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Regulation of the Visual Cycle: Retinol Dehydrogenase and Retinol Fluorescence Measurements In Vertebrate Retina

Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 533)

Abstract

The initial and only light-activated step in vision is the photoisomerization of the ligand of the visual pigment,11-cis retinal to all-trans retinal, which occurs while being covalently bound to a lysine deep in the membrane region of the visual pigment. This event leads to the activation of the g-protein, transducin, which in turn activates c-gmp phosphodiesterase causing the destruction of c-gmp, the closure of cation channels in the plasma membrane of the photoreceptor, and eventually to the reduction in release of synaptic transmitter to other retinal neurons in the visual pathway. However, the visual pigment containing retinal in its all-trans form is now incapable of absorbing photons in the visual region of the spectrum and can no longer activate the transduction cascade. In order to do so, it must be regenerated into a form that contains 1 1-cis retinal. The biochemical reactions by which this occurs are collectively called the visual cycle. This complex series of reactions is initiated in the photoreceptors themselves, by the reduction of all-trans retinal to all-trans retinol by all-trans retinol dehydrogenase (rdh) and the cofactor nadph. All the subsequent steps in the regeneration of 11-cis retinal take place in the retinal pigment epithelium. Regenerated 11-cis retinal is then transported from the retinal pigment epithelium through the extracellular matrix back to the photoreceptor cells where it condenses with opsin to reform visual pigment.

Keywords

Retinal Pigment Epithelium Outer Segment Dark Adaptation Visual Pigment Cone Photoreceptor 
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References

  1. Alpern, M., Rushton, W. A. and Torii, S., 1970, The attenuation of rod signals by bleachings. J. Physiol. 207(2):449-61.PubMedGoogle Scholar
  2. Blaner, W. S. and Churchich, J. E., 1980, The membrane bound retinol dehydrogenase from bovine rod outer segments. Biochem. Biophys. Res. Commun. 94(3):820-6.PubMedCrossRefGoogle Scholar
  3. Boll, F., 1877, Zur anatomie und physiologie der retina. Arch. Anat. Physiol 4-36. [Translation: 1977, On the anatomy and physiology of the retina. Vis. Res. 17(11-12):1249-65].Google Scholar
  4. Cohen, G. B., Oprian, D. D., and Robinson, P. R., 1992, Mechanism of activation and inactivation of opsin: Role of GIul l3 and Lys296. Biochemistry. 31(50):12592-601.PubMedCrossRefGoogle Scholar
  5. Denton, E. J., 1959, The contributions of the oriented photosensitive and other molecules to the absorption of the whole retina. Proc. R. Soc. (Lond.) Series B. 150:78-94.CrossRefGoogle Scholar
  6. Fain, G. L., Matthews, H. R., and Cornwall, M. C., 1996, Dark adaptation in vertebrate photoreceptors. Trends Neurosci. 19(11):502-7.PubMedCrossRefGoogle Scholar
  7. Fukada Y., and Yoshizawa, T., 1981, Activation of phosphodiesterase in frog rod outer segment by an intermediate of rhodopsin photolysis. II. Biochim. Biophys. Acta. 675(2):195-200.PubMedCrossRefGoogle Scholar
  8. Futterman, S., 1963, Metabolism of the retina. J. Biol. Chem. 238:1145-50.PubMedGoogle Scholar
  9. Futterman, S., Hendrickson, A., Bishop, P. E., Rollins, M. H., and Vacano, E., 1970, Metabolism of glucose and reduction of retinaldehyde in retinal photoreceptors. J. Neurochem. 17(2):149-56.PubMedCrossRefGoogle Scholar
  10. Haeseleer, F., Huang, J., Lebioda, L., Saari, J. C., and Palczewski, K., 1998, Molecular characterization of a novel short-chain dehydrogenase/reductase that reduces all-trans-retinal. J. Biol. Chem. 273(34):21790-9.PubMedCrossRefGoogle Scholar
  11. Harosi, F. I., and MacNichol Jr. E. F., 1974, Dichroic microspectrophotometer: A computer-assisted, rapid, wavelength-scanning photometer for measuring linear dichroism in single cells. J. Opt. Soc. Am. 64(7):903-18.PubMedCrossRefGoogle Scholar
  12. Hofmann, K. P., Pulvermuller, A., Buczylko, J., Van Hooser, P., and Paczewski, K., 1992, The role of arrestin and retinoids in the regeneration pathway of rhodopsin. J. Biol. Chem. 267(22):15701-6.PubMedGoogle Scholar
  13. Hsu, S. C., and Molday, R. S., 1991, Glycolytic enzymes and a GLUT-1 glucose transporter in the outer segments of rod and cone photoreceptor cells. J. Biol. Chem. 266(32):21745-52.PubMedGoogle Scholar
  14. Hsu, S. C., and Molday, R. S., 1994, Glucose metabolism in photoreceptor outer segments. Its role in phototransduction and in NADPH-requiring reactions. J. Biol. Chem. 269(27):17954-9.PubMedGoogle Scholar
  15. Ishiguro, S., Suzuki, Y., Tamai, M., and Mizuno, K., 1991, Purification of retinol dehydrogenase from bovine retinal rod outer segments. J. Biol. Chem. 266(23):15520-4.PubMedGoogle Scholar
  16. Jager, S., Palczewski, K., and Hofmann, K. P., 1996, Opsin/all-trans-retinal complex activates transducin by different mechanisms than photolyzed rhodopsin. Biochemistry. 35(9):2901-8.PubMedCrossRefGoogle Scholar
  17. Jin, J., Crouch, R. K., Corson, D. W., Katz, B. M., MacNichol, E. F., and Cornwall, M. C., 1993, Noncovalent occupancy of the retinal-binding pocket of opsin diminishes bleaching adaptation of retinal cones. Neuron. 11(3):513-22.PubMedCrossRefGoogle Scholar
  18. Kaplan, M. W., Liebman, P. A., 1977, Slow bleach-induced birefringence changes in rod outer segments. J. Physiol. 265(3):657-72.PubMedGoogle Scholar
  19. Kaplan, M. W., 1985, Distribution and axial diffusion of retinol in bleached rod outer segments of frogs (Rana pipiens). Exp. Eye Res. 40(5):721.9.PubMedCrossRefGoogle Scholar
  20. Kefalov, V. J., Crouch, R. K., and Cornwall, M. C., 2001, Role of nncovalent binding of 11-cis-retinal to opsin in dark adaptation of rod and cone photoreceptors. Neuron. 29(3):749-55.PubMedCrossRefGoogle Scholar
  21. Kemp, C. M., 1973, Dichroism in rods during bleaching, In: Langer, H., editor, Biochemistry and Physiology of Visual Pigments. Berlin: Springer-Verlag. p. 307-12.CrossRefGoogle Scholar
  22. Kuhne W., 1879, Chemische vorgange in der netzhaut, (ed. Hermann, L.) Vol. 3 [Translation: Hubbard, R., Wald, G., 1977, Chemical processes in the retina. Vis. Res. 17(11-12):1269-316].Google Scholar
  23. Lamb, T. D., 1980, Spontaneous quantal events induced in toad rods by pigment bleaching. Nature. 287(5780):349-51.PubMedCrossRefGoogle Scholar
  24. Li, X. B., Szerencsei, R. T., and Schnetkamp, P. P., 1994, The glucose transporter in the plasma membrane of the outer segments of bovine retinal rods. Exp. Eye Res. 59(3):351-8.PubMedCrossRefGoogle Scholar
  25. Liebman, P. A., 1969, Microspectrophotometry of retinal cells. Ann. N. Y. Acad. Sci. 157:250-64.CrossRefGoogle Scholar
  26. Lopez-Escalera, R., Li, X. B., and Szerencsei, P. P., 1991, Glycolysis and glucose uptake in intact outer segments isolated from bovine retinal rods. Biochemistry. 30(37):8970-6.PubMedCrossRefGoogle Scholar
  27. McConnell, D. G., Ozga, G. W., and Solze, D. A., 1969, Evidence for glycolysis in bovine retinal microsomes and photoreceptor outer segments. Biochim. Biophys. Acta. 184(1):11-28.PubMedCrossRefGoogle Scholar
  28. Melia Jr., T. J., Cowan, C. W., Angleson, J. K., and Wensel, T. G., 1997, A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin. Biophys. J. 73(6): 3182-91.PubMedCrossRefGoogle Scholar
  29. Nicotra, C., and Livrea, M. A., 1982, Retinol dehydrogenase from bovine retinal rod outer segments. Kinetic mechanism of the solubilized enzyme. J Biol. Chem. 257(19):11836-41.PubMedGoogle Scholar
  30. Palczewski, K., Jager, S., Buczylko, J., Crouch, R. K., Bredberg, D. L., Hofmann, K. P., Asson-Batres, M. A., and Saari, J. C., 1994, Rod outer segment retinol dehydrogenase: Substrate specificity and role in phototransduction. Biochemistry. 33(46):13741-50.PubMedCrossRefGoogle Scholar
  31. Paupoo, A. A., Mahroo, O. A., Friedburg, C., and Lamb, T. D., 2000, Human cone photoreceptor responses measured by the electroretinogram a-wave during and after exposure to intense illumination. J. Physiol. 529(Pt2):469-82.PubMedCrossRefGoogle Scholar
  32. Rattner, A., Smallwood, P. M., and Nathans, J., 2000, Identification and characterization of all-trans-retinol dehydrogenase from photoreceptor outer segments, the visual cycle enzyme that reduces all-trans-retinal to all-trans-retinol. J. Biol. Chem. 275(15):11034-43.PubMedCrossRefGoogle Scholar
  33. Saari, J. C., Garwin, G. G., Van Hooser, J. P., and Palczewski K., 1998, Reduction of all-trans-retinal limits regeneration of visual pigment in mice. Vis. Res. 38(10):1325-33.PubMedCrossRefGoogle Scholar
  34. Sakmar, T. P., Franke, R. R., and Khorana, H. G., 1989, Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Nat. Acad. Sci. U. S. A. 86(21):8309-13.CrossRefGoogle Scholar
  35. Schnetkamp, P. P., and Daemen, F. J., 1981, Transfer of high-energy phosphate in bovine rod outer segments. A nucleotide buffer system. Biochim. Biophys. Acta. 672(3):307-12.PubMedCrossRefGoogle Scholar
  36. Sears, R. C., and Kaplan, M. W., 1989, Axial diffusion of retinol in isolated frog rod outer segments following substantial bleaches of visual pigment. Vis. Res. 29(11):1485-92.PubMedCrossRefGoogle Scholar
  37. Surya, A., Foster, K. W., and Knox, B. E., 1995, Transducin activation by the bovine opsin apoprotein. J. Biot. Chem. 270(10): 5024-31.CrossRefGoogle Scholar
  38. Thomas, M. M., and Lamb, T. D., 1999, Light adaptation and dark adaptation of human rod photoreceptors measured from the a-wave of the electroretinogram. J. Physiol. 518(Pí2): 479-96.PubMedCrossRefGoogle Scholar
  39. Wald, G., 1935, Carotenoids and the visual cycle. J. Gen. PhysioL 19(2):351-71.PubMedCrossRefGoogle Scholar
  40. Wallimann, T., Wegmann, G., Moser, H., Huber, R., and Eppenberger, H. M., 1986, High content of creatine kinase in chicken retina: Compartmentalized localization of creatine kinase isoenzymes in photoreceptor cells. Proc. Nat. Acad. Sci. U. S. A. 83(11):3816-9.Google Scholar
  41. Zimmerman, W. F., Yost, M. T., and Daemen, F. J., 1974, Dynamics and function of vitamin A compounds in rat retina after a small bleach of rhodopsin. Nature. 250(461):66-7.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2003

Authors and Affiliations

  1. 1.Department of Physiology and BiophysicsBoston University School of MedicineBostonUSA
  2. 2.Department of OphthalmologyMedical University of South CarolinaCharlestonUSA
  3. 3.National Eye InstituteNational Institutes of HealthBethesdaUSA
  4. 4.Department of Physiology and BiophysicsUniversity of Colorado School of MedicineDenverUSA

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