Retinophilin is a light-regulated phosphoprotein required to suppress photoreceptor dark noise in Drosophila

Journal of Neuroscience

Volumn 30, Issue 4, 2010, Pages 1238-1249

  Mecklenburg, Kirk L ^a   Takemori, Nobuaki ^b,e   Komori, Naoka ^b   Chu, Brian ^c   Hardie, Roger C ^c   Matsumoto, Hiroyuki ^b   O'Tousa, Joseph E ^d  

^a INDIANA UNIVERSITY SOUTH BEND   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF NOTRE DAME   (United States)

^e EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN III; PHOSPHOPROTEIN; RETINOPHILIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DARKNESS; DELETION MUTANT; DEPHOSPHORYLATION; DROSOPHILA; ELECTROPHYSIOLOGY; GENETICS; LIGHT EXPOSURE; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEOMICS;

ADAPTATION, OCULAR; AMINO ACID MOTIFS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; DARK ADAPTATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; EYE PROTEINS; LIGHT; MEMBRANE POTENTIALS; MICROVILLI; MUTATION; PHOSPHOPROTEINS; PHOTIC STIMULATION; PHOTORECEPTOR CELLS; PHOTORECEPTOR CELLS, INVERTEBRATE; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; VISION, OCULAR;

EID: 75349112834     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4464-09.2010     Document Type: Article

References (55)

1. Ahmad ST, Natochin M, Artemyev NO, O'Tousa JE (2007) The Drosophila rhodopsin cytoplasmic tail domain is required for maintenance of rhabdomere structure. FASEB J 21:449-455.
2. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270-2275.
3. Byk T, Bar-Yaacov M, Doza YN, Minke B, Selinger Z (1993) Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proc Natl Acad Sci U S A 90:1907-1911.
4. Cagan RL, Ready DF (1989) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346-362.
5. Chorna-Ornan I, Tzarfaty V, Ankri-Eliahoo G, Joel-Almagor T, Meyer NE, Huber A, Payre F, Minke B (2005) Light-regulated interaction of Dmoesin with TRP and TRPL channels is required for maintenance of photoreceptors. J Cell Biol 171:143-152.
6. Cronin MA, Diao F, Tsunoda S (2004) Light-dependent subcellular translocation of Gqalpha in Drosophila photoreceptors is facilitated by the photoreceptor-specific myosin III NINAC. J Cell Sci 117:4797-4806.
7. Cuttell L, Vaughan A, Silva E, Escaron CJ, Lavine M, Van Goethem E, Eid JP, Quirin M, Franc NC (2008) Undertaker, a Drosophila Junctophilin, links Draper-mediated phagocytosis and calcium homeostasis. Cell 135:524-534.
8. Elia N, Frechter S, Gedi Y, Minke B, Selinger Z (2005) Excess of Gβe over Gqαe in vivo prevents dark, spontaneous activity of Drosophila photoreceptors. J Cell Biol 171:517-526.
9. Frechter S, Elia N, Tzarfaty V, Selinger Z, Minke B (2007) Translocation of Gqα mediates long-term adaptation in Drosophila photoreceptors. J Neurosci 27:5571-5583.
10. Freeman M (1996) Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87:651-660.
11. Gubbels MJ, Vaishnava S, Boot N, Dubremetz JF, Striepen B (2006) A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J Cell Sci 119:2236-2245.
12. Hardie RC, Postma M (2008) Phototransduction in microvillar photoreceptors of Drosophila and other invertebrates. In: The senses - a comprehensive reference. Vision, Vol 1 (Masland R, Albright T, eds), pp 77-130. San Diego: Academic.
13. Hardie RC, Martin F, Cochrane GW, Juusola M, Georgiev P, Raghu P (2002) Molecular basis of amplification in Drosophila phototransduction: roles for G protein, phospholipase C, and diacylglycerol kinase. Neuron 36:689-701.
14. 2+. J Physiol 524:179-194.
15. Hofstee CA, Henderson S, Hardie RC, Stavenga DG (1996) Differential effects of ninaC proteins (p132 and p174) on light-activated currents and pupil mechanism in Drosophila photoreceptors. Vis Neurosci 13:897-906.
16. Hyde DR, Mecklenburg KL, Pollock JA, Vihtelic TS, Benzer S (1990) Twenty Drosophila visual system cDNA clones: one is a homolog of human arrestin. Proc Natl Acad Sci U S A 87:1008-1012.
17. Im YJ, Davis AJ, Perera IY, Johannes E, Allen NS, Boss WF (2007) The N-terminal membrane occupation and recognition nexus domain of Arabidopsis phosphatidylinositol phosphate kinase 1 regulates enzyme activity. J Biol Chem 282:5443-5452.
18. Katz B, Minke B (2009) Drosophila photoreceptors and signaling mechanisms. Front Cell Neurosci 3:2.
19. Kosloff M, Elia N, Joel-Almagor T, Timberg R, Zars TD, Hyde DR, Minke B, Selinger Z (2003) Regulation of light-dependent Gqα translocation and morphological changes in fly photoreceptors. EMBO J 22:459-468.
20. Krispel CM, Sokolov M, Chen YM, Song H, Herrmann R, Arshavsky VY, Burns ME (2007) Phosducin regulates the expression of transducin βγ subunits in rod photoreceptors and does not contribute to phototransduction adaptation. J Gen Physiol 130:303-312.
21. Larrivee DC, Conrad SK, Stephenson RS, Pak WL (1981) Mutation that selectively affects rhodopsin concentration in the peripheral photoreceptors of Drosophila melanogaster. J Gen Physiol 78:521-545.
22. Lee BY, Thulin CD, Willardson BM (2004) Site-specific phosphorylation of phosducin in intact retina. Dynamics of phosphorylation and effects on G protein βγ dimer binding. J Biol Chem 279:54008-54017.
23. 2+-dependent metarhodopsin inactivation mediated by calmodulin and NINAC myosin III. Neuron 59:778-789.
24. Ma H, Lou Y, Lin WH, Xue HW (2006) MORN motifs in plant PIPKs are involved in the regulation of subcellular localization and phospholipid binding. Cell Res 16:466-478.
25. Mann M, Ong SE, Grønborg M, Steen H, Jensen ON, PandeyA (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20:261-268.
26. Matsumoto H, Komori N (1999) Protein identification on two-dimensional gels archived nearly two decades ago by in-gel digestion and matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Anal Biochem 270:176-179.
27. Matsumoto H, Pak WL (1984) Light-induced phosphorylation of retina-specific polypeptides of Drosophila in vivo. Science 223:184-186.
28. Matsumoto H, O'Tousa JE, Pak WL (1982) Light-induced modification of Drosophila retinal polypeptides in vivo. Science 217:839-841.
29. Matsumoto H, Isono K, Pye Q, Pak WL (1987) Gene encoding cytoskeletal proteins in Drosophila rhabdomeres. Proc Natl Acad Sci U S A 84:985-989.
30. Matsumoto H, Kurien BT, Takagi Y, Kahn ES, Kinumi T, Komori N, Yamada T, Hayashi F, Isono K, Pak WL, Jackson KW, Tobin SL (1994) Phosrestin I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase in Drosophila photoreceptors. Neuron 12:997-1010.
31. Matsumoto H, Kahn ES, Komori N (1999) The emerging role of mass spectrometry in molecular biosciences: studies of protein phosphorylation in fly eyes as an example. Novartis Found Symp 224:225-244; discussion 244-228.
32. Mecklenburg KL (2007) Drosophila retinophilin contains MORN repeats and is conserved in humans. Mol Genet Genomics 277:481-489.
33. Minke B, Stephenson RS (1985) The characteristics of chemically induced noise in Musca photoreceptors. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 156:339-356.
34. Montell C (1998) TRP trapped in fly signaling web. Curr Opin Neurobiol 8:389-397.
35. Pak WL (1995) Drosophila in vision research. The Friedenwald Lecture. Invest Ophthalmol Vis Sci 36:2340-2357.
36. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, Huppert K, Tan LR, Winter CG, Bogart KP, Deal JE, Deal-Herr ME, Grant D, Marcinko M, Miyazaki WY, Robertson S, Shaw KJ, Tabios M, Vysotskaia V, Zhao L, Andrade RS, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nat Genet 36:288-292.
37. α-terminal acetylation of eukaryotic proteins. J Biol Chem 275:36479-36482.
38. Porter JA, Montell C (1993) Distinct roles of the Drosophila ninaC kinase and myosin domains revealed by systematic mutagenesis. J Cell Biol 122:601-612.
39. Porter JA, Hicks JL, Williams DS, Montell C (1992) Differential localizations of and requirements for the two Drosophila ninaC kinase/myosins in photoreceptor cells. J Cell Biol 116:683-693.
40. Qin J, Chait BT (1997) Identification and characterization of posttranslational modifications of proteins by MALDI ion trap mass spectrometry. Anal Chem 69:4002-4009.
41. Shieh BH, Niemeyer B (1995) A novel protein encoded by the InaD gene regulates recovery of visual transduction in Drosophila. Neuron 14:201-210.
42. Song H, Belcastro M, Young EJ, Sokolov M (2007) Compartment-specific phosphorylation of phosducin in rods underlies adaptation to various levels of illumination. J Biol Chem 282:23613-23621.
43. Steele FR, Washburn T, Rieger R, O'Tousa JE (1992) Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell 69:669-676.
44. Tabuchi K, Sawamoto K, Suzuki E, Ozaki K, Sone M, Hama C, Tanifuji-Morimoto T, Yuasa Y, Yoshihara Y, Nose A, Okano H (2000) GAL4/UAS-WGA system as a powerful tool for tracing Drosophila transsynaptic neural pathways. J Neurosci Res 59:94-99.
45. Takemori N, Komori N, Thompson JN Jr, Yamamoto MT, Matsumoto H (2007) Novel eye-specific calmodulin methylation characterized by protein mapping in Drosophila melanogaster. Proteomics 7:2651-2658.
46. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6:11-22.
47. Thummel CS, Boulet AM, Lipshitz HD (1988) Vectors for Drosophila P-element-mediated transformation and tissue culture transfection. Gene 74:445-456.
48. Trojan P, Rausch S, Giessl A, Klemm C, Krause E, Pulvermüller A, Wolfrum U (2008) Light-dependent CK2-mediated phosphorylation of centrins regulates complex formation with visual G-protein. Biochim Biophys Acta 1783:1248-1260.
49. Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS (1997) A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 388:243-249.
50. Wang T, Montell C (2007) Phototransduction and retinal degeneration in Drosophila. Pflugers Arch 454:821-847.
51. Wilson JR, Jing C, Walker PA, Martin SR, Howell SA, Blackburn GM, Gamblin SJ, Xiao B (2002) Crystal structure and functional analysis of the histone methyltransferase SET7/9. Cell 111:105-115.
52. Xu H, Lee SJ, Suzuki E, Dugan KD, Stoddard A, Li HS, Chodosh LA, Montell C (2004) A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J 23:811-822.
53. Yamada T, Takeuchi Y, Komori N, Kobayashi H, Sakai Y, Hotta Y, Matsumoto H (1990) A 49-kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin homolog. Science 248:483-486.
54. Yang Z, Edenberg HJ, Davis RL (2005) Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nucleic Acids Res 33:e148.
55. Zuker CS (1996) The biology of vision of Drosophila. Proc Natl Acad Sci U S A 93:571-576.