031. [DOI] [PubMed] [Google Scholar]
  11. Maeda A., Asato A. E., Liu R. S., Yoshizawa T. Interaction of aromatic retinal analogues with apopurple membranes of Halobacterium halobium. Biochemistry. 1984 May 22;23(11):2507–2513. doi: 10.1021/bi00306a029. [DOI] [PubMed] [Google Scholar]
  12. Muradin-Szweykowska M., Pardoen J. A., Dobbelstein D., Van Amsterdam L. J., Lugtenburg J. Bacteriorhodopsins with chromophores modified at the beta-ionone site. Formation and light-driven action of the proton pump. Eur J Biochem. 1984 Apr 2;140(1):173–176. doi: 10.1111/j.1432-1033.1984.tb08082.x. [DOI] [PubMed] [Google Scholar]
  13. Nathans J. Molecular biology of visual pigments. Annu Rev Neurosci. 1987;10:163–194. doi: 10.1146/annurev.ne.10.030187.001115. [DOI] [PubMed] [Google Scholar]
  14. Oesterhelt D., Schuhmann L. Reconstitution of bacteriorhodopsin. FEBS Lett. 1974 Aug 30;44(3):262–265. doi: 10.1016/0014-5793(74)81153-1. [DOI] [PubMed] [Google Scholar]
  15. Rao V. J., Zingoni J. P., Crouch R., Denny M., Liu R. S. Isomers of 3,7,11-trimethyldodeca-2,4,6,8,10-pentaenal (a linear analogue of retinal) and lower homologues in their interaction with bovine opsin and bacterioopsin. Photochem Photobiol. 1985 Feb;41(2):171–174. doi: 10.1111/j.1751-1097.1985.tb03467.x. [DOI] [PubMed] [Google Scholar]
  16. Schreckenbach T., Walckhoff B., Oesterhelt D. Studies on the retinal-protein interaction in bacteriorhodopsin. Eur J Biochem. 1977 Jun 15;76(2):499–511. doi: 10.1111/j.1432-1033.1977.tb11620.x. [DOI] [PubMed] [Google Scholar]
  17. Spudich E. N., Sundberg S. A., Manor D., Spudich J. L. Properties of a second sensory receptor protein in Halobacterium halobium phototaxis. Proteins. 1986 Nov;1(3):239–246. doi: 10.1002/prot.340010306. [DOI] [PubMed] [Google Scholar]
  18. Spudich J. L., Bogomolni R. A. Mechanism of colour discrimination by a bacterial sensory rhodopsin. Nature. 1984 Dec 6;312(5994):509–513. doi: 10.1038/312509a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Spudich J. L., Bogomolni R. A. Sensory rhodopsins of halobacteria. Annu Rev Biophys Biophys Chem. 1988;17:193–215. doi: 10.1146/annurev.bb.17.060188.001205. [DOI] [PubMed] [Google Scholar]
  20. Spudich J. L., McCain D. A., Nakanishi K., Okabe M., Shimizu N., Rodman H., Honig B., Bogomolni R. A. Chromophore/protein interaction in bacterial sensory rhodopsin and bacteriorhodopsin. Biophys J. 1986 Feb;49(2):479–483. doi: 10.1016/S0006-3495(86)83657-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stoeckenius W. A model for the function of bacteriorhodopsin. Soc Gen Physiol Ser. 1979;33:39–47. [PubMed] [Google Scholar]
  22. Stoeckenius W., Bogomolni R. A. Bacteriorhodopsin and related pigments of halobacteria. Annu Rev Biochem. 1982;51:587–616. doi: 10.1146/annurev.bi.51.070182.003103. [DOI] [PubMed] [Google Scholar]
  23. Takahashi T., Yan B., Mazur P., Derguini F., Nakanishi K., Spudich J. L. Color regulation in the archaebacterial phototaxis receptor phoborhodopsin (sensory rhodopsin II). Biochemistry. 1990 Sep 11;29(36):8467–8474. doi: 10.1021/bi00488a038. [DOI] [PubMed] [Google Scholar]
  24. Tsuda M., Nelson B., Chang C. H., Govindjee R., Ebrey T. G. Characterization of the chromophore of the third rhodopsin-like pigment of Halobacterium halobium and its photoproduct. Biophys J. 1985 May;47(5):721–724. doi: 10.1016/S0006-3495(85)83969-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yan B., Takahashi T., Johnson R., Derguini F., Nakanishi K., Spudich J. L. All-trans/13-cis isomerization of retinal is required for phototaxis signaling by sensory rhodopsins in Halobacterium halobium. Biophys J. 1990 Apr;57(4):807–814. doi: 10.1016/S0006-3495(90)82600-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yan B., Takahashi T., McCain D. A., Rao V. J., Nakanishi K., Spudich J. L. Effects of modifications of the retinal beta-ionone ring on archaebacterial sensory rhodopsin I. Biophys J. 1990 Mar;57(3):477–483. doi: 10.1016/S0006-3495(90)82564-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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