Skip to main content
Log in

Spectral characteristics of fluorophores formed via interaction between all-trans-retinal with rhodopsin and lipids in photoreceptor membrane of retina rod outer segments

  • Published:
Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology Aims and scope

Abstract

It is shown that all-trans-retinal under model conditions of its excessive accumulation in photoreceptor membranes interacts with amino groups of rhodopsin and lipids, forming at least three distinct fluorophores with fluorescence quantum yield 20–40 times higher than that of free all-trans-retinal. These retinal derivatives are likely precursors of photo- and cytotoxic fluorophores of lipofuscin and in particular of A2E. Spectral characteristics of fluorophores have been described. Picosecond time-resolved laser fluorescence spectroscopy was used to study kinetics of fluorescence decay of both free and bound all-trans-retinal; fluorophores were determined and their lifetimes have been measured. Based on calculations it is shown that the decay kinetics of all-trans-retinal derivatives consists of three components with lifetimes equal to 48, 208, and 900 ps; kinetics of free all-trans-retinal is monoexponential with lifetime of 31 ps. The chemical nature of fluorophores with the lifetimes obtained is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Palczewski, K., Jager, S., Buczylko, J., Crouch, R.C., Bredberg, D.L., Hofmann, K.P., Asson-Batres, M.A., and Saari, J.C., Rod Outer Segment Retinol Dehydrogenase: Substrate Specificity and Role in Phototransduction, Biochemistry, 1994, vol. 33, pp. 13741–13750.

    Article  PubMed  CAS  Google Scholar 

  2. Kim, S.R., He J., Yanase, E., Jang, Y.P., Berova, N., Sparrow, J.R., and Nakanishi, K., Characterization of Dihydro-A2PE: An Intermediate in the A2E Biosynthetic Pathway, Biochemistry, 2007, vol. 46, pp. 10122–10129.

    Article  PubMed  CAS  Google Scholar 

  3. Liu, J., Itagaki Y., Ben-Shabat, S., Nakanishi, K., and Sparrow, J.R., The Biosynthesis of A2E, a Fluorophore of Aging Retina, Involves the Formation of the Precursor, A2-PE, in the Photoreceptor Outer Segment Membrane, J. Biol. Chem., 2000, vol. 275, pp. 29354–29360.

    Article  PubMed  CAS  Google Scholar 

  4. Fishkin, N.E., Sparrow, J.R., Allikmets, R., and Nakanishi, K., Isolation and Characterization of a Retinal Pigment Epithelial Cell Fluorophore: An All-trans-Retinal Dimer Conjugate, Proc. Natl. Acad. Sci. USA, 2005, vol. 102, no. 20, pp. 7091–7096.

    Article  PubMed  CAS  Google Scholar 

  5. Fishkin, N.E., Jang, Y.-P., Itagaki, Y., Sparrow, J.R., and Nakanishi, K., A2-Rhodopsin: A New Fluorophore Isolated from Photoreceptor Outer Segments, Org. Biomol. Chem., 2003, vol. 1, pp. 1101–1105.

    Article  PubMed  CAS  Google Scholar 

  6. Rozanowska, M. and Sarna, T., Light-Induced Damage to the Retina: Role of Rhodopsin Chromophore Revisited, Photochem. Photobiol., 2005, vol. 81, pp. 1305–1330.

    Article  PubMed  CAS  Google Scholar 

  7. Kim, S.R., Nakanishi, K., Itagaki, Y., and Sparrow, J., Photooxidation of A2-PE, a Photoreceptor Outer Segment Fluorophore, and Protection by Lutein and Zeaxanthin, Exp. Eye Res., 2006, vol. 82, pp. 828–839.

    Article  PubMed  CAS  Google Scholar 

  8. Ben-Shabat, S., Itagaki, Y,, Jockusch, S., Sparrow, J.R., Turro, N.J., and Nakanishi, K., Formation of a Nonaoxirane from A2E, a Lipofuscin Fluorophore Related to Macular Degeneration, and Evidence of Singlet Oxygen Involvement, Angew. Chem. Int. Ed., 2002, vol. 42, no. 5, pp. 814–817.

    Article  Google Scholar 

  9. Suter, M., Reme, C., Grimm, C., Wenzel, A., Jaattela, M., Esser, P., Kociok, N., and Richter, C., Age-Related Macular Degeneration: The Lipofuscin Component A2E Detaches Pro-Apoptotic Proteins from Mitochondria and Induces Apoptosis in Mammalian Retinal Pigment Epithelial Cells, J. Biol. Chem., 2000, vol. 275, no. 50, pp. 39625–39630.

    Article  PubMed  CAS  Google Scholar 

  10. Wang, J.J., Klein, R., and Smith, W., Cataract Surgery and the 5-Year Incidence of Late-Stage Age-Related Maculopathy: Pooled Findings from the Beaver Dam and Blue Mountains Eye Studies, Ophthalmol., 2003, vol. 110, pp. 1960–1967.

    Article  Google Scholar 

  11. Loguinova, M.Yu., Rostovtseva, Ye.V., Feldman, T.B., and Ostrovsky, M.A, Light Damaging Action of All-trans-Retinal and Its Derivatives on Rhodopsin Molecules in the Photoreceptor Membrane, Biochemistry (Moscow), 2008, vol. 73, no.2, pp. 162–172.

    Google Scholar 

  12. Papermaster, D.S., Preparation of Rod Outer Segments, Methods in Enzymology, Biomembranes, Part H, 1982, vol. 81, pp. 48–52.

    CAS  Google Scholar 

  13. Gorbunkov, M.V., Konyashkin, A.V., Kostryukov, P.V., Morozov, V.B., Olenin, A.N., Rusov, V.A., Telegin, L.S., Tunkin, V.G., Shabalin, Yu.V., and Yakovlev, D.V., Pulsed-Diode-Pumped, All-Solid-State, Electro-Optically Controlled Picosecond Nd:YAG Lasers, Quantum Electronics, 2005, vol. 35, no. 1, pp. 2–6.

    Article  CAS  Google Scholar 

  14. Sachs, K., Maretzki, D., Meyer, C.K., and Hofmann, K.P., Diffusible Ligand All-trans-Retinal Activates Opsin via Palmitoylation-Dependent Mechanism, J. Biol. Chem., 2000, vol. 275, no. 9, pp. 6189–6194.

    Article  PubMed  CAS  Google Scholar 

  15. Ben-Shabat, S., Parish, C.A., Vollmer, H.R., Itagaki, Y., Fishkin, N., Nakanishi, K. and Sparrow, J.R., Biosynthetic Studies of A2E, a Major Fluorophore of Retinal Pigment Epithelial Lipofuscin, J. Biol. Chem., 2003, vol. 277, pp. 7183–7190.

    Article  Google Scholar 

  16. Jockusch, S., Ren, R.X., Jang, Y.P., Itagaki, Y., Vollmer-Snarr, H.R., Sparrow, J.R., Nakanishi, K., and Turro, N.J., Photochemistry of A1E, a Retinoid with a Conjugated Pyridinium Moiety: Competition between Pericyclic Photooxygenation and Pericyclization, J. Am. Chem. Soc., 2004, vol. 126, pp. 4646–4652.

    Article  PubMed  CAS  Google Scholar 

  17. Kochendoerfer, G.G. and Mathies, R.A., Spontaneous Emission Study of the Femtosecond Isomerization Dynamics of Rhodopsin, J. Phys. Chem., 1996, vol. 100, pp. 14526–14532.

    Article  CAS  Google Scholar 

  18. Bachilo, S.M., Bondarev, S.L., and Gillbro, T., Fluorescence Properties of Protonated and Unprotonated Schiff Bases of Retinal at Room Temperature, J. Photochem. Photobiol. B: Biol., 1996, vol. 34, pp. 39–46.

    Article  CAS  Google Scholar 

  19. Takeuchi, S. and Tahara, T., Ultrafast Fluorescence Study on the Excited Singlet-State Dynamics of All-trans-Retinal, J. Phys. Chem., 1997, vol. 101, pp. 3052–3060.

    CAS  Google Scholar 

  20. Tahara, T. and Hamaguchi, H., Picosecond Time-Resolved Fluorescence Study of All-trans Retinal: The Existence of Two Fluorescent Singlet Excited States, Chem. Phys. Lett., 1995, vol. 234, pp. 275–280.

    Article  CAS  Google Scholar 

  21. Harper, W.S. and Gaillard, E.R., A Photochemical Study of (E,E,E,E)-2-[9-(2-Hydroxyethyl)Imino-3,7-Dimethyl-1,3,5,7-Decatrien-1-Y]-1,3,3-Trimethylcyclohexene, a Derivative of All-trans-Retinal and Ethanolamine, Photochem. Photobiol., 2003, vol. 78, no. 3, pp. 298–305.

    Article  PubMed  CAS  Google Scholar 

  22. Fu, P.P., Cheng, S.-H., Coop, L., Xia, Q., Culp, S.J., Tolleson, W.H., Wamer, W.G., and Howard, P.C., Photoreaction, Phototoxicity and Photocarcinogenisity of Retinoids, J. Environ. Sci. Health., Part 3, 2003, vol. C21, no. 2, pp. 165–197.

    CAS  Google Scholar 

  23. Lamb, L.E., Ye, T., Haralampus-Grynaviski, N.M., Williams, T.R., Pawlak, A., Sarna, T., and Simopn, J.D., Primary Photophysical Properties of A2E in Solution, J. Phys. Chem., 2001, vol. 105, pp. 11507–11512.

    CAS  Google Scholar 

  24. Sokolov, A.V., Sokolov, V.S., Feldman, T.B., and Ostrovsky, M.A., Interaction of All-trans-Retinal with Bilayer Lipid Membranes, Biol. Membrany (Rus.), 2008, vol. 25, no. 6, pp. 501–508.

    Google Scholar 

  25. Roberts, J.E., Kukielczak, B.M., Hu, D.N., Miller, D.S., Bilski, P., Sik, R.H., Motten, A.G., and Chignell, C.F., The Role of A2E in Prevention or Enhancement of Light Damage in Human Retinal Pigment Epithelial Cells, Photochem. Photobiol., 2002, vol. 75, no. 2, pp. 184–190.

    Article  PubMed  CAS  Google Scholar 

  26. Pawlak, A., Wrona, M., Rozanowska, M., Zareba, M., Lamb, L.E., Roberts, J.E., Simon, J.D., and Sarna, T., Comparison of the Aerobic Photoreactivity of A2E with Its Precursor Retinal, Photochem. Photobiol., 2003, vol. 77, no. 3, pp. 253–258.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Yu. Loguinova.

Additional information

Original Russian Text © M.Yu. Loguinova, V.E. Zagidullin, T.B. Feldman, Y.V. Rostovtseva, V.Z. Paschenko, A.B. Rubin, M.A. Ostrovsky, 2009, published in Biologicheskie Membrany, 2009, Vol. 26, No. 2, pp. 83–93.

The article was translated by the authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Loguinova, M.Y., Zagidullin, V.E., Feldman, T.B. et al. Spectral characteristics of fluorophores formed via interaction between all-trans-retinal with rhodopsin and lipids in photoreceptor membrane of retina rod outer segments. Biochem. Moscow Suppl. Ser. A 3, 134–143 (2009). https://doi.org/10.1134/S1990747809020056

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1990747809020056

Key words

Navigation