Abstract
Drosophilavision research has benefited from simultaneous application of genetic, molecular, electrophysiological analyses. The work establishes an essential role of Ca2+in regulation of phototransduction. Many different proteins are the targets of Ca2+regulation and these proteins act at multiple steps of the process. These targets include proteins involved in the rhodopsin cycle, proteins responsible for intermediate steps of phototransduction, and the TRP and TRPL light-gated channels. The regulation of these phototransduction components by Ca2+occurs in three different ways. First, the presence of Ca2+/calmodulin-binding sites in phototransduction-mediating proteins places these proteins under Ca2+control. Second, a protein kinase C regulated by Ca2+phosphorylates proteins to modulate their activity. Finally, some proteins contain Ca2+-binding sites and apparently are directly regulated by Ca2+. Here I review the photoreceptor proteins regulated by Ca2+and summarize current views on the roles of these proteins in theDrosophilaphotoresponse.
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References
Montell C. Visual transduction inDrosophila.Annu Rev Cell Dev Biol 1999; 15:231–68.
Minke B, Hardie RC. Genetic dissection ofDrosophilaphototransduction. In: Stavenga DG, DeGrip WJ, Pugh ENJ, eds. Handbook of Biological Physics. Amsterdam: Elsevier, 2000:449–525.
Hardie RC. Phototransduction inDrosophila melanogaster.J Exp Biol 2001; 204:3403–9.
Hardie RC, Raghu P. Visual transduction inDrosophila.Nature 2001; 413:186–93.
Bentrop J, Paulsen R. Light-modulated ADP-ribosylation, protein phosphorylation and protein binding in isolated fly photoreceptor membranes. Eur J Biochem 1986; 161:61–7.
Cassill JA, Whitney M, Joazeiro CA et al. Isolation ofDrosophilagenes encoding G protein-coupled receptor kinases. Proc Natl Acad Sci USA 1991; 88:11067–70.
Fortini ME, Skupski MP, Boguski MS, Hariharan IK. A survey of human disease gene counterparts in theDrosophilagenome. J Cell Biol 2000; 150:F23–30.
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; 90:1907–11.
Dolph PJ, Ranganathan R, Colley NJ et al. Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 1993; 260:1910–6.
Kahn ES, Matsumoto H. Calcium/calmodulin-dependent kinase II phosphorylatesDrosophilavisual arrestin. J Neurochem 1997; 68:169–75.
Matsumoto H, Kurien BT, Takagi Y et al. Phosrestin I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase inDrosophilaphotoreceptors. Neuron 1994; 12:997–1010.
Alloway PG, Dolph PJ. A role for the light-dependent phosphorylation of visual arrestin. Proc Natl Acad Sci USA 1999; 96:6072–7.
Alloway PG, Howard L, Dolph Pi. The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 2000; 28:129–38.
Kiselev A, Socolich M, Vinos J et al. A molecular pathway for light-dependent photorecptor apoptosis inDrosophila.Neuron 2000; 28:139–52.
Steele F, O’Tousa JE. Rhodopsin activation causes retinal degeneration inDrosophila rdgCmutant. Neuron 1990; 4:883–90.
Andreeva AV, Evans DE, Hawes CR et al. PP7, a plant phosphatase representing a novel evolutionary branch of eukaryotic protein Ser/Thr phosphatases. Biochem Mol Biol Int 1998; 44:703–15.
Cohen PT. Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem Sci 1997; 22:245–51.
Vinos J, Jalink K, Hardy RW et al. A G protein-coupled receptor phosphatase required for rhodopsin function. Science 1997; 277:687–90.
Huang X, Honkanen RE. Molecular cloning, expression, and characterization of a novel human serine/threonine protein phosphatase, PP7, that is homologous toDrosophilaretinal degeneration C gene product(rdgC).J Biol Chem 1998; 273:1462–8.
Ramulu P, Kennedy M, Xiong WH et al et al. Normal light response, photoreceptor integrity, and rhodopsin dephosphorylation in mice lacking both protein phosphatases with EFhands (PPEF-1 and PPEF-2). Mol Cell Biol 2001; 21:8605–14.
Kutuzov MA, Bennett N. Calcium-activated opsin phosphatase activity in retinal rod outer segments. Eur J Biochem 1996; 238:613–22.
Ramulu P, Nathans J. Cellular and subcellular localization, N-terminal acylation, and calcium binding ofCaenorhabditis elegansprotein phosphatase with EF- hands. J Biol Chem 2001; 276:25127–35.
Scott K, Zuker C. TRP, TRPL and trouble in photoreceptor cells. Curr Opin Neurobiol 1998; 8:383–8.
Ranganathan R, Bacskai BJ, Tsien RY, Zuker CS. Cytosolic calcium transients: spatial localization and role inDrosophilaphotoreceptor cell function. Neuron 1994; 13:837–48.
Hardie RC. INDO-I measurements of absolute resting and light-induced Ca2+concentration inDrosophilaphotoreceptors. J Neurosci 1996; 16:2924–33.
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; 12:1257–67.
Shieh BH, Zhu MY. Regulation of the TRP Ca2+channel by INAD inDrosophilaphotoreceptors. Neuron 1996; 16:991–8.
Huber A, Sander P, Gobert A et al. The transient receptor potential protein (Trp), a putative store-operated Ca2+channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. Embo J 1996; 15:7036–45.
Tsunoda S, Sierralta J, Sun Y et al. A multivalent PDZ-domain protein assembles signalling complexes in a G- protein-coupled cascade. Nature 1997; 388:243–9.
Tsunoda S, Zuker CS. The organization of INAD-signaling complexes by a multivalent PDZ domain protein inDrosophilaphotoreceptor cells ensures sensitivity and speed of signaling. Cell Calcium 1999; 26:165–71.
Huber A, Sander P, Paulsen R. Phosphorylation of the InaD gene product, a photoreceptor membrane protein required for recovery of visual excitation. J Biol Chem 1996; 271:11710–7.
Xu XZ, Choudhury A, Li X, Montell C. Coordination of an array of signaling proteins through homo-and heteromeric interactions between PDZ domains and target proteins. J Cell Biol 1998; 142:545–55.
Running Deer JL, Hurley JB, Yarfitz SL. G protein control ofDrosophilaphotoreceptor phospholipase C. J Biol Chem 1995; 270:12623–8.
Oberwinkler J, Stavenga DG. Calcium transients in the rhabdomeres of dark-and light-adapted fly photoreceptor cells. J Neurosci 2000; 20:1701–9.
Richard EA, Ghosh S, Lowenstein JM, Lisman JE. Ca2+/calmodulin-binding peptides block phototransduction inLimulusventral photoreceptors: evidence for direct inhibition of phospholipase C. Proc Natl Acad Sci USA 1997; 94:14095–9.
Dabdoub A, Payne R. Protein kinase C activators inhibit the visual cascade inLimulusventral photoreceptors at an early stage. J Neurosci 1999; 19:10262–9.
Tanaka C, Nishizuka Y. The protein kinase C family for neuronal signaling. Annu Rev Neurosci 1994; 17:551–67.
Schaeffer E, Smith D, Mardon G, Quinn W, Zuker C. Isolation and characterization of two newDrosophilaprotein kinase C genes, including one specifically expressed in photoreceptor cells. Cell 1989; 57:403–12.
Hardie RC, Peretz A, Pollock JA, Minke B. Ca2+limits the development of the light response inDrosophilaphotoreceptors. Proc R Soc Lond B Biol Sci 1993; 252:223–9.
Smith DP, Ranganathan R, Hardy RW, Marx J, Tsuchida T, Zuker CS. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptor-specific protein kinase C. Science 1991; 254:1478–84.
Huber A, Sander P, Bahner M, Paulsen R. The TRP Ca2+channel assembled in a signaling complex by the PDZ domain protein INAD is phosphorylated through the interaction with protein kinase C (ePKC). FEBS Lett 1998; 425:317–22.
Li HS, Porter JA, Montell C. Requirement for the NINAC kinase/myosin for stable termination of the visual cascade. J Neurosci 1998; 18:9601–6.
Milligan SC, Alb JG, Jr., EIagina RB, Bankaitis VA, Hyde DR. The phosphatidylinositol transfer protein domain ofDrosophilaretinal degeneration B protein is essential for photoreceptor cell survival and recovery from light stimulation. J Cell Biol 1997; 139:351–63.
Vihtelic TS, Goebl M, Milligan S, O’Tousa JE, Hyde DR. Localization ofDrosophilaretinal degeneration B, a membrane-associated phosphatidylinositol transfer protein. J Cell Biol 1993; 122:1013–22.
Hardie RC, Raghu P, Moore S et al. Calcium influx via TRP channels is required to maintain PIP2 levels inDrosophilaphotoreceptors. Neuron 2001; 30:149–59.
Montell C, Rubin GM. TheDrosophila ninaClocus encodes two photoreceptor cell specific proteins with domains homologous to protein kinases and the myosin heavy domain head. Cell 1988; 52:757–772.
Porter JA, Montell C. Distinct roles of theDrosophila NinaCkinase and myosin domains revealed by systematic mutagenesis. J. Cell Biol. 1993; 122:601–612.
Porter JA, Minke B, Montell C. Calmodulin binding toDrosophila NinaCrequired for termination of phototransduction. Embo J 1995; 14:4450–9.
Anion A, Cook B, Gillo B et al. Calmodulin regulation of light adaptation and store-operated dark current inDrosophilaphotoreceptors. Proc Natl Acad Sci USA 1997; 94:5894–9.
Martin JH, Benzer S, Rudnicka M, Miller CA. Calphotin: ADrosophilaphotoreceptor cell calcium-binding protein. Proc Natl Acad Sci USA 1993; 90:1531–5.
Ballinger DG, Xue N, Harshman KD. ADrosophilaphotoreceptor cell-specific protein, calphotin, binds calcium and contains a leucine zipper. Proc Natl Acad Sci USA 1993; 90:1536–40.
Yang Y, Ballinger D. Mutations in calphotin, the gene encodinga Drosophilaphotoreceptor cell-specific calcium-binding protein, reveal roles in cellular morphogenesis and survival. Genetics 1994; 138:413–21.
Hardie RC. Photolysis of caged Ca2+facilitates and inactivates but does not directly excite light-sensitive channels inDrosophilaphotoreceptors. J Neurosci 1995; 15:889–902.
Schwarz EM, Benzer S. Caix, a Na-Ca exchanger gene ofDrosophila melanogaster.Proc Natl Acad Sci USA 1997; 94:10249–54.
Haug-Collet K, Pearson B, Webel R et al. Cloning and characterization of a potassium-dependent sodium/calcium exchanger inDrosophila.J Cell Biol 1999; 147:659–70.
Xu XZ, Wes PD, ChenHet al. Retinal targets for calmodulin include proteins implicated in synaptic transmission. J Biol Chem 1998; 273:31297–307.
Hasan G, Rosbash M.Drosophilahomologs of two mammalian intracellular Ca(2+)-release channels: identification and expression patterns of the inositol 1,4,5- triphosphate and the ryanodine receptor genes. Development 1992; 116:967–75.
Xu XZ, Chien F, Butler A et al. TRPgamma, aDrosophilaTRP-related subunit, forms a regulated cation channel with TRPL. Neuron 2000; 26:647–57.
Hardie RC, Reuss H, Lansdell SJ, Millar NS. Functional equivalence of native light-sensitive channels in theDrosophila trp301mutant and TRPL cation channels expressed in a stably transfected Drosophila cell line. Cell Calcium 1997; 21:431–40.
Niemeyer BA, Suzuki E, Scott K et al. TheDrosophilalight-activated conductance is composed of the two channels TRP and TRPL. Cell 1996; 85:651–9.
Hardie RC, Raghu P. Activation of heterologously expressedDrosophilaTRPL channels: Ca2+ is not required and InsP3 is not sufficient. Cell Calcium 1998; 24:153–63.
Zimmer S, Trost C, Wissenbach U et al. Modulation of recombinant transient-receptor-potential-like (TRPL) channels by cytosolic Ca2+. Pflugers Arch 2000; 440:409–17.
Henderson SR, Reuss H, Hardie RC. Single photon responses inDrosophilaphotoreceptors and their regulation by Ca2+. J Physiol 2000; 524 Pt 1:179–94.
Phillips AM, Bull A, Kelly LE. Identification ofa Drosophilagene encoding a calmodulinbinding protein with homology to the trp phototransduction gene. Neuron 1992; 8:631–42.
Scott K, Sun Y, Beckingham K, Zuker CS. Calmodulin regulation ofDrosophilalight-activated channels and receptor function mediates termination of the light response in vivo. Cell 1997; 91:375–83.
Chevesich J, Kreuz AJ, Montell C. Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex. Neuron 1997; 18:95–105.
Hardie RC, Peretz A, Suss-Toby E et al. Protein kinase C is required for light adaptation inDrosophilaphotoreceptors. Nature 1993; 363:634–7.
Warr CG, Kelly LE. Identification and characterization of two distinct calmodulin-binding sites in the Trpl ion-channel protein ofDrosophila melanogaster.Biochem J 1996; 314:497–503.
Salcedo E, Huber A, Henrich S et al. Blue-and green-absorbing visual pigments ofDrosophila:Ectopic expression and physiological characterization of the R8 photoreceptor cell-specific Rh5 and Rh6 rhodopsins. J Neurosci 1999; 19:10716–26.
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O’Tousa, J. (2002). Ca2+Regulation ofDrosophilaPhototransduction. 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_30
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DOI: https://doi.org/10.1007/978-1-4615-0121-3_30
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