Abstract
In invertebrates, a large body of evidence about the molecular mechanisms governing the visual cascade has been derived from the molecular genetic dissection of the components of the Drosophila photoreceptor machinery (1 – 5). As the best genetically characterized metazoan system, Drosophila provides an advantage in some respects over the mammalian system in that the genes can be both molecularly and genetically dissected facilitating the association of a particular gene product with its in vivo cellular function. Several of the Drosophila mutants identified with changes in the light evoked responses also lead to photoreceptor degeneration. These are of particular interest, as retinal degeneration is a major cause of inherited blindness in humans. In addition, electrophysiological studies in Limulus photoreceptors cells have also provided us with an important insight into the physiology of the invertebrate visual cascade (6).
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Pak, W. L., Grossfield, J., and White, N.V. (1969). Nonphototactic mutants in a study of vision of Drosophila. Nature (London) 222, 351–354.
Pak, W. L., Grossfield, J., and Arnold, K. (1970). Mutants of the visual pathway of Drosophila melanogaster. Nature (London) 227, 518–520.
Pak, W. L. (1979) Study of photoreceptor function using Drosophila mutants. In Breakefield XO (ed): “Neuro genetics: Genetic Approaches to the Nervous System,” New York: Elsevier North Holland, pp 67–99.
Pak, W. L. (1991) Molecular genetic studies of photoreceptor function using Drosophila mutants. In D. Farber and G. Chader (ed): “Molecular Biology of the Retina: Basic Clinically Relevant Studies,” New York: Wiley-Liss, Inc. pp 1–32.
Ranganathan, R., Harris, W. A., and Zucker, C.S. (1991). The molecular genetics of invertebrate phototransduction. Trends in Neuroscience 14, 486–493.
Payne, R. (1986). Phototransduction by microvillar photoreceptors of invertebrates: mediation of a visual cascade by inositol triphosphate. Photobiochem. Photobiophys. 13, 373–397.
Pugh Jr., E. N., and Lamb, T. D. (1990). Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res. 30, 1923–1948.
Stryer, L. (1991). Visual excitation and recovery. J. Biol. Chem. 266, 10711–10714.
Kaupp, U. B., and Koch, K.-W. (1992). Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu. Rev. Physiol. 54, 153–175.
Wright, A. F. (1992). New insights into genetic eye disease. Trends in Genetics 8, 85–91.
Hargrave, P. A. and McDowell, J. H. (1992). Rhodopsin and phototransduction: a model system for G-protein-linked receptors. The FASEB J. 6, 2323–2331.
O’Tousa, J. E. and Pak, W. L. (1988). Molecular analysis of visual pigments genes. Photobiochem. Photobiol. 47, 877–882.
Palczewski, K., Buczylko, J., Lebioda, L., Crabb, J. and Polans, A. (1993). Identification of the N-terminal region in rhodopsin kinase involved in its interaction with rhodopsin. J. Biol. Chem. 268, 6004–6013.
Kelleher, D. J. and Jonhson, G.L. (1986). Phosphorylation of rhodopsin by protein kinase C in vitro. J. Biol. Chem. 261, 4749–4757.
Doza, Y.N., Minke, B., Chorev, M. and Selinger, Z. (1992). Characterization of fly rhodopsin kinase. Eur. J. Biochem. 209, 1035–1040.
Dolf, P. J., Ranaganathan, R., Colley, N. J., Hardy, R. W., Socolich, M. and Zucker, C. S. (1993). Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 260, 1910–1916.
Gurevich, V. V., and Benovic, J. L. (1993). Visual arrestin interaction with rhodopsin. J. Biol. Chem. 268, 11628–11638.
Payne, R., Flores, T. M. and Fein, A. (1990) Feedback inhibition by calcium limits the release of calcium by inositol triphosphate in Limulus ventral photoreceptors. Neuron 4, 547–555.
Sandier, C. and Kirschfeld, K. (1991). Light-induced extracellular calcium and sodium concentration changes in the retina of Calliphora: involvement in the mechanism of light adaptation. J. Comp. Physiol. 169, 229–311.
Hardie, R. C. and Minke, B. (1993). Novel Ca2+ channels underlying transduction in drosophila photoreceptors: implications for phosphoinositide-mediated Ca2+ mobilization. Trends in Neuroscience 76, 371–376.
Ranganathan, R., Bacskai, B., Tsien, R. and Zucker, C.S. (1994). Cytosolic calcium transients: spatial localization and role in Drosophila photoreceptor cell function. Neuron 13, 837–848.
Hardie, R. C. (1995). Photolysis of caged Ca2+ facilitates and inactivates but does not directly excite light-sensitive channels in Drosophila photoreceptors. J. Neuroscience 15, 889–902.
Fain, G. L. and Matthews, H. R. (1990). Calcium and the mechanism of light adaptation in vertebrate photoreceptors. Trends in Neuroscience 13, 378–384.
Gray-Keller, M. P. and Detwiler, P. B. (1994). The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13, 849–861.
Lee, Y.-J., Shah, S., Suzuki, E., Zars, T., O’Day, P. and Hyde, D. R. (1994) The Drosophila dgq gene encodes a Ga protein that mediates phototransduction. Neuron 13, 1143–1157.
Fung, B. K.-K. (1987) Transducin:structure, function, and role in phototransduction. In Osborne N. N., Chader G. J., eds. “Progress in Retinal Research,” Oxford: Pergamon Press, 6, 151–177.
Bloomquist, B. T., Shortridge, R. D., Schneuwly, S., Perdew, M., Montell, C., Steller, H., Rubin, G., and Pak, W. L. (1988). Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54, 723–733.
Hotta, Y., and Benzer, S. (1970). Genetic dissection of the Drosophila nervous system by means of mosaics. Proc. Natl. Acad. Sci. USA 67, 1156–1163.
Inoue, H. Yoshioka, T. and Hotta, Y. (1985). A genetic study of inositol triphosphate involvement in phototransduction using Drosophila mutants. Biochem. Biophys. Res. Commun. 132, 513–519.
Meyertholen, E. P., Stein, P. J., Williams, M. A., and Ostroy, S. E. (1987). Studies of the Drosophila norpA phototransduction mutant, II. Photoreceptor degeneration and rhodopsin maintenance. J. Comp. Physiol. 161, 793–798.
Bowes, C., Li, T. Danciger, M., Baxter, L., Applebury, M., and Farber, D. (1990) Retinal degeneration in the rd mouse is caused by a defect in the b subunit of the rod cGMP-phosphodiesterase. Nature 347, 677–680.
Lem, J., Flannery, J., Li, T., Applebury, M., Färber, D. and Simon, M. (1992) Retinal degeneration is rescued in transgenic rd mice by expression of the cGMP phosphodiesterase b subunit. Proc. Natl. Acad. Sci. USA 89, 4422–4426.
Farber, D. B. and Lolley, R. N. (1974) Cyclic guanosine monophosphate: elevations in degenerating photoreceptor cells of the C3H mouse retina. Science 186, 449–451.
Farber, D. B. and Lolley, R. N. (1976) Enzymatic basis for cyclic GMP accumulation in degenerative photoreceptor cells of mouse retina. J. Cyclic Nucleotide Res. 2, 139–148.
Hardie, R. and Minke, B. (1992). The trp gene is essential for a light-activated Ca2+ channle in Drosophila photoreceptors. Neuron 8, 643–651.
Phillips, A. M., Bull, A. and Kelly, L. E. (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8, 631–642.
Yau, K.-W. (1994). Phototransduction mechanism in retinal rods and cones. Invest. Ophtalmol. Vis. Sci. 36, 263–275.
Johnson, E. C., Robinson, P. R., and Lisman, J. E. (1986). Cyclic GMP is involved in the excitation of invertebrate photoreceptors. Nature 324, 468–470.
Bacigalupo, J., Johnson, E., Vergara, C., and Lisman, J. (1991). Light-dependent channels from excised patches of Limulus ventral photoreceptors are open by cGMP. Proc. Natl. Acad. Sci. USA 88, 7938–7942.
Fein, A., Payne, R., Corson, D. W., Berridge, M. J. and Irvine, R. (1984) Photoreceptor excitation and adaptation by inositol 1,4,5-triphosphate. Nature 311, 157–160.
Brown, J., Rubin, L., Ghalayini, A., Tarver, A., Irvine, R., Berridge, M. and Anderson, R. E. (1984) Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus phootreceptors. Nature 311, 160–162.
Shin, J., Richard, E. and Lisman, J. E. (1993). Ca2+ is an obligatory intermediate in the excitation cascade of Limulus photoreceptors. Neuron, 77, 845–855.
Anderson, R. E., and Brown, J. E. (1988). Phosphoinositides in the retina. In Osborne N. N. and Chader G. J., eds. “Progress in Retinal Research,” Oxford: Pergamon Press, 9, 211–228.
Das, N. D., Yoshioka, T., Samuelson, D., and Shichi, H. (1986). Immunocytochemical localization of phosphatidyl-4,5-biphosphate in dark-and light-adapted rat retinas. Cell Struc. Funct. 77, 53–63.
Gehm, B. D., and McConnel, D. G. (1990). Phosphatidylinositol-4,5-biphosphate phospholipase C in bovine rod outer segments. Biochemistry 29, 5447–5452.
Ghalayini, A., and Anderson, R. E. (1984). Phosphatidylinositol 4,5-bisphosphate: light-mediated breakdown in the vertebrate retina. Biochem. Biophys. Res. Comm. 124, 503–506.
Hayashi, F., and Amakawa, T. (1985). Light-mediated breakdown of phosphatidylinositol-4,5-biphosphate in isolated rod outer segments of frog photoreceptor. Biochem. Biophy. Res. Comm. 128, 954–959.
Jelsema, C. L. (1989). Regulation of phospholipase A2 and phospholipase C in rod outer segments of bovine retina involves a common GTP-binding protein but different mechanisms of action. Ann. N. Y. Acad. Sci. 559, 158–177.
Jelsema, C. L., and Axelrod, J. (1987). In Sensory Transduction (Discussions in Neurosciences), Hudspeth, A., Macleish, P., Margolis, F. eds. (Foundations for the Study of the Nervous System, Geneva), Vol. 4, 79–84.
Millar, F., and Hawthorne, J. (1985). Polyphosphoinositide metabolism in response to light stimulation of retinal rod outer segments. Biochem. Soc. Trans. 13, 984–985.
Millar, F. A., Fisher, S. C., Muir, C. A., Edwards, E., and N., H. J. (1988). Polyphosphoinositide hydrolysis in response to light stimulation of rat and chick retina and retinal rod outer segments. Biochem. Biophys. Acta 970,205–211.
Yoshioka, T., and Inoue, H. (1987). Inositol phospholipid in visual excitation. Neurosc. Res. Suppl. 6, S15–S24.
Ghalayini, A., Tarver, A., Mackin, W.M., Koutz, C.A. and Anderson, R. E. (1991) Identification and immunolocalization of phospholipase C in bovine rod outer segments. J. Neurochem. 57, 1405–1412.
Peng, Y.-W., Sharp, A. H., Snyder, S. H., and Yau, K.-W. (1991). Localization of the inositol 1,4,5-triphosphate receptor in synaptic terminals in the vertebrate retina. Neuron 6, 525–531.
Day, N. S., Koutz, C. A. and Anderson, R. E. (1993). Inositol-1,4,5-trisphosphate receptors in the vertebrate retina. Current Eye Res. 12, 981–992.
Bonigk, W., Altenhofen, W., Muller, F., Dose, A., Illing, M., Molday, R. S., and Kaupp, U. B. (1993). Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron 10, 865–877.
Haynes, L. W., and Yau, K.-W. (1990). Single channel measurement from the cGMP-activated conductance of catfish retinal cones. J. Physiol. 429, 451–481.
Lerea, C. L., Bunt-Milam, A. H., and Hurley, J. B. (1989). a-transducin is present in blue-, green-,and red-sensitive cone photoreceptors in the human retina. Neuron 3, 367–376.
Li, T., Volpp, K., and Applebury, M. L. (1990). Bovine cone photoreceptor cGMP phosphodiesterase structure deduced from a cDNA clone. Proc. Natl. Acad. Sci. USA 87, 293–297.
Tomita, T. (1965). Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb. Symp. Quant. Biol. 30, 559–566.
Solessio, E., and Engbretson, G. A. (1993). Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards. Nature 364, 442–445.
Rohlich, P., van Veen, Th. and Szel, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.
Rhee, S.-G., Suh, P.-G., Ryu, S.-H., and Lee, S. (1989). Studies of inositol phospholipid-specific phospholipase C. Science 244, 546–550.
Ferreira, P., Shortridge, R. and Pak, W. (1991). Identification and characterization of norpA-like retina-specific bovine cDNA”. Molecular Neurobiology of Drosophila, pg. 51, Cold Spring Harbor, New York.
Ferreira, P. and Pak, W. (1992). Retina-specific bovine cDNAs encoding homologs of the norpA and ninaA proteins of Drosophila. Society for Neuroscience, vol. 18, pg.137.
Ferreira, P., Shortridge, R., and Pak, W. (1993). Distinctive subtypes of bovine phospholipase C that have preferential expression in the retina and high homology to the norpA gene product of Drosophila. Proc. Natl. Acad. Sci. USA 90, 6042–6046.
Nakagawa, T., Okano, H., Furuichi, T., Aruga, J., and Mikoshiba, K. (1991). The subtypes of the mouse inositol 1,4,5-triphosphate receptor are expressed in a tissue-specific and developmentally specific manner. Proc. Natl. Acad. Sci. USA 88, 6244–6248.
Shortridge, R., Yoon, J., Lending, C., Bloomquist, B., Perdew, M., and Pak, W. (1991). A Drosophila phospholipase C gene that is expressed in the central nervous system. J. Biol. Chem. 266, 12474–12480.
Katan, M., Kriz, R., Totty, N., Philip, R., Moldrum, E., Aldape, R., Knopf, J., and Parker, P. (1988). Determination of the primary structure of PLC-154 demonstrates diversity of phosphoinositide-specific phospholipase C activities. Cell 54, 171–177.
Park, D., Jhon, D.-Y, Kriz, R., Knopf, J. and Rhee, S. G. (1992). Cloning, sequencing, expression, and Gq-independent activation of phospholipase C-b2. J. Biol. Chem. 267, 16048–16055.
Stahl M.L., Ferenz, C.R., Kelleher, K.L., Kriz, R.W., Knopf, J.L. (1988). Sequence similarity of phospholipase C with the non-catalytic region of src. Nature 332, 269–272.
Shu, P.-G., Ryu, S., Moon, K.H., Suh, H.W. and Rhee, S. G. (1988). Cloning and sequencing of multiple forms of phospholipase C. Cell 54, 161–169.
Bourne, H. R., Sanders, D. A., and McCormick, F. (1991). The GTPase superfamily: conserved structure and molecular mechanism. Nature (London) 349, 117–127.
Rechsteiner, M. (1990). PEST sequences are signals for rapid intracellular proteolysis. Sem. Cell Biol. 1, 433–440.
Carter-Dawson, L. and LaVail, M. (1979). Rods and cones in the mouse retina. J. Comp. Neur. 188, 245–262.
Ferreira, P. and Pak, W. (1994). Bovine phospholipase C highly homologous to the norpA protein of Drosophila expressed specifically in cones. J. Biol. Chem., 269, 3129–3131.
Schneuwly, S., Burg, M., Lending, C., Perdew, M., and Pak, W. L. (1991). Proprieties of photoreceptor-specific phospholipase C encoded by the norpA gene of Drosophila melanogaster. J. Biol. Chem. 266, 24314–24319.
Zhu, L., McKay, R., and Shortridge, R. (1993). Tissue-specific expression of phopholipase C encoded by the norpA gene of Drosophila melanogaster. J. Biol. Chem. 268, 15994–16001.
Min, D. S., Kim, D., Lee, Y., Seo, J., Suh, P.-G. and Ryu, S. H. (1993) Purification of a novel phospholipase C isozyme from bovine cerebellum. J. Biol. Chem. 268, 12207–12212.
Lee, C.-W., Park, D. J., Lee, K.-H., Kim, C. G., and Rhee, S. G. (1993). Purification, molecular cloning, and sequencing of phospholipase C-b4. J. Biol. Chem., 268, 21318–21327.
Stephenson, R. S., O’Tousa, J., Scavarda, N. J., Randall, L. L., and Pak, W. L. (1983). Drosophila mutants with reduced opsin content. In D. J. Cosens, & D. Vince-Price (Ed.), The Biology of Photoreception (pp. 447–501). Soc. Exp. Biol., Cambridge, U.K.: Cambridge University Press.
Larrivee, D. C., Conrad, S. K., Stephenson, R. S., and Pak, W. L. (1981). Mutation that selectively affect rhodopsin concentration in the peripheral photoreceptors of Drosophila. J. Gen. Physiol. 78, 521–545.
Schneuwly, S., Shortridge, R., Larrivee, D., Ono, T., Ozaki, M., and Pak, W. (1989). Drosophila ninaA gene encodes an eye-specific cyclophilin (cyclosporine A binding protein). Proc. Natl. Acad. Sci. USA 86, 5390–5394.
Shieh, B.-H., Stamnes, M. A., Seavello, S., Harris, G. L., and Zuker, C. S. (1989). The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporin A-binding protein. Nature 338, 67–70.
Stamnes, A. M., Shieh, B.-H., Chuman, L., Harris, L. G., and Zuker, C. S. (1991). The cyclophilin homolog ninaA is a tissue-specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell 65, 219–227.
Fisher, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F. X. (1989). Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337, 476–478.
Takahashi, N., Hayano, T., and Suzuki, M. (1989). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337, 473–475.
Ondek, B., Hardy, R., Baker, E., Stamnes, M., Shieh, B.-H., and Zuker, C. (1992). Genetic dissection of cyclophilin function. J. Biol. Chem. 267, 16460–16466.
Baker, E.K., N.C. Colley, & Zuker, C.S. (1994). The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J. 13, 4886–4895.
Ferreira, P. and Pak, W. (1993). Retina-specific bovine homologs of ninaA. Molecular Neurobiology of Drosophila, pg. 158, Cold Spring Harbor, New York.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1995 Springer Science+Business Media New York
About this chapter
Cite this chapter
Ferreira, P.A., Pak, W.L. (1995). Characterization of Vertebrate Homologs of Drosophila Photoreceptor Proteins. In: Anderson, R.E., LaVail, M.M., Hollyfield, J.G. (eds) Degenerative Diseases of the Retina. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-1897-6_30
Download citation
DOI: https://doi.org/10.1007/978-1-4615-1897-6_30
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-5774-2
Online ISBN: 978-1-4615-1897-6
eBook Packages: Springer Book Archive