Compartmentalization and Ca2+ buffering are essential for prevention of light-induced retinal degeneration

Journal of Neuroscience

Volumn 32, Issue 42, 2012, Pages 14696-14708

  Weiss, Shirley ^a   Kohn, Elkana ^a   Dadon, Daniela ^a   Katz, Ben ^a   Peters, Maximilian ^a   Lebendiker, Mario ^b   Kosloff, Mickey ^c   Colley, Nansi Jo ^d   Minke, Baruch ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY OF HAIFA   (Israel)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALPHOTIN; CYTOPLASM PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN; UNCLASSIFIED DRUG; BUFFER; CALCIUM BINDING PROTEIN; CALPHOTIN PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN;

ANIMAL TISSUE; ARTICLE; CALCIUM HOMEOSTASIS; CELL COMPARTMENTALIZATION; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DROSOPHILA; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; ELECTRORETINOGRAPHY; FEMALE; GRANULE CELL; HUMAN; HUMAN CELL; LIGHT; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR CELL; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION; WESTERN BLOTTING; ANIMAL; CELL STRAIN HEK293; DARK ADAPTATION; DROSOPHILA MELANOGASTER; METABOLISM; PATHOLOGY; PH; PHYSIOLOGY; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BUFFERS; CALCIUM; CALCIUM-BINDING PROTEINS; CELL COMPARTMENTATION; DARK ADAPTATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; LIGHT; PHOTORECEPTOR CELLS, INVERTEBRATE; RETINAL DEGENERATION;

EID: 84867590095     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2456-12.2012     Document Type: Article

References (45)

1. Abramoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics International 11:36-42.
2. 2+ signalling takes the local route. Curr Opin Neurobiol 2:302-307.
3. Avidor-Reiss T, Maer AM, Koundakjian E, Polyanovsky A, Keil T, Subramaniam S, Zuker CS (2004) Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis. Cell 117:527-539.
4. Ballinger DG, Xue N, Harshman KD (1993) A Drosophila photoreceptor cell-specific protein, calphotin, binds calcium and contains a leucine zipper. Proc Natl Acad Sci U S A 90:1536-1540.
5. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
6. Chang HY, Ready DF (2000) Rescue of photoreceptor degeneration in rhodopsin-null Drosophila mutants by activated Rac1. Science 290:1978-1980.
7. 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.
8. Cosens D, Perry MM (1972) The fine structure of the eye of a visual mutant, A-type of Drosophila melanogaster. J Insect Physiol 18:1773-1786.
9. Elia N, Frechter S, Gedi Y, Minke B, Selinger Z (2005) Excess of Gβ over Gqα in vivo prevents dark, spontaneous activity of Drosophila photoreceptors. J Cell Biol 171:517-526.
10. Endo H, Persson P, Watanabe T (2000) Molecular cloning of the crustacean DD4 cDNA encoding a Ca(2+)-binding protein. Biochem Biophys Res Commun 276:286-291.
11. Franceschini N, Kirschfeld K (1971a) In vivo optical study of photoreceptor elements in the compound eye of Drosophila (in French). Kybernetik 8:1-13.
12. Franceschini N, Kirschfeld K (1971b) Pseudopupil phenomena in the compound eye of Drosophila (in French). Kybernetik 9:159-182.
13. Franceschini N, Kirschfeld K (1976) Le contrôle automatique du flux lumineux dans l'oeil composé des diptéres. Biol Cybern 21:181-203.
14. Gu Y, Oberwinkler J, Postma M, Hardie RC (2005) Mechanisms of light adaptation in Drosophila photoreceptors. Curr Biol 15:1228-1234.
15. 2+ facilitates and inactivates but does not directly excite light-sensitive channels in Drosophila photoreceptors. J Neurosci 15:889-902.
16. 2+concentration in Drosophila photoreceptors. J Neurosci 16:2924-2933.
17. 2+ channel in Drosophila photoreceptors. Neuron 8:643-651.
18. Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186-193.
19. 2+channel essential for phosphoinositide-mediated photoreception, forms a signaling complex with NorpA, InaC and InaD. EMBO J 15:7036-7045.
20. Iakhine R, Chorna-Ornan I, Zars T, Elia N, Cheng Y, Selinger Z, Minke B, Hyde DR (2004) Novel dominant rhodopsin mutation triggers two mechanisms of retinal degeneration and photoreceptor desensitization. J Neurosci 24:2516-2526.
21. Katz B, Minke B (2009) Drosophila photoreceptors and signaling mechanisms. Front Cell Neurosci 3:2.
22. Katz B, Minke B (2012) Phospholipase C-mediated suppression of dark noise enables single-photon detection in Drosophila photoreceptors. J Neurosci 32:2722-2733.
23. Kirschfeld K, Vogt K (1980) Calcium ions and pigment migration in fly photoreceptors. Naturwissenschaften 67:516-517.
24. Koch C, Zador A (1993) The function of dendritic spines: devices subserv-ing biochemical rather than electrical compartmentalization. J Neurosci 13:413-422.
25. Lee YS, Carthew RW (2003) Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30:322-329.
26. Lenzi D, Roberts WM (1994) Calcium signalling in hair cells: multiple roles in a compact cell. Curr Opin Neurobiol 4:496-502.
27. Lo MV, Pak WL (1981) Light-induced pigment granule migration in the retinular cells of Drosophila melanogaster. Comparison of wild type with ERG-defective mutants. J Gen Physiol 77:155-175.
28. Martin JH, Benzer S, Rudnicka M, Miller CA (1993) Calphotin: a Drosophila photoreceptor cell calcium-binding protein. Proc Natl Acad Sci U S A 90:1531-1535.
29. Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS (1996) The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85:651-659.
30. Oberwinkler J, Stavenga DG (1998) Light dependence of calcium and membrane potential measured in blowfly photoreceptors in vivo. J Gen Physiol 112:113-124.
31. Oberwinkler J, Stavenga DG (2000a) Calcium transients in the rhabdomeres of dark- and light-adapted fly photoreceptor cells. J Neurosci 20:1701-1709.
32. Oberwinkler J, Stavenga DG (2000b) Calcium imaging demonstrates colocalization of calcium influx and extrusion in fly photoreceptors. Proc Natl Acad Sci U S A 97:8578-8583.
33. 2+ channels: impact on cell function. J Physiol 586:3043-3054.
34. 2+ underlies the voltage dependence of Drosophila TRPL channel. J Gen Physiol 129:17-28.
35. Parnas M, Peters M, Dadon D, Lev S, Vertkin I, Slutsky I, Minke B (2009) Carvacrol is a novel inhibitor of Drosophila TRPL and mammalian TRPM7 channels. Cell Calcium 45:300-309.
36. Peretz A, Suss-Toby E, Rom-Glas A, Arnon A, Payne R, Minke B (1994a) The light response of Drosophila photoreceptors is accompanied by an increase in cellular calcium: effects of specific mutations. Neuron 12:1257-1267.
37. 2+ influx into Drosophila photoreceptors. J Gen Physiol 104:1057-1077.
38. Satoh AK, Li BX, Xia H, Ready DF (2008) Calcium-activated myosin V closes the Drosophila pupil. Curr Biol 18:951-955.
39. 2+ buffers. Cold Spring Harb Perspect Biol 2:a004051.
40. Tsunoda S, Sierralta J, Sun Y, Bodner R, Suzuki E, Becker A, Socolich M, Zuker CS (1997) A multivalent PDZ-domain protein assembles signaling complexes in a G-protein-coupled cascade. Nature 388: 243-249.
41. 2+ exchanger CalX. Neuron 45:367-378.
42. Yang Y, Ballinger D (1994) Mutations in calphotin, the gene encoding a Drosophila photoreceptor cell-specific calcium-binding protein, reveal roles in cellular morphogenesis and survival. Genetics 138:413-421.
43. Yoon J, Cohen Ben-Ami HC, Hong YS, Park S, Strong LL, Bowman J, Geng C, Baek K, Minke B, Pak WL (2000) Novel mechanism of massive photoreceptor degeneration caused by mutations in the trp gene of Drosophila. J Neurosci 20:649-659.
44. Zhivotovsky B, Orrenius S (2011) Calcium and cell death mechanisms: a perspective from the cell death community. Cell Calcium 50:211-221.
45. Zhou Z, Neher E (1993) Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J Physiol 469:245-273.