Light activation of the phosphoinositide cycle in intrinsically photosensitive chicken retinal ganglion cells

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 11, 2010, Pages 5491-5498

  Contín, Maria Ana ^a   Verra, Daniela M ^a   Salvador, Gabriela ^b   Ilincheta, Monica ^b   Giusto, Norma M ^b   Guido, Mario E ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; CALCIUM ION; DIACYLGLYCEROL KINASE; INOSITOL TRISPHOSPHATE 3 KINASE; MELANOPSIN; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PROTEIN OPN4M; PROTEIN OPN4X; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CHICKEN; CONTROLLED STUDY; DARKNESS; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; LIGHT EXPOSURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSTIMULATION; PRIORITY JOURNAL; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

1-PHOSPHATIDYLINOSITOL 4-KINASE; ANILINE COMPOUNDS; ANIMALS; CALCIUM; CELLS, CULTURED; CHICK EMBRYO; DARK ADAPTATION; DIACYLGLYCEROL KINASE; DNA PRIMERS; ESTRENES; INOSITOL 1,4,5-TRISPHOSPHATE; LIGHT; MICROSCOPY, FLUORESCENCE; PHOSPHATIDYLINOSITOLS; PHOSPHODIESTERASE INHIBITORS; PHOTIC STIMULATION; PYRROLIDINONES; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ROD OPSINS; TYPE C PHOSPHOLIPASES; XANTHENES;

EID: 78549273743     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-5643     Document Type: Article

References (63)

1. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295: 1070-1073.
2. Hattar S, Liao HW, Takao M, Berson DM, Yau KW. Melanopsincontaining retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002;295:1065-1070.
3. Hattar S, Lucas RJ, Mrosovsky N, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature. 2003;424:76-81.
4. Lucas RJ, Hattar S, Takao M, Berson DM, Foster RG, Yau KW. Diminished pupillary light reflex at high irradiances in melanopsinknockout mice. Science. 2003;299:245-247.
5. Panda S, Sato TK, Castrucci AM, et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002;298:2213-2216.
6. Valdez DJ, Nieto PS, Garbarino-Pico E, et al. A nonmammalian vertebrate model of blindness reveals functional photoreceptors in the inner retina. FASEB J. 2009;23:1186-1195.
7. Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD. A novel human opsin in the inner retina. J Neurosci. 2000; 20:600-605.
8. Arendt D. Evolution of eyes and photoreceptor cell types. Int J Devel Biology. 2003;47:563-571.
9. Isoldi MC, Rollag MD, Castrucci AM, Provencio I. Rhabdomeric phototransduction initiated by the vertebrate photopigment melanopsin. Proc Natl Acad Sci USA. 2005;102:1217-1221.
10. Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr Biol. 2005;15:1065-1069.
11. Melyan Z, Tarttelin EE, Bellingham J, Lucas RJ, Hankins MW. Addition of human melanopsin renders mammalian cells photoresponsive. Nature. 2005;433:741-745.
12. Panda S, Nayak SK, Campo B, Walker JR, Hogenesch JB, Jegla T. Illumination of the melanopsin signaling pathway. Science. 2005; 307:600-604.
13. Qiu X, Kumbalasiri T, Carlson SM, et al. Induction of photosensitivity by heterologous expression of melanopsin. Nature. 2005; 433:745-749.
14. Warren EJ, Allen CN, Brown RL, Robinson DW. The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur J Neurosci. 2006;23:2477-2487.
15. Contin MA, Verra DM, Guido ME. An invertebrate-like phototransduction cascade mediates light detection in the chicken retinal ganglion cells. FASEB J. 2006;20:2648-2650.
16. Berson DM. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci. 2003;26:314-320.
17. Bellingham J, Chaurasia SS, Melyan Z, et al. Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates. PLoS Biol. 2006;4:e254.
18. Torii M, Kojima D, Okano T, et al. Two isoforms of chicken melanopsins show blue light sensitivity. FEBS Lett. 2007;581: 5327-5331.
19. Tomonari S, Takagi A, Akamatsu S, Noji S, Ohuchi H. A noncanonical photopigment, melanopsin, is expressed in the differentiating ganglion, horizontal, and bipolar cells of the chicken retina. Dev Dyn. 2005;234:783-790.
20. Tomonari S, Takagi A, Noji S, Ohuchi H. Expression pattern of the melanopsin-like (cOpn4m) and VA opsin-like genes in the developing chicken retina and neural tissues. Gene Expr Patterns. 2007;7:746-753.
21. Bailey MJ, Cassone VM. Melanopsin expression in the chick retina and pineal gland. Brain Res Mol Brain Res. 2005;134:345-348.
22. Chaurasia SS, Rollag MD, Jiang G, et al. Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types. J Neurochem. 2005;92:158-170.
23. Lima LH, Scarparo AC, Isoldi MC, Visconti MA, Castrucci AM. Melanopsin in chicken melanocytes and retina. Biol Rhythm Res. 2006;37:393-404.
24. Bailey MJ, Chong NW, Xiong J, Cassone VM. Chickens' Cry2: molecular analysis of an avian cryptochrome in retinal and pineal photoreceptors. FEBS Lett. 2002;513:169-174.
25. Haque R, Chaurasia SS, Wessel JH 3rd, Iuvone PM. Dual regulation of cryptochrome 1 mRNA expression in chicken retina by light and circadian oscillators. Neuroreport. 2002;13:2247-2251.
26. Kubo Y, Akiyama M, Fukada Y, Okano T. Molecular cloning, mRNA expression, and immunocytochemical localization of a putative blue-light photoreceptor CRY4 in the chicken pineal gland. J Neurochem. 2006;97:1155-1165.
27. Yamamoto K, Okano T, Fukada Y. Chicken pineal Cry genes: light-dependent up-regulation of cCry1 and cCry2 transcripts. Neurosci Lett. 2001;313:13-16.
28. Berson DM. Phototransduction in ganglion-cell photoreceptors. Pflugers Arch. 2007;454:849-855.
29. Hardie RC, Raghu P. Visual transduction in Drosophila. Nature. 2001;413:186-193.
30. Lee YJ, Shah S, Suzuki E, Zars T, O'Day PM, Hyde DR. The Drosophila dgq gene encodes a G alpha protein that mediates phototransduction. Neuron. 1994;13:1143-1157.
31. Montell C. Visual transduction in Drosophila. Annu Rev Cell Dev Biol. 1999;15:231-268.
32. Hardie RC. TRP channels in Drosophila photoreceptors: the lipid connection. Cell Calcium. 2003;33:385-393.
33. Sekaran S, Foster RG, Lucas RJ, Hankins MW. Calcium imaging reveals a network of intrinsically light-sensitive inner-retinal neurons. Curr Biol. 2003;13:1290-1298.
34. Graham DM, Wong KY, Shapiro P, Frederick C, Pattabiraman K, Berson DM. Melanopsin ganglion cells use a membrane-associated rhabdomeric phototransduction cascade. J Neurophysiol. 2008; 99:2522-2532.
35. LaLonde MM, Janssens H, Rosenbaum E, et al. Regulation of phototransduction responsiveness and retinal degeneration by a phospholipase D-generated signaling lipid. J Cell Biol. 2005; 169: 471-479.
36. Suh BC, Inoue T, Meyer T, Hille B. Rapid chemically induced changes of PtdIns(4,5)P2 gate KCNQ ion channels. Science. 2006; 314:1454-1457.
37. Brocco MA, Panzetta P. Survival and differentiation of purified embryonic chick retinal ganglion cells cultured at low density in a chemically defined medium. J Neurosci Methods. 1997;75:15-20.
38. Garbarino-Pico E, Carpentieri AR, Contin MA, et al. Retinal ganglion cells are autonomous circadian oscillators synthesizing Nacetylserotonin during the day. J Biol Chem. 2004;279:51172-51181.
39. Bobu C, Craft CM, Masson-Pevet M, Hicks D. Photoreceptor organization and rhythmic phagocytosis in the Nile rat Arvicanthis ansorgei: a novel diurnal rodent model for the study of cone pathophysiology. Invest Ophthalmol Vis Sci. 2006;47:3109-3118.
40. Bird IM. Phosphoinositidase C activation assay. I Cell labeling, stimulation, and recovery of cellular [3H]phosphoinositides and [3H]phosphoinositols. Methods Mol Biol. 1998;105:1-9.
41. Bird IM. Phosphoinositidase C activation assay. II. Simple analysis of recovered cellular phosphoinositides and phosphoinositols. Methods Mol Biol. 1998;105:11-23.
42. Bird IM. Preparation of [3H]phosphoinositol standards and conversion of [3H]phosphoinositides to [3H]phosphoinositols. Methods Mol Biol. 1998;105:65-76.
43. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37:911-917.
44. Jolles J, Bar PR, Gispen WH. Modulation of brain polyphosphoinositide metabolism by ACTH and beta-endorphin: structure-activity studies. Brain Res. 1981;224:315-326.
45. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509.
46. Baldridge WH, Kurennyi DE, Barnes S. Calcium-sensitive calcium influx in photoreceptor inner segments. J Neurophysiol. 1998;79: 3012-3018.
47. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156-159.
48. Agranoff BW, Fisher SK. Inositol, lithium, and the brain. Psychopharmacol Bull. 2001;35:5-18.
49. Hardie RC, Martin F, Cochrane GW, Juusola M, Georgiev P, Raghu P. Molecular basis of amplification in Drosophila phototransduction: roles for G protein, phospholipase C, and diacylglycerol kinase. Neuron. 2002;36:689-701.
50. Zuker CS. The biology of vision of Drosophila. Proc Natl Acad Sci USA. 1996;93:571-576.
51. Thanos S, Mey J. Development of the visual system of the chick, II: mechanisms of axonal guidance. Brain Res Brain Res Rev. 2001; 35:205-245.
52. Hartwick AT, Bramley JR, Yu J, et al. Light-evoked calcium responses of isolated melanopsin-expressing retinal ganglion cells. J Neurosci. 2007;27:13468-13480.
53. Wong KY, Dunn FA, Graham DM, Berson DM. Synaptic influences on rat ganglion-cell photoreceptors. J Physiol. 2007;582:279-296.
54. Schmidt TM, Kofuji P. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci. 2009;29:476-482.
55. Fisher SK, Heacock AM, Agranoff BW. Inositol lipids and signal transduction in the nervous system: an update. J Neurochem. 1992;58:18-38.
56. Hardie RC. Phototransduction in Drosophila melanogaster. J Exp Biol. 2001;204:3403-3409.
57. Goto K, Kondo H. Functional implications of the diacylglycerol kinase family. Adv Enzyme Regul. 2004;44:187-199.
58. Sakane F, Imai S, Yamada K, Kanoh H. The regulatory role of EF-hand motifs of pig 80K diacylglycerol kinase as assessed using truncation and deletion mutants. Biochem Biophys Res Commun. 1991;181:1015-1021.
59. Kai M, Sakane F, Imai S, Wada I, Kanoh H. Molecular cloning of a diacylglycerol kinase isozyme predominantly expressed in human retina with a truncated and inactive enzyme expression in most other human cells. J Biol Chem. 1994;269:18492-18498.
60. Giusto NM, Ilincheta de Boschero MG. Synthesis of polyphosphoinositides in vertebrate photoreceptor membranes. Biochim Biophys Acta. 1986;877:440-446.
61. Huang Z, Ghalayini A, Guo XX, Alvarez KM, Anderson RE. Lightmediated activation of diacylglycerol kinase in rat and bovine rod outer segments. J Neurochem. 2000;75:355-362.
62. Wu L, Niemeyer B, Colley N, Socolich M, Zuker CS. Regulation of PLC-mediated signalling in vivo by CDP-diacylglycerol synthase. Nature. 1995;373:216-222.
63. Harris WA, Stark WS. Hereditary retinal degeneration in Drosophila melanogaster: a mutant defect associated with the phototransduction process. J Gen Physiol. 1977;69:261-291.