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Localization of retinal photoisomerase in the compound eye of the honeybee

Published online by Cambridge University Press:  02 June 2009

W. Clay Smith  and
Timothy H. Goldsmith
W. Clay Smith
Affiliation:
Yale University, Department of Biology, New Haven
Timothy H. Goldsmith
Affiliation:
Yale University, Department of Biology, New Haven
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Abstract

The distribution of honeybee retinal photoisomerase, a soluble light-requiring enzyme that stereospecifically forms W-cis retinal, was investigated by immunoelectron microscopy and by HPLC. Immunolocalization with polyclonal antibodies shows that the highest concentration of retinal photoisomerase is located in the proximal portion of the primary pigment cells in large aggregates (approximately 2 μm diameter).

Photoisomerase is also located in the peripheral portion of the photoreceptor cells, laterally displaced from the rhabdom, but in much lower concentration. Because of the larger volume of the photoreceptor cells, about half of the total immunoreactivity is associated with the primary pigment cells.

Dissection of the eye with the subsequent use of HPLC to assay for photoisomerase activity showed that most of the photoisomerase activity is associated with tissues near the cornea. The same tissue also supports the reduction of W-cis retinal to W-cis retinol. These biochemical findings are consistent with the immunolocalization of retinal photoisomerase to the high-concentration aggregates in the primary pigment cells that surround the crystalline cones. The major synthesis of W-cis retinol therefore takes place in the primary pigment cells, and the retinoid must be moved into the photoreceptor cells to be available to newly synthesized opsin. The immunoreactivity of the photoreceptor cells appears to reflect the presence of some isomerase without an attached retinoid chromophore.

Keywords

PhotoreceptorVisual cyclePhotoisomeraseHoneybee
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 3 , September 1991 , pp. 237 - 249
Copyright
Copyright © Cambridge University Press 1991

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References

Adler, R. & Farber, D. (1986). The Retina: A Model for Cell Biology Studies. Orlando, Florida: Academic Press, Inc.Google Scholar
Baumann, O. & Walz, B. (1989). Topography of Ca2+-sequestering endoplasmic reticulum in photoreceptors and pigmented glial cells in the compound eye of the honeybee drone. Cell and Tissue Research 255, 511–522.CrossRefGoogle Scholar
Boschek, C. (1971). On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Zeitschrift für Zellforschung 118, 369–409.CrossRefGoogle ScholarPubMed
Chi, C. & Carlson, S.D. (1976). The large pigment cell of the compound eye of the house fly (Musca domestica). Cell and Tissue Research 170, 77–88.Google ScholarPubMed
Coles, J.A. (1989). Functions of glial cells in the retina of the honeybee drone. Glia 2, 1–9.CrossRefGoogle ScholarPubMed
Deigner, P.S., Law, W.C., Canada, F.J. & Rando, R.R. (1989). Membrances as the energy source in the endergonic transformation of vitamin A to 11-cis-retinol. Science 244, 968–971.CrossRefGoogle Scholar
Goldsmith, T.H. (1958). The visual system of the honeybee. Proceedings of the National Academy of Sciences of the U.S.A. 44, 123–126.CrossRefGoogle ScholarPubMed
Goldsmith, T.H., Smith, W.C. & Friedman, M.A. (1990). Limulus eyes contain a retinal photoisomerase. Investigative Ophthalmology and Visual Science (Suppl.) 31, 73.Google Scholar
Goldsmith, T.H., Marks, B.C. & Bernard, G.D. (1986). Separation and identification of geometric isomers of 3-hydroxyretinoids and occurrence in the eyes of insects. Vision Research 26, 1763–1769.CrossRefGoogle ScholarPubMed
Goodman, D.S. (1984). Plasma retinol-binding protein. In The Retinoids, Vol 2, ed. Sporn, M.B., Roberts, A.B. & Goodman, D.S., pp. 41–88. Orlando, Florida: Adacemic Press, Inc.CrossRefGoogle Scholar
Hara, T. & Hara, R. (1972). Cephalopod retinochrome. In Handbook of Sensory Physiology, Vol VII/I, ed. Dartnall, H., pp. 720–746. Berlin-Heidelberg-New York: Springer-Verlag.Google Scholar
Isono, K., Tanimura, T., Oda, Y. & Tsukahara, Y. (1988). Dependency on light and vitamin A derivatives of the biogenesis of 3-hydroxyretinal and visual pigment in the compound eyes of Drosophila melanogaster. Journal of General Physiology 92, 587–600.CrossRefGoogle ScholarPubMed
Nowotny, A. (1979). Basic Exercises in Immunocytochemistry. Berlin-Heidelberg-New York: Springer-Verlag.CrossRefGoogle Scholar
Paulsen, R. & Bentrop, J. (1984). Reversible phosphorylation of opsin induced by irradiation of blowfly retinae. Journal of Comparative Physiology A 155, 39–45.CrossRefGoogle Scholar
Pepe, I.M. & Cugnoli, C. (1980). Isolation and characterization of a water-soluble photopigment from honeybee compound eye. Vision Research 20, 97–102.CrossRefGoogle ScholarPubMed
Pepe, I.M., Cugnoli, C., Peluso, N., Vergani, L. & Boero, A. (1987). Structure of a protein catalyzing the formation of 11-cis-retinal in the visual cycle of invertebrate eyes. Cell Biophysics 10, 15–22.CrossRefGoogle ScholarPubMed
Pepe, I.M., Schwemer, J. & Paulsen, R. (1982). Characteristics of retinal-blinding proteins from the honeybee retina. Vision Research 22, 775–781.CrossRefGoogle Scholar
Perrelet, A. (1970). The fine structure of the retina of the honey bee drone: an electron microscopical study. Zeitschrift für Zellforschung 108, 530–562.CrossRefGoogle ScholarPubMed
Perrelet, A. & Baumann, F. (1969). Presence of three small retinula cells in the ommatidium of the honey-bee drone eye. Journal of Microscopy 8, 497–502.Google Scholar
Polak, J.M. & Van Noorden, S. (1983). Immunocytochemistry: Practical Applications in Pathology and Biology. Bristol-London: Wright-PSG.Google Scholar
Pringle, J.W.S. (1938). Proprioception in insects, I: A new type of mechanical receptor from the palps of the cockroach. Journal of Experimental Biology 15, 101–113.CrossRefGoogle Scholar
Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. Journal of Cell Biology 17, 208–212.CrossRefGoogle ScholarPubMed
Schwemer, J. (1984). Renewal of visual pigment in photoreceptors of the blowfly. Journal of Comparative Physiology A 154, 535–547.CrossRefGoogle Scholar
Schwemer, J. (1988). Cycle of 3-hydroxy retinoids in an insect eye. In Molecular Physiology of Retinal Proteins, ed. Hara, T., pp. 299–304. Japan: Yamada Science Foundation.Google Scholar
Schwemer, J. (1989). Visual pigments of compound eyes—structure, photochemistry, and regeneration. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 112–133. Berlin-Heidelberg-New York: Springer-Verlag.CrossRefGoogle Scholar
Schwemer, J., Pepe, I.M., Paulsen, R. & Cugnoli, C. (1984). Light-induced trans-cis isomerization of retinal by a protein from the honeybee retina. Journal of Comparative Physiology A 154, 549–554.CrossRefGoogle Scholar
Smith, W.C. & Goldsmith, T.H. (1991). The role of retinal photoisomerase in the visual cycle of the honeybee. Journal of General Physiology 97, 143–165.CrossRefGoogle ScholarPubMed
Somogyi, P. & Takagi, H. (1982). A note on the use of picric acid-para-formaldehyde-glutaraldehyde fixative for correlated light and electron-microscopic immunocytochemistry. Neuroscience 7, 1779–1783.CrossRefGoogle ScholarPubMed
Timms, B.G. (1986). Postembedding immunogold labeling for electron microscopy using “LR White” resin. American Journal of Anatomy 175, 267–275.CrossRefGoogle ScholarPubMed
Trehan, A., Canada, F.J. & Rando, R.R. (1990). Inhibitors of retinylester formation also prevent the biosynthesis of 11-cis-retinol. Biochemistry 29, 309–312.CrossRefGoogle Scholar
Trujillo-Cenoz, O. & Melamed, J. (1966). Electron microscope observations on the peripheral and intermediate retinas of dipterans. In Functional Organization of the Compound Eye, ed. Bernhard, C., pp. 339–361. Oxford: Pergamon Press.Google Scholar
Vaitukaitis, J.L. (1981). Production of antisera with small doses of immunogen: multiple intradermal injections. Methods in Enzymology 73, 46–52.CrossRefGoogle ScholarPubMed
Varela, F.G. & Porter, K.R. (1969). Fine structure of the visual system of the honeybee (Apis mellifera). I. The retina. Journal of Ultrastructural Research 29, 236–259.CrossRefGoogle ScholarPubMed
Vogt, K. (1983). Is the fly visual pigment a rhodopsin? Zeitschrift für Naturforschung 38 C, 329–333.CrossRefGoogle Scholar
Walz, B. (1983). Association between cytoskeletal microtubules and Ca2+-sequestering smooth ER in Semper cells of fly ommatidia. European Journal of Cell Biology 32, 92–98.Google ScholarPubMed
Wray, W., Boulikas, T., Wray, V.P. & Hancock, R. (1981). Silver staining of proteins in polyacrylamide gels. Analytical Biochemistry 118, 197–203.CrossRefGoogle ScholarPubMed