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PMID: 10339563 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

How vertebrate and invertebrate visual pigments differ in their mechanism of photoactivation.

Nakagawa M, Iwasa T, Kikkawa S, Tsuda M, Ebrey TG

Abstract

In vertebrate visual pigments, a glutamic acid serves as a negative counterion to the positively charged chromophore, a protonated Schiff base of retinal. When photoisomerization leads to the Schiff base deprotonating, the anionic glutamic acid becomes protonated, forming a neutral species that activates the visual cascade. We show that in octopus rhodopsin, the glutamic acid has no anionic counterpart. Thus, the "counterion" is already neutral, so no protonated form of an initially anionic group needs to be created to activate. This helps to explain another observation-that the active photoproduct of octopus rhodopsin can be formed without its Schiff base deprotonating. In this sense, the mechanism of light activation of octopus rhodopsin is simpler than for vertebrates, because it eliminates one of the steps required for vertebrate rhodopsins to achieve their activating state.

MeSH Terms
Amino Acid Sequence Animals Humans Isomerism Light Microvilli/physiology Molecular Sequence Data Octopodiformes Photoreceptor Cells, Invertebrate/physiology Retinal Pigments/chemistry,physiology Rhodopsin/chemistry,physiology,radiation effects Schiff Bases Sequence Alignment Sequence Homology, Amino Acid Species Specificity Spectrophotometry Vertebrates Vision, Ocular/physiology
Chemicals
Retinal Pigments Schiff Bases Rhodopsin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Nakagawa M
Department of Life Science, Himeji Institute of Technology, Harima Science Garden City, Akoh-gun, Hyogo 678-1297, Japan.
Iwasa T
Kikkawa S
Tsuda M
Ebrey T G
References (20)
20 references, click to expand
  1. Transient spectra of intermediates in the photolytic sequence of octopus rhodopsin.
    Biochim Biophys Acta. 1979 Mar 15;545(3):537-46 PMID: 34434
  2. A novel photointermediate of octopus rhodopsin activates its G-protein.
    FEBS Lett. 1998 Oct 2;436(2):259-62 PMID: 9781691
  3. Resonance Raman spectra of octopus acid and alkaline metarhodopsins.
    Biochim Biophys Acta. 1980 Jul 24;624(1):211-7 PMID: 7407234
  4. Flash photolysis and low temperature photochemistry of bovine rhodopsin with a fixed 11-ene.
    Biophys J. 1981 Aug;35(2):543-6 PMID: 7272450
  5. Cyclic GMP cascade of vision.
    Annu Rev Neurosci. 1986;9:87-119 PMID: 2423011
  6. Resonance Raman spectroscopy of octopus rhodopsin and its photoproducts.
    Biochemistry. 1987 Aug 11;26(16):4941-7 PMID: 3663635
  7. Effect of carboxylic acid side chains on the absorption maximum of visual pigments.
    Science. 1989 Nov 17;246(4932):928-30 PMID: 2573154
  8. Octopus photoreceptor membranes. Surface charge density and pK of the Schiff base of the pigments.
    Biophys J. 1990 Aug;58(2):493-501 PMID: 2207250
  9. Determinants of visual pigment absorbance: identification of the retinylidene Schiff's base counterion in bovine rhodopsin.
    Biochemistry. 1990 Oct 16;29(41):9746-52 PMID: 1980212
  10. Aspartic acid 85 in bacteriorhodopsin functions both as proton acceptor and negative counterion to the Schiff base.
    J Biol Chem. 1992 Dec 25;267(36):25730-3 PMID: 1464589
  11. Infrared studies of octopus rhodopsin. Existence of a long-lived intermediate and the states of the carboxylic group of Asp-81 in rhodopsin and its photoproducts.
    FEBS Lett. 1993 Feb 15;317(3):223-7 PMID: 8425608
  12. Constitutive activation of opsin: influence of charge at position 134 and size at position 296.
    Biochemistry. 1993 Jun 15;32(23):6111-5 PMID: 8099498
  13. A mutant rhodopsin photoproduct with a protonated Schiff base displays an active-state conformation: a Fourier-transform infrared spectroscopy study.
    Biochemistry. 1994 Nov 22;33(46):13700-5 PMID: 7947779
  14. Invertebrate visual pigments.
    Photochem Photobiol. 1995 Jul;62(1):1-16 PMID: 7638252
  15. Activating mutations of rhodopsin and other G protein-coupled receptors.
    Annu Rev Biophys Biomol Struct. 1996;25:287-314 PMID: 8800472
  16. Rhodopsin activation blocked by metal-ion-binding sites linking transmembrane helices C and F.
    Nature. 1996 Sep 26;383(6598):347-50 PMID: 8848049
  17. Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin.
    Science. 1996 Nov 1;274(5288):768-70 PMID: 8864113
  18. Ultraviolet resonance Raman evidence for the absence of tyrosinate in octopus rhodopsin and the participation of Trp residues in the transition to acid metarhodopsin.
    FEBS Lett. 1996 Dec 2;398(2-3):239-42 PMID: 8977115
  19. Rhodopsin: a prototypical G protein-coupled receptor.
    Prog Nucleic Acid Res Mol Biol. 1998;59:1-34 PMID: 9427838
  20. 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):2503-7 PMID: 288039
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-05-25
Pages
6189-92
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC26857
Subset
IM
Grants
NEI NIH HHS · R01 EY001323 · United States
NEI NIH HHS · EY01323 · United States
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