Abstract
We discuss in this chapter the role of Ca2+homeostasis in maintaining the structural integrity of photoreceptor cells inDrosophila.Both insufficient and excessive amounts of Ca2+in photoreceptor cells appear to lead to cell degeneration. Because one of the two classes of light-sensitive channels inDrosophilaphotoreceptors is highly Ca2+-permeable, how well this class of channels functions can profoundly affect Ca2+homeostasis. We will begin by reviewingDrosophilaphototransduction, emphasizing what is known about the mechanism of activation of light-sensitive channels. We will then describe Ca2+entry through light-sensitive channels and the presumed mechanisms by which too Iittle and too much Ca2+entry can both cause photoreceptor degeneration. We will conclude the chapter with discussions of two examples of mutations known to cause unregulated Ca2+entry through light-sensitive channels, leading to massive photoreceptor degeneration.
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References
Pak WL.Drosophilain vision research. Invest Ophthal Vis Sci 1995; 36:2340–2357.
Zucker CS. The biology of vision inDrosophila.Proc Natl Acad Sci USA 1996; 93:571–576.
Montell C. Visual transduction inDrosophila.Annu Rev Cell Dev Biol 1999; 15:231–268.
Minke B, Hardie RC. Genetic dissection ofDrosophilaPhototransduction. In: Stavenga DG, DeGrip WJ, Pugh Jr EN, eds. Handbook of Biological Physics, Vol. 3, 2000:449–525.
Pak WL, Ostroy SE, Deland MC et al. Photoreceptor mutant ofDrosophila:Is protein involved in intermediate steps of phototransduction? Science 1976; 194:956–959.
Bloomquist BB, Shortridge RD, Schneuwly S et al. Isolation of a putative phospholipase C gene ofDrosophila norpA and it role in phototransduction. Cell 1988; 54:723–733.
Montell C, Rubin GM. Molecular characterization of theDrosophila trplocus: A putative integral membrane protein required for phototransduction. Neuron 1989; 2:1313–1323.
Wong F, Schaefer EL, Roop BC et al. Proper function of theDrosophila trpgene product during pupal development is important for normal visual transduction in the adult. Neuron 1989; 3:81–94.
Hardie RC, Minke B. Thetrpgene is essential for a light activated Ca2+ channel inDrosophilaphotoreceptors. Neuron 1992; 8:643–651.
Phillips AM, Bull A, Kelly LE. Identification of aDrosophilagene encoding a calmodulinbinding protein with homology to the trp phototransduction gene. Neuron 1992; 8:631–642.
Niemeyer BA, Suzuki E, Scott K et al. TheDrosophilalight-activated conductance is composed of the two channels Trp and Trpl. Cell 1996; 85:651–659.
Scott K, Sun Y, Beckingham K et al. Calmodulin regulation ofDrosophilalight-activated channels and receptor function mediates termination of the light response in vivo. Cell 1997; 91:375–383.
Reuss H, Mojet MH, Chyb S et al. In vivo analysis of the Drosophila light-sensitive channels, TRP and TRPL. Neuron 1997; 19:1249–1259.
Xu X-ZS, Li H-S, Guggino WB et al. Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell 1997; 89:1155–1164.
Berridge MJ. Cell signalling-A tale of two messengers. Nature 1993; 365:388–389.
Minke B, Selinger Z. Inositol lipid pathway in fly photoreceptors: Excitation, calcium mobilization and retinal degeneration. In: Osborne NN, Chader GJ, eds. Progress in Retinal Research. Oxford: Pergamon, 1992:99–124.
Ranganathan R, Bacskai BJ, Tsein RY et al. Cytosolic calcium transients: spatial localization and rolein Drosophilaphotoreceptor cell function. Neuron 1994; 13:837–848.
Hardie RC. Calcium signaling: setting store by calcium channels. Curr Biol 1996; 6:1371–1373.
Acharya JK, Jalink K, Hardy RW et al. InsP3 receptor essential for growth and differentiation but not for vision inDrosophila.Neuron 1997; 18:881–887.
Raghu P, Colley NJ, Webel R et al. Normal phototransduction inDrosophilaphotoreceptors lacking an InsP3 receptor gene. Mol and Cell Neurosci 2000; 15:429–445.
Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate theDrosophilalight-sensitive channels TRP and TRPL. Nature 1999; 397:255–259.
Choma-Ornan I, Joel-Almagor T, Ben-Ami HC et al. A common mechanism underlies vertebrate calcium signaling and Drosophila phototransduction. J Neurosci 2001; 21:2622–2629.
Agam K, von Campenhausen M, Levy S et al. Metabolic stress reversibly activates theDrosophilalight-sensitive channels TRP and TRPL in vivo. J Neurosci 2000; 20:5748–5755.
Arslan P, Corps AN, Hesketh TR et al. cis-unsaturated fatty acids uncouple mitochondria and stimulate glycolysis in intact lymphocytes. J Biochem 1984; 217:419–425.
Hermesh O, Kalderon B, Bar TJ. Mitochondria uncoupling by a long chain fatty acyl analogue. J Biol Chem 1998; 273:3937–3942.
Hardie RC. Whole-cell recordings of the light induced current in dissociatedDrosophilaphotoreceptors: evidence for feedback by calcium permeating the light-sensitive channels. Proc Natl Acad Sci USA 1991; 245:203–210.
Peretz A, Sandler C, Kirschfeld K et al. Genetic dissection of light-induced Ca2+ influx intoDrosophilaphotoreceptors. J Gen Physiol 1994; 104:1057–1077.
Raghu P, Usher K, Jonas S et al. Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant, rdgA. Neuron 2000; 26:169–179.
Yoon J, Ben-Ami HC, Hong YS et al. Novel mechanism of massive photoreceptor degeneration caused by mutations in thetrpgene ofDrosophila.J Neurosci 2000; 20:649–659.
Trump BF, Berezesky IK. The role of altered [Ca21; regulation in apoptosis, oncosis, and necrosis. Biochim Biophys Acta 1996; 1313:173–178.
Lee JM, Zipfel GJ, Choi DW. The changing landscape of ischaemic brain injury mechanisms. Nature 1999; 399:A7–A14.
Alloway PG, Howard L, Dolph PJ. The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 2000; 28:129–138.
Byk T, Bar Yaacov M, Doza YN et al. Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proc Natl Acad Sci USA 1993; 90:1907–1911.
Dolph PJ, Ranganathan R, Colley NJ et al. Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 1993; 260:1910–1916.
Vinos J, Jalink K, Hardy RW et al. A G protein-coupled receptor phosphatase required for rhodopsin function. Science 1997; 277:687–690.
Kiselev A, Socolich M, Vinos J et al. A molecular pathway for light-dependent photoreceptor apoptosis inDrosophila.Neuron 1999; 28:139–152.
Kahn ES, Matsumoto H. Calcium/calmodulin-dependent kinase II phosphorylatesDrosophilavisual arrestin. J. Neurochem. 1997; 68:169–175.
Alloway PG, Dolph PJ. A role for the light-dependent phosphorylation of visual arrestin. Proc Natl Acad Sci USA 1999; 96:6072–6077.
Harris WA, Stark WS. Hereditary retinal degeneration ofDrosophila melanogaster:A mutant defect associated with the phototransduction process. J Gen Physiol 1977; 69:261–291.
Stark WS, Sapp R. Retinal degeneration and photoreceptor maintenance inDrosophila: rdgBand its interaction with other mutants. Inherited and environmentally induced retinal degenerations: Allan R. Liss, 1989:467–489.
Steel F, O’Tousa JE. Rhodopsin activation causes retinal degeneration inDrosophila rdgCmutant. Neuron 1990; 4:883–890.
Smith DP, Ranganathan R, Hardy RW et al. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 1991; 254:1478–1484.
Leonard DS, Bowman VD, Ready DF et al. Degeneration of photoreceptors in rhodopsin mutants ofDrosophila.J Neurobiol 1992; 23:605–626.
Dolph Pi, Ranganathan R, Colley NJ et al. Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 1993; 260:1910–1916.
Pak WL. Retinal degeneration mutants ofDrosophila.In: Wright A, Jay B, eds. Modern Genetics: Molecular Genetics of Inherited Eye Disorders. Chur: Harwood Academic Publishers, 1994:29–52.
Vihtelic TS, Goebl M, Milligan S et al. Localization ofDrosophilaretinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J Cell Biol 1993; 122:1013–1022.
Hotta Y, Benzer S. Genetic dissection of theDrosophilanervous system by means of mosaics. Proc Natl Acad Sci USA 1970; 67:1156–1163.
Pak WL. Mutations affecting the vision ofDrosophila melanogaster.In: King RC, ed. Handbook of Genetics, Vol. 3. New York: Plenum, 1975:703–733.
Johnson MA, Frayer KL, Stark WS. Characteristics ofrdgA:Mutants with retinal degeneration inDrosophila.J Insect Physiol 1982; 28:233–242.
Matsumoto E, Hirosawa K, Takagawa K et al. Structure of retinular cells ina Drosophila melanogastervisual mutant, rdga, at early stages of degeneration. Cell Tissue Res. 1988; 252:293–300.
Yoshioka T, Inoue H, Hotta Y. Defective phospholipid metabolism in the retinular cell membrane ofnorpA (no receptor potential)visual transduction mutants ofDrosophila.Biochem Biophys Res Com 1983; 111:567–573.
Yoshioka T, Inoue H, Hotta Y. Absence of diglyceride kinase activity in the photoreceptor cells ofDrosophilamutant. Biochem Biophys Res Corn 1984; 119:389–395.
Inoue H, Yoshioka T, Hotta Y. Diacylglycerol kinase defect ina Drosophilaretinal degeneration mutant rdga. J Biol Chem 1989; 264:5996–6000.
Masai I, Okazaki A, Hosoya T et al.Drosophilaretinal degeneration A gene encodes an eye-specific diacylglycerol kinase with cysteine-rich zinc-finger motifs and ankyrin repeats. Proc Natl Acad Sci USA 1993; 90:11157–11161.
Hochstrate P. Lanthanum mimics thetrpphotoreceptor mutant ofDrosophilain the blowfly Calliphora. J Comp Physiol A 1989; 166:179–188.
Suss-Toby E, Selinger Z, Minke B. Lanthanum reduces the excitation efficiency in fly photoreceptors. J Gen Physiol 1991; 98:849–868.
Cosens DJ, Manning A. Abnormal retinogram froma Drosophilamutant. Nature 1969; 224:285–287.
Cosens D. Blindness ina Drosophilamutant. J Insect Physiol 1971; 17:285–302.
Pak WL. Study of photoreceptor function usingDrosophilamutant. In: Breakfield X, ed. Neurogenetics: Genetic Approaches to the Nervous System. New York: Elsevier-North Holland, 1979:67–99.
Minke B, Wu C-F, Pak WL. Induction of photoreceptor voltage noise in the dark inDrosophilamutant. Nature 1975; 258:84–87.
Cosens DJ, Perry MM. The fine structure of the eye of a visual mutant, A-type, ofDrosophila melanogaster.J Insect Physiol 1972; 18:1773–1786.
Li C, Geng C, Leung H-T et al. INAF, a protein required for transient receptor potential Ca2+ channel function. Proc Nati Acad Sci USA 1999; 96:13474–13479.
Pak WL. Molecular genetic studies of photoreceptor function usingDrosophilamutant. In: Chader GJ, Farber D, eds. Molecular Biology of the Retina: Basic and Clinically Relevant Studies. New York: Wiley-Liss, 1991:1–32.
Peretz A, Suss-Toby E, Rom-Glas A et al. The light response ofDrosophilaphotoreceptors is accompanied by an increase in cellular calcium: effects of specific mutations. Neuron 1994; 12:1257–1267.
Franceschini N. Pupil and pseudopupi1 in the compound eye ofDrosophila.In: Wehner R, ed. Information Processing in the Visual System of Arthropods. New York: Springer-Verlag, 1972:75–82.
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Geng, C., Pak, W.L. (2002). Photoreceptor Degeneration and Ca2+ Influx Through Light-Activated Channels of Drosophila . In: Baehr, W., Palczewski, K. (eds) Photoreceptors and Calcium. Advances in Experimental Medicine and Biology, vol 514. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0121-3_33
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DOI: https://doi.org/10.1007/978-1-4615-0121-3_33
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