Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T17:03:03.909Z Has data issue: false hasContentIssue false

Light-modulated subcellular localization of the alpha-subunit of GTP-binding protein Gq in crayfish photoreceptors

Published online by Cambridge University Press:  02 June 2009

Akihisa Terakita
Affiliation:
Institute of Biology, Oita University, Oita 870-11, Japan
Hideki Takahama
Affiliation:
Institute of Biology, Oita University, Oita 870-11, Japan
Satoshi Tamotsu
Affiliation:
First Department of Physiology, Hamamatsu University School of Medicine, Hamamatsu 431-31, Japan
Tatsuo Suzuki
Affiliation:
Department of Pharmacology, Hyogo College of Medicine, Nishinomiya 663, Japan
Takahiko Hariyama
Affiliation:
Graduate School of Information Sciences, SKK Building, Tohoku University, Sendai 980-77, Japan
Yasuo Tsukahara
Affiliation:
Graduate School of Information Sciences, SKK Building, Tohoku University, Sendai 980-77, Japan Photodynamics Research Center, The Institute of Chemical and Physical Research (RIKEN), Aoba-ku Koeji, Sendai 980, Japan

Abstract

Gq-type GTP-binding protein (Gq) plays an important role in invertebrate visual phototransduction. The subcellular localization of the alpha subunit of visual Gq in crayfish photoreceptor was investigated immunocytochemically and biochemically to demonstrate the details of the rhodopsin-Gq interaction. The localization of Gq(alpha) changed depending on the light condition. In the dark, Gq(alpha) was localized in the whole rhabdoms as the membrane-bound form. In the light, half of the Gq(alpha) was localized in the cytoplasm as the soluble form. The translocation of Gq(alpha) was reversible. The light-modulated translocation possibly controls the amount of Gq that can be activated by rhodopsin. In vitro hydroxylamine treatment of rhabdomeric membranes suggested that the translocation was regulated by the fatty-acid modification of Gq(alpha).

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bernards, H. (1916). Der Bau des Komplexauges von Astacus fluviatilis (Potamobius astacus L.). Zeitschrift für Wissenschftliche Zooligie 116, 649707.Google Scholar
Brann, M. R. & Cohen, L. V. (1987). Diurnal expression of transducin mRNA and translocation of transducin in rods of rat retina. Science 235, 585587.CrossRefGoogle ScholarPubMed
Camp, L. A. & Hofmann, S. L. (1993). Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. Journal of Biological Chemistry 268, 2256622574.Google Scholar
Chabre, M. & Deterre, P. (1989). Molecular mechanism of visual transduction. European Journal of Biochemistry 179, 255266.Google Scholar
Cummins, D. & Goldsmith, T. H. (1981). Cellular identification of the violet receptor in the crayfish eyes. Journal of Comparative Physiology A 142, 199202.Google Scholar
De Court, H. G. & Sigmund, C. (1985). Monoclonal antibodies to crayfish rhodopsin. I. Biochemical characterization and cross-reactivity. European Journal of Cell Biology 38, 106112.Google Scholar
Krebs, W. & Lietz, R. (1982). Apical region of the crayfish retina. Cell and Tissue Research 222, 409415.Google Scholar
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage. Nature 227, 680685.CrossRefGoogle ScholarPubMed
Lee, Y.-J., Dobbs, M. B., Verardi, M. L. & Hyde, D. R. (1990). dgq: A Drosophila gene encoding a visual system-specific Gα molecule. Neuron 5, 889898.Google Scholar
Lee, Y.-J., Shah, S., Suzuki, E., Zars, T., O'Dav, P. M. & Hyde, D. R. (1994). The Drosophila dgq gene encodes a Gα protein that mediates phototransduction. Neuron 13, 11431157.CrossRefGoogle Scholar
Lerea, C. L., Somers, D. E., Hurley, J. B., Klock, I. B. & Bunt-Milam, A. H. (1986). Identification of specific transducin a sub-units in retinal rod and cone photoreceptors. Science 234, 7780.Google Scholar
Levis, M. J. & Bourne, H. R. (1992). Activation of the α subunit of Gs in intact cells alters its abundance, rate of degradation, and membrane avidity. Journal of Cell Biology 119, 12971307.CrossRefGoogle ScholarPubMed
Linder, M. E., Middleton, P., Hepler, J. R., TausslO, R., Gllman, A. G. & Mumby, S. M. (1993). Lipid modification of G Proteins: a subunits are palmitoylated. Proceedings of the National Academy of Sciences of the U.S.A. 90, 36753679.Google Scholar
Magee, A. I., Koyama, A. H., Malfer, C., Wen, D. & Schlesinger, M. J. (1984). Release of fatty acids from virus glycoproteins by hydroxylamine. Biochimica Biophysica Acta 798, 156166.Google Scholar
Negishi, M., Hashimoto, H. & Ichikawa, A. (1992). Translocation of a subunit of stimulatory guanine nucleotide-binding proteins through stimulation of the prostacyclin receptor in mouse mastocytoma cell. Journal of Biological Chemistry 267, 23632369.CrossRefGoogle Scholar
Nobes, C., Baverstock, J. & Saibil, H. (1992). Activation of the GTP-binding protein Gq by rhodopsin in squid photoreceptors. Biochemical Journal 287, 545548.CrossRefGoogle ScholarPubMed
Parenti, M., Vigano, M. A., Newman, C. M. H., Milligan, G. & Magee, A. I. (1993). A novel N-terminal motif for palmitoylation of G-protein α subunits. Biochemical Journal 291, 349353.Google Scholar
Philp, N. J., Chang, W. & Long, K. (1987). Light-stimulated protein movement in rod photoreceptor cells of the rat retina. FEBS Letters 225, 127132.Google Scholar
Pottinger, J. D. D., Ryba, N. J. P., Keen, J. N. & Findlay, J. B. C. (1991). The identification and purification of the heterotrimeric GTP-binding protein from squid (Loligo forbesi) photoreceptors. Biochemical Journal 279, 323326.Google Scholar
Ranganathan, R., Harris, W. A. & Zuker, C. S. (1991). The molecular genetics of invertebrate phototransduction. Trends in Neuro-science 11, 486493.Google Scholar
Ransnäs, L. A., Svoboda, P., Jasper, J. R. & Insel, P. A. (1989). Stimulation of β-adrenergic receptors of S49 lymphoma cells redistributes the α subunit of the stimulatory G protein between cytosol and membranes. Proceedings of the National Academy of Sciences of the U.S.A. 86, 79007903.CrossRefGoogle ScholarPubMed
Rayer, B., Naynert, M. & Stieve, H. (1990). Phototransduction: Different mechanisms in vertebrates and invertebrates. Journal of Photochemistry and Photobiology 7, 107148.Google Scholar
Roof, D. J. & Heth, C. A. (1988). Expression of transducin in retinal rod photoreceptor outer segments. Science 241, 845846.Google Scholar
Ryba, N. J. P., Findlay, J. B. C. & Reid, J. D. (1993). The molecular cloning of the squid (Loligo forbesi) visual Gq-α subunit and its expression in Saccharomyces cerevisiae. Biochemical Journal 292, 333341.Google Scholar
Simon, M. I., Strathmann, M. P. & Gautam, N. (1991). Diversity of G-proteins in signal transduction. Science 252, 802808.Google Scholar
Strathmann, M. & Simon, M. I. (1990). G-protein diversity: A distinct class of α subunits is present in vertebrates and invertebrates. Proceedings of the National Academy of Sciences of the U.S.A. 87, 91139117.Google Scholar
Stryer, L. (1986). Cyclic GMP cascade of vision. Annual Review of Neuroscience 9, 87119.Google Scholar
Suzuki, T., Narita, K., Yoshihara, K., Nagai, K. & Kito, Y. (1993) Immunochemical detection of GTP-binding protein in cephalopod photoreceptors by anti-peptide antibodies. Zoological Science 10, 425430.Google ScholarPubMed
Suzuki, T., Narita, K., Yoshihara, K., Nagai, K. & Kito, Y. (1995). Phosphatidyl inositol-phospholipase C in squid photoreceptor membrane is activated by stable metarhodopsin via GTP-binding protein, Gq. Vision Research 35, 10111017.CrossRefGoogle ScholarPubMed
Szuts, E. Z., Wood, S. F., Reid, M. S. & Fein, A. (1986). Light stimulates the rapid formation of inositol trisphosphate in squid retinas. Biochemical Journal 240, 929932.CrossRefGoogle ScholarPubMed
Terakita, A., Hariyama, T., Tsukahara, Y., Katsukura, Y. & Tashiro, H. (1993 a). Interaction of GTP-binding protein Gq with photoactivated rhodopsin in the photoreceptor membranes of crayfish. FEBS Letters 330, 197200.Google Scholar
Terakita, A., Tsukahara, Y., Hariyama, T., Seki, T. & Tashiro, H. (1993 b). Light-induced binding of proteins to rhabdomeric membranes in the retina of crayfish (Procambarus clarkii). Vision Research 33, 24212426.Google Scholar
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences of the U.S.A. 76, 43504354.Google Scholar
Veit, M., Nürnberg, B., Spicher, K., Harteneck, C., Ponimaskin, E., Schultz, G. & Schmidt, M. F. G. (1994). The α-subunit of G-proteins G12 and G13 are palmitoylated, but not amidically myris-toylated. FEBS Letters 339, 160164.CrossRefGoogle Scholar
Wedegaertner, P. B., Chu, D. H., Wilson, P. T., Levis, M. J. & Bourne, H. R. (1993). Palmitoylation is required for signaling functions and membrane attachment of Gqα and Gsα. Journal of Biological Chemistry 268, 2500125008.Google Scholar
Wedegaertner, P. B. & Bourne, H. R. (1994). Activation and depalmitoylation of Gsα. Cell 77, 10631070.Google Scholar
Whelan, J. P. & Mcginnis, J. F. (1988). Light-dependent subcellular movement of photoreceptor proteins. Journal of Neuroscience Research 20, 263270.Google Scholar
Yarfitz, S. & Hurley, J. B. (1994). Transduction mechanisms of vertebrate and invertebrate photoreceptor. Journal of Biological Chemistry 269, 1432914332.Google Scholar