Molecular genetics of retinal degeneration a drosophila perspective

Fly

Volumn 5, Issue 4, 2011, Pages 356-368

  Shieh, Bih Hwa ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Arrestin; Autophagy; Autosomal dominant retinitis pigmentosa; Drosophila; Phospholipase c ; Rhabdomeres; Rhodopsin; Unfolded protein response; Vision

Indexed keywords

EID: 82855176847     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.5.4.17809     Document Type: Article

References (149)

1. Franceschini N. Pupil and psueopupil in the compound eye of Drosophila. In: Wehner R, Ed. Information Processing in the Visual Systems of Arthropods. Berlin: Springer-Verlag 1972; 75-82.
2. Knust E. Photoreceptor morphogenesis and retinal degeneration: lessons from Drosophila. Curr Opin Neurobiol 2007; 17:541-547.
3. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993; 118:401-415.
4. Elliott DA, Brand AH. The GAL4 system: a versatile system for the expression of genes. Methods Mol Biol 2008; 420:79-95.
5. Carthew RW. Gene silencing by double-stranded RNA. Curr Opin Cell Biol 2001; 13:244-248.
6. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 2011; 8:405-407.
7. Zelhof AC, Hardy RW. WASp is required for the correct temporal morphogenesis of rhabdomere microvilli. J Cell Biol 2004; 164:417-426.
8. Britt SG, Feiler R, Kirschfeld K, Zuker CS. Spectral tuning of rhodopsin and metarhodopsin in vivo. Neuron 1993; 11:29-39.
9. Lin SW, Sakmar TP. Colour tuning mechanisms of visual pigments. Novartis Found Symp 1999; 224:124-135.
10. O'Tousa JE, Baehr W, Martin RL, Hirsh J, Pak WL, Applebury ML. The Drosophila ninaE gene encodes an opsin. Cell 1985; 40:839-850.
11. Zuker CS, Cowman AF, Rubin GM. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 1985; 40:851-858.
12. Montell C, Jones K, Zuker C, Rubin G. A second opsin gene expressed in the ultraviolet-sensitive R7 photoreceptor cells of Drosophila melanogaster. J Neurosci 1987; 7:1558-1566.
13. Zuker CS, Montell C, Jones K, Laverty T, Rubin GM. A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: homologies with other signaltransducing molecules. J Neurosci 1987; 7:1550-1557.
14. Papatsenko D, Sheng G, Desplan C. A new rhodopsin in R8 photoreceptors of Drosophila: evidence for coordinate expression with Rh3 in R7 cells. Development 1997; 124:1665-1673.
15. Huber A, Schulz S, Bentrop J, Groell C, Wolfrum U, Paulsen R. Molecular cloning of Drosophila Rh6 rhodopsin: the visual pigment of a subset of R8 photoreceptor cells. FEBS Lett 1997; 406:6-10.
16. Cowman AF, Zuker CS, Rubin GM. An opsin gene expressed in only one photoreceptor cell type of the Drosophila eye. Cell 1986; 44:705-710.
17. Foord SM, Bonner TI, Neubig RR, Rosser EM, Pin JP, Davenport AP, et al. International Union of Pharmacology. XLVI. G protein-coupled receptor list. Pharmacol Rev 2005; 57:279-288.
18. Hong Y, Ackerman L, Jan LY, Jan YN. Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc Natl Acad Sci USA 2003; 100:12712-12717.
19. Salmena L, Carracedo A, Pandolfi PP. Tenets of PTEN tumor suppression. Cell 2008; 133:403-414.
20. Janmey PA. Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu Rev Physiol 1994; 56:169-191.
21. Stocker H, Andjelkovic M, Oldham S, Laffargue M, Wymann MP, Hemmings BA, Hafen E. Living with lethal PIP3 levels: viability of flies lacking PTEN restored by a PH domain mutation in Akt/PKB. Science 2002; 295:2088-2091.
22. Pinal N, Goberdhan DC, Collinson L, Fujita Y, Cox IM, Wilson C, Pichaud F. Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr Biol 2006; 16:140-149.
23. Berger S, Bulgakova NA, Grawe F, Johnson K, Knust E. Unraveling the genetic complexity of Drosophila stardust during photoreceptor morphogenesis and prevention of light-induced degeneration. Genetics 2007; 176:2189-2200.
24. Pellikka M, Tanentzapf G, Pinto M, Smith C, McGlade CJ, Ready DF, Tepass U. Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 2002; 416:143-149.
25. Richard M, Muschalik N, Grawe F, Ozuyaman S, Knust E. A role for the extracellular domain of Crumbs in morphogenesis of Drosophila photoreceptor cells. Eur J Cell Biol 2009; 88:765-777.
26. Zuker CS. The biology of vision of Drosophila. Proc Natl Acad Sci USA 1996; 93:571-576.
27. Scott K, Becker A, Sun Y, Hardy R, Zuker C. Gqalpha protein function in vivo: genetic dissection of its role in photoreceptor cell physiology. Neuron 1995; 15:919-927.
28. Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, et al. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 1988; 54:723-733.
29. Raghu P, Usher K, Jonas S, Chyb S, Polyanovsky A, Hardie RC. Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant, rdgA. Neuron 2000; 26:169-179.
30. Leung HT, Tseng-Crank J, Kim E, Mahapatra C, Shino S, Zhou Y, et al. DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron 2008; 58:884-896.
31. Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, et al. Normal phototransduction in Drosophila photoreceptors lacking an InsP(3) receptor gene. Mol Cell Neurosci 2000; 15:429-445.
32. Pak WL, Leung HT. Genetic approaches to visual transduction in Drosophila melanogaster. Receptors Channels 2003; 9:149-167.
33. Wang T, Montell C. Phototransduction and retinal degeneration in Drosophila. Pflugers Arch 2007; 454:821-847.
34. 2+ channel by INAD in Drosophila photoreceptors. Neuron 1996; 16:991-998.
35. Adamski FM, Zhu MY, Bahiraei F, Shieh BH. Interaction of eye protein kinase C and INAD in Drosophila. Localization of binding domains and electrophysiological characterization of a loss of association in transgenic flies. J Biol Chem 1998; 273:17713-17719.
36. Shieh BH, Zhu MY, Lee JK, Kelly IM, Bahiraei F. Association of INAD with NORPA is essential for controlled activation and deactivation of Drosophila phototransduction in vivo. Proc Natl Acad Sci USA 1997; 94:12682-12687.
37. Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, et al. A multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade. Nature 1997; 388:243-249.
38. van Huizen R, Miller K, Chen DM, Li Y, Lai ZC, Raab RW, et al. Two distantly positioned PDZ domains mediate multivalent INAD-phospholipase C interactions essential for G protein-coupled signaling. EMBO J 1998; 17:2285-2297.
39. 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; 142:545-555.
40. Fain GL, Hardie R, Laughlin SB. Phototransduction and the evolution of photoreceptors. Curr Biol 2010; 20:114-124.
41. Vinos J, Jalink K, Hardy RW, Britt SG, Zuker CS. A G protein-coupled receptor phosphatase required for rhodopsin function. Science 1997; 277:687-690.
42. Steele FR, Washburn T, Rieger R, O'Tousa JE. Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase. Cell 1992; 69:669-676.
43. Kahn ES, Matsumoto H. Calcium/calmodulin-dependent kinase II phosphorylates Drosophila visual arrestin. J Neurochem 1997; 68:169-175.
44. Alloway PG, Dolph PJ. A role for the light-dependent phosphorylation of visual arrestin. Proc Natl Acad Sci USA 1999; 96:6072-6077.
45. Dolph PJ, Ranganathan R, Colley NJ, Hardy RW, Socolich M, Zuker CS. Arrestin function in inactivation of G protein-coupled receptor rhodopsin in vivo. Science 1993; 260:1910-1916.
46. Smith DP, Ranganathan R, Hardy RW, Marx J, Tsuchida T, Zuker CS. Photoreceptor deactivation and retinal degeneration mediated by a photoreceptorspecific protein kinase C. Science 1991; 254:1478-1484.
47. Popescu DC, Ham AJ, Shieh BH. Scaffolding protein INAD regulates deactivation of vision by promoting phosphorylation of transient receptor potential by eye protein kinase C in Drosophila. J Neurosci 2006; 26:8570-8577.
48. Hardie RC, Peretz A, Suss-Toby E, Rom-Glas A, Bishop SA, Selinger Z, Minke B. Protein kinase C is required for light adaptation in Drosophila photoreceptors. Nature 1993; 363:634-637.
49. Ranganathan R, Harris GL, Stevens CF, Zuker CS. A Drosophila mutant defective in extracellular calciumdependent photoreceptor deactivation and rapid desensitization. Nature 1991; 354:230-232.
50. Rosenbaum EE, Hardie RC, Colley NJ. Calnexin is essential for rhodopsin maturation, Ca2+ regulation and photoreceptor cell survival. Neuron 2006; 49:229-241.
51. Baker EK, Colley NJ, Zuker CS. The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J 1994; 13:4886-4895.
52. Shetty KM, Kurada P, O'Tousa JE. Rab6 regulation of rhodopsin transport in Drosophila. J Biol Chem 1998; 273:20425-20430.
53. Satoh AK, O'Tousa JE, Ozaki K, Ready DF. Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 2005; 132:1487-1497.
54. Matsumoto H, Isono K, Pye Q, Pak WL. Gene encoding cytoskeletal proteins in Drosophila rhabdomeres. Proc Natl Acad Sci USA 1987; 84:985-989.
55. Satoh AK, Ready DF. Arrestin1 mediates light-dependent rhodopsin endocytosis and cell survival. Curr Biol 2005; 15:1722-1733.
56. Kiselev A, Socolich M, Vinos J, Hardy RW, Zuker CS, Ranganathan R. A molecular pathway for lightdependent photoreceptor apoptosis in Drosophila. Neuron 2000; 28:139-152.
57. Xu H, Lee SJ, Suzuki E, Dugan KD, Stoddard A, Li HS, et al. A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J 2004; 23:811-822.
58. Chinchore Y, Mitra A, Dolph PJ. Accumulation of rhodopsin in late endosomes triggers photoreceptor cell degeneration. PLoS Genet 2009; 5:1000377.
59. Webel R, Menon I, O'Tousa JE, Colley NJ. Role of asparagine-linked oligosaccharides in rhodopsin maturation and association with its molecular chaperone, NinaA. J Biol Chem 2000; 275:24752-24759.
60. Katanosaka K, Tokunaga F, Kawamura S, Ozaki K. N-linked glycosylation of Drosophila rhodopsin occurs exclusively in the amino-terminal domain and functions in rhodopsin maturation. FEBS Lett 1998; 424:149-154.
61. O'Tousa JE. Requirement of N-linked glycosylation site in Drosophila rhodopsin. Vis Neurosci 1992; 8:385-390.
62. Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science 2001; 291:2364-2369.
63. Schneuwly S, Shortridge RD, Larrivee DC, Ono T, Ozaki M, Pak WL. Drosophila ninaA gene encodes an eye-specific cyclophilin (cyclosporine A binding protein). Proc Natl Acad Sci USA 1989; 86:5390-5394.
64. Shieh BH, Stamnes MA, Seavello S, Harris GL, Zuker CS. The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporine A-binding protein. Nature 1989; 338:67-70.
65. Colley NJ, Baker EK, Stamnes MA, Zuker CS. The cyclophilin homolog ninaA is required in the secretory pathway. Cell 1991; 67:255-263.
66. von Lintig J, Dreher A, Kiefer C, Wernet MF, Vogt K. Analysis of the blind Drosophila mutant ninaB identifies the gene encoding the key enzyme for vitamin A formation invivo. Proc Natl Acad Sci USA 2001; 98:1130-1135.
67. Kiefer C, Sumser E, Wernet MF, Von Lintig J. A class B scavenger receptor mediates the cellular uptake of carotenoids in Drosophila. Proc Natl Acad Sci USA 2002; 99:10581-10586.
68. Voolstra O, Kiefer C, Hoehne M, Welsch R, Vogt K, von Lintig J. The Drosophila class B scavenger receptor NinaD-I is a cell surface receptor mediating carotenoid transport for visual chromophore synthesis. Biochemistry 2006; 45:13429-13437.
69. Ahmad ST, Joyce MV, Boggess B, O'Tousa JE. The role of Drosophila ninaG oxidoreductase in visual pigment chromophore biogenesis. J Biol Chem 2006; 281:9205-9209.
70. Wang T, Jiao Y, Montell C. Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction. J Cell Biol 2007; 177:305-316.
71. Ozaki K, Nagatani H, Ozaki M, Tokunaga F. Maturation of major Drosophila rhodopsin, ninaE, requires chromophore 3-hydroxyretinal. Neuron 1993; 10:1113-1119.
72. Voolstra O, Oberhauser V, Sumser E, Meyer NE, Maguire ME, Huber A, von Lintig J. NinaB is essential for Drosophila vision but induces retinal degeneration in opsin-deficient photoreceptors. J Biol Chem 2010; 285:2130-2139.
73. Kock I, Bulgakova NA, Knust E, Sinning I, Panneels V. Targeting of Drosophila rhodopsin requires helix 8 but not the distal C-terminus. PLoS One 2009; 4:6101.
74. Ahmad ST, Natochin M, Artemyev NO, O'Tousa JE. The Drosophila rhodopsin cytoplasmic tail domain is required for maintenance of rhabdomere structure. Faseb J 2007; 21:449-455.
75. Leonard DS, Bowman VD, Ready DF, Pak WL. Degeneration of photoreceptors in rhodopsin mutants of Drosophila. J Neurobiol 1992; 23:605-626.
76. Kumar JP, Ready DF. Rhodopsin plays an essential structural role in Drosophila photoreceptor development. Development 1995; 121:4359-4370.
77. Iakhine R, Chorna-Ornan I, Zars T, Elia N, Cheng Y, Selinger Z, et al. Novel dominant rhodopsin mutation triggers two mechanisms of retinal degeneration and photoreceptor desensitization. J Neurosci 2004; 24:2516-2526.
78. Kurada P, Tonini TD, Serikaku MA, Piccini JP, O'Tousa JE. Rhodopsin maturation antagonized by dominant rhodopsin mutants. Vis Neurosci 1998; 15:693-700.
79. Sung CH, Davenport CM, Hennessey JC, Maumenee IH, Jacobson SG, Heckenlively JR, et al. Rhodopsin mutations in autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA 1991; 88:6481-6485.
80. Dryja TP, McEvoy JA, McGee TL, Berson EL. Novel rhodopsin mutations Gly114Val and Gln184Pro in dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci 2000; 41:3124-3127.
81. Mendes HF, van der Spuy J, Chapple JP, Cheetham ME. Mechanisms of cell death in rhodopsin retinitis pigmentosa: implications for therapy. Trends Mol Med 2005; 11:177-185.
82. Noorwez SM, Ostrov DA, McDowell JH, Krebs MP, Kaushal S. A high-throughput screening method for small-molecule pharmacologic chaperones of misfolded rhodopsin. Invest Ophthalmol Vis Sci 2008; 49:3224-3230.
83. Illing ME, Rajan RS, Bence NF, Kopito RR. A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J Biol Chem 2002; 277:34150-34160.
84. Colley NJ, Cassill JA, Baker EK, Zuker CS. Defective intracellular transport is the molecular basis of rhodopsin-dependent dominant retinal degeneration. Proc Natl Acad Sci USA 1995; 92:3070-3074.
85. Kurada P, O'Tousa JE. Retinal degeneration caused by dominant rhodopsin mutations in Drosophila. Neuron 1995; 14:571-579.
86. Galy A, Roux MJ, Sahel JA, Leveillard T, Giangrande A. Rhodopsin maturation defects induce photoreceptor death by apoptosis: a fly model for RhodopsinPro23His human retinitis pigmentosa. Hum Mol Genet 2005; 14:2547-2557.
87. Griciuc A, Aron L, Roux MJ, Klein R, Giangrande A, Ueffing M. Inactivation of VCP/ter94 suppresses retinal pathology caused by misfolded rhodopsin in Drosophila. PLoS Genet 2010; 6:1001075.
88. Dryja TP, McGee TL, Hahn LB, Cowley GS, Olsson JE, Reichel E, et al. Mutations within the rhodopsin gene in patients with autosomal dominant retinitis pigmentosa. N Engl J Med 1990; 323:1302-1327.
89. Robinson PR, Cohen GB, Zhukovsky EA, Oprian DD. Constitutively active mutants of rhodopsin. Neuron 1992; 9:719-725.
90. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519-529.
91. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005; 115:2656-2664.
92. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2:326-332.
93. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002; 3:99-111.
94. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001; 107:881-891.
95. Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003; 23:7448-7459.
96. Urano F, Bertolotti A, Ron D. IRE1 and efferent signaling from the endoplasmic reticulum. J Cell Sci 2000; 113:3697-3702.
97. Hamanaka RB, Bennett BS, Cullinan SB, Diehl JA. PERK and GCN2 contribute to eIF2alpha phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 2005; 16:5493-5501.
98. Ryoo HD, Domingos PM, Kang MJ, Steller H. Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J 2007; 26:242-252.
99. Mendes CS, Levet C, Chatelain G, Dourlen P, Fouillet A, Dichtel-Danjoy ML, et al. ER stress protects from retinal degeneration. EMBO J 2009; 28:1296-1307.
100. Lin JH, Walter P, Yen TS. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 2008; 3:399-425.
101. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 2002; 16:1345-1355.
102. Chang HY, Ready DF. Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 2000; 290:1978-1980.
103. Sparrow JR, Boulton M. RPE lipofuscin and its role in retinal pathobiology. Exp Eye Res 2005; 80:595-606.
104. 2+ exchanger CalX. Neuron 2005; 45:367-378.
105. Masai I, Suzuki E, Yoon CS, Kohyama A, Hotta Y. Immunolocalization of Drosophila eye-specific diacylgylcerol kinase, rdgA, which is essential for the maintenance of the photoreceptor. J Neurobiol 1997; 32:695-706.
106. Vihtelic TS, Hyde DR, O'Tousa JE. Isolation and characterization of the Drosophila retinal degeneration B (rdgB) gene. Genetics 1991; 127:761-768.
107. Stark WS, Sapp R. Retinal degeneration and photoreceptor maintenance in Drosophila: rdgB and its interaction with other mutants. Prog Clin Biol Res 1989; 314:467-489.
108. Dasgupta U, Bamba T, Chiantia S, Karim P, Tayoun AN, Yonamine I, et al. Ceramide kinase regulates phospholipase C and phosphatidylinositol-4,5-bisphosphate in phototransduction. Proc Natl Acad Sci USA 2009; 106:20063-20068.
109. Georgiev P, Garcia-Murillas I, Ulahannan D, Hardie RC, Raghu P. Functional INAD complexes are required to mediate degeneration in photoreceptors of the Drosophila rdgA mutant. J Cell Sci 2005; 118:1373-1384.
110. Johnson MA, Frayer KL, Stark WS. Characterization of rdgA: mutants with retinal degeneration in Drosophila. J Insect Physiol 1982; 28:233-242.
111. Wang T, Montell C. A phosphoinositide synthase required for a sustained light response. J Neurosci 2006; 26:12816-12825.
112. Hassan BA, Prokopenko SN, Breuer S, Zhang B, Paululat A, Bellen HJ. Skittles, a Drosophila phosphatidylinositol-4-phosphate 5-kinase, is required for cell viability, germline development and bristle morphology, but not for neurotransmitter release. Genetics 1998; 150:1527-1537.
113. Alloway PG, Howard L, Dolph PJ. The formation of stable rhodopsin-arrestin complexes induces apoptosis and photoreceptor cell degeneration. Neuron 2000; 28:129-138.
114. Inoue H, Yoshioka T, Hotta Y. Diacylglycerol kinase defect in a Drosophila retinal degeneration mutant rdgA. J Biol Chem 1989; 264:5996-6000.
115. LaLonde MM, Janssens H, Rosenbaum E, Choi SY, Gergen JP, Colley NJ, et al. Regulation of phototransduction responsiveness and retinal degeneration by a phospholipase D-generated signaling lipid. J Cell Biol 2005; 169:471-479.
116. Garcia-Murillas I, Pettitt T, Macdonald E, Okkenhaug H, Georgiev P, Trivedi D., et al. Lazaro encodes a lipid phosphate phosphohydrolase that regulates phosphatidylinositol turnover during Drosophila phototransduction. Neuron 2006; 49:533-546.
117. Kwon Y, Montell C. Dependence on the Lazaro phosphatidic acid phosphatase for the maximum light response. Curr Biol 2006; 16:723-729.
118. Yoon J, Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, et al. Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci 2000; 20:649-659.
119. Arundine M, Tymianski M. Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 2003; 34:325-337.
120. Wang T, Jiao Y, Montell C. Dissecting independent channel and scaffolding roles of the Drosophila transient receptor potential channel. J Cell Biol 2005; 171:685-694.
121. 2+ regulation of Drosophila phototransduction. Adv Exp Med Biol 2002; 514:493-505.
122. Matsumoto H, Kurien BT, Takagi Y, Kahn ES, Kinumi T, Komori N, et al. Phosrestin I undergoes the earliest light-induced phosphorylation by a calcium/calmodulin-dependent protein kinase in Drosophila photoreceptors. Neuron 1994; 12:997-1010.
123. Byk T, Bar-Yaacov M, Doza YN, Minke B, Selinger Z. Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell. Proc Natl Acad Sci USA 1993; 90:1907-1911.
124. Lee SJ, Xu H, Montell C. Rhodopsin kinase activity modulates the amplitude of the visual response in Drosophila. Proc Natl Acad Sci USA 2004; 101:11874-11879.
125. Orem NR, Dolph PJ. Loss of the phospholipase C gene product induces massive endocytosis of rhodopsin and arrestin in Drosophila photoreceptors. Vision Res 2002; 42:497-505.
126. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 2007; 69:451-482.
127. Orem NR, Xia L, Dolph PJ. An essential role for endocytosis of rhodopsin through interaction of visual arrestin with the AP-2 adaptor. J Cell Sci 2006; 119:3141-3148.
128. Sevrioukov EA, He JP, Moghrabi N, Sunio A, Kramer H. A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol Cell 1999; 4:479-486.
129. Sriram V, Krishnan KS, Mayor S. Deep-orange and carnation define distinct stages in late endosomal biogenesis in Drosophila melanogaster. J Cell Biol 2003; 161:593-607.
130. Warner TS, Sinclair DA, Fitzpatrick KA, Singh M, Devlin RH, Honda BM. The light gene of Drosophila melanogaster encodes a homologue of VPS41, a yeast gene involved in cellular-protein trafficking. Genome 1998; 41:236-243.
131. Acharya JK, Dasgupta U, Rawat SS, Yuan C, Sanxaridis PD, Yonamine I, et al. Cell-nonautonomous function of ceramidase in photoreceptor homeostasis. Neuron 2008; 57:69-79.
132. Ishii I, Fukushima N, Ye X, Chun J. Lysophospholipid receptors: signaling and biology. Annu Rev Biochem 2004; 73:321-354.
133. Acharya U, Patel S, Koundakjian E, Nagashima K, Han X, Acharya JK. Modulating sphingolipid biosynthetic pathway rescues photoreceptor degeneration. Science 2003; 299:1740-1743.
134. Bursch W, Ellinger A, Gerner C, Frohwein U, Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD or others? Ann NY Acad Sci 2000; 926:1-12.
135. Nicholson DW. Caspase structure, proteolytic substrates and function during apoptotic cell death. Cell Death Differ 1999; 6:1028-1042.
136. Yang YL, Li XM. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res 2000; 10:169-177.
137. Steller H. Regulation of apoptosis in Drosophila. Cell Death Differ 2008; 15:1132-1138.
138. Conradt B. Genetic control of programmed cell death during animal development. Annu Rev Genet 2009; 43:493-523.
139. Hsu CD, Whaley MA, Frazer K, Miller DA, Mitchell KA, Adams SM, O'Tousa JE. Limited role of developmental programmed cell death pathways in Drosophila norpA retinal degeneration. J Neurosci 2004; 24:500-507.
140. Davidson FF, Steller H. Blocking apoptosis prevents blindness in Drosophila retinal degeneration mutants. Nature 1998; 391:587-591.
141. Levine B, Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest 2005; 115:2679-2688.
142. Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102-1109.
143. He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93.
144. Komatsu M, Kominami E, Tanaka K. Autophagy and neurodegeneration. Autophagy 2006; 2:315-317.
145. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies. Cell Death Differ 2009; 16:46-56.
146. Wang T, Lao U, Edgar BA. TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J Cell Biol 2009; 186:703-711.
147. Midorikawa R, Yamamoto-Hino M, Awano W, Hinohara Y, Suzuki E, Ueda R, Goto S. Autophagydependent rhodopsin degradation prevents retinal degeneration in Drosophila. J Neurosci 2010; 30:10703-10719.
148. Schinz RH, Lo MV, Larrivee DC, Pak WL. Freezefracture study of the Drosophila photoreceptor membrane: mutations affecting membrane particle density. J Cell Biol 1982; 93:961-967.
149. Ni L, Guo P, Reddig K, Mitra M, Li HS. Mutation of a TADR protein leads to rhodopsin and Gq-dependent retinal degeneration in Drosophila. J Neurosci 2008; 28:13478-13487.