Circadian rhythm of contrast sensitivity is regulated by a dopamine-neuronal PAS-domain protein 2-adenylyl cyclase 1 signaling pathway in retinal ganglion cells

Journal of Neuroscience

Volumn 33, Issue 38, 2013, Pages

  Hwang, Christopher K ^a   Chaurasia, Shyam S ^a,b,c   Jackson, Chad R ^a,d   Chan, Guy C K ^e   Storm, Daniel R ^e   Michael Iuvone, P ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SINGAPORE EYE RESEARCH INSTITUTE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d VANDERBILT UNIVERSITY   (United States)

^e UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; DOPAMINE 4 RECEPTOR; HOMEODOMAIN PROTEIN; MESSENGER RNA; NEURONAL PAS DOMAIN PROTEIN 2; PROTEIN BMAL1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTRAST SENSITIVITY; CONTROLLED STUDY; GENETIC TRANSFECTION; HISTOCHEMISTRY; IMMUNOFLUORESCENCE MICROSCOPY; LASER CAPTURE MICRODISSECTION; LIGHT INTENSITY; METABOLIC REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; VISUAL ACUITY;

ADENYLATE CYCLASE; ANIMALS; ARNTL TRANSCRIPTION FACTORS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA-GALACTOSIDASE; CELL LINE, TRANSFORMED; CIRCADIAN RHYTHM; CONTRAST SENSITIVITY; DOPAMINE; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; PHOTIC STIMULATION; RECEPTORS, DOPAMINE D4; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; TRANSFECTION; VISUAL ACUITY; VISUAL PATHWAYS;

EID: 84884173918     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2039-13.2013     Document Type: Article

References (65)

1. Balkema GW, Cusick K, Nguyen TH (2001) Diurnal variation in synaptic ribbon length and visual threshold. Vis Neurosci 18:789-797. CrossRef Medline
2. Barlow HB, Hill RM, Levick WR (1964) Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J Physiol 173:377-407. Medline
3. Barnard AR, Hattar S, Hankins MW, Lucas RJ (2006) Melanopsin regulates visual processing in the mouse retina. Curr Biol 16:389-395. CrossRef Medline
4. Bassi CJ, Powers MK (1986) Daily fluctuations in the detectability of dim lights by humans. Physiol Behav 38:871-877. CrossRef Medline
5. Cahill GM, Besharse JC (1991) Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light andD2 dopamine receptors. J Neurosci 11:2959-2971. Medline
6. Chan GC, Lernmark U, Xia Z, Storm DR (2001) DNAelements of the type 1 adenylyl cyclase gene locus enhance reporter gene expression in neurons and pinealocytes. Eur J Neurosci 13:2054-2066. CrossRef Medline
7. Cohen AI, Todd RD, Harmon S, O'Malley KL (1992) Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc Natl Acad Sci U S A 89:12093-12097. CrossRef Medline
8. DeBruyne JP, Weaver DR, Reppert SM (2007) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10:543-545. CrossRef Medline
9. Dkhissi-Benyahya O, Coutanson C, Knoblauch K, Lahouaoui H, Leviel V, Rey C, Bennis M, Cooper HM (2013) The absence of melanopsin alters retinal clock function and dopamine regulation by light. Cell Mol Life Sci. Advance online publication. Retrieved August 11, 2013. doi:10.1007/ s00018-013-1338-9. CrossRef Medline
10. Douglas RM, Alam NM, Silver BD, McGill TJ, Tschetter WW, Prusky GT (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci 22:677-684. CrossRef Medline
11. Doyle SE, McIvor WE, Menaker M (2002) Circadian rhythmicity in dopamine content of mammalian retina: role of the photoreceptors. J Neurochem 83:211-219. CrossRef Medline
12. Feigenspan A, Bormann J (1994) Facilitation of GABAergic signaling in the retina by receptors stimulating adenylate cyclase. Proc Natl Acad Sci U S A 91:10893-10897. CrossRef Medline
13. Fukuhara C, Liu C, Ivanova TN, Chan GC, Storm DR, Iuvone PM, Tosini G (2004) Gating of the cAMP signaling cascade and melatonin synthesis by the circadian clock in mammalian retina. J Neurosci 24:1803-1811. CrossRef Medline
14. Garcia JA, Zhang D, Estill SJ, Michnoff C, Rutter J, Reick M, Scott K, Diaz- Arrastia R, McKnight SL (2000) Impaired cued and contextual memory in NPAS2-deficient mice. Science 288:2226-2230. CrossRef Medline
15. Gekakis N, Staknis D, Nguyen HB, Davis FC, Wilsbacher LD, King DP, Takahashi JS, Weitz CJ (1998) Role of the CLOCK protein in the mammalian circadian mechanism. Science 280:1564-1569. CrossRef Medline
16. Greengard P, Jen J, Nairn AC, Stevens CF (1991) Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253:1135-1138. CrossRef Medline
17. Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, Perreau-Lenz S, Brunk I, Spanagel R, Ahnert-Hilger G, Meijer JH, Albrecht U (2008) Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol 18:678-683. CrossRef Medline
18. Haque R, Ali FG, Biscoglia R, Abey J, Weller J, Klein D, Iuvone PM (2010) CLOCK and NPAS2 have overlapping roles in the circadian oscillation of arylalkylamine N-acetyltransferase mRNA in chicken cone photoreceptors. J Neurochem 113:1296-1306. CrossRef Medline
19. Hogenesch JB, Gu YZ, Jain S, Bradfield CA (1998) The basic-helix-loophelix- PAS orphan MOP3 forms transcriptionally active complexes with circadian and hypoxia factors. Proc Natl Acad Sci U S A 95:5474-5479. CrossRef Medline
20. Hogenesch JB, Gu YZ, Moran SM, Shimomura K, Radcliffe LA, Takahashi JS, Bradfield CA (2000) The basic helix-loop-helix-PAS protein MOP9 is a brain-specific heterodimeric partner of circadian and hypoxia factors. J Neurosci 20:RC83. Medline
21. Iuvone PM, Galli CL, Garrison-Gund CK, Neff NH (1978) Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons. Science 202:901-902. CrossRef Medline
22. Jackson CR, Chaurasia SS, Zhou H, Haque R, Storm DR, Iuvone PM (2009) Essential roles of dopamine D4 receptors and the type 1 adenylyl cyclase in photic control of cyclic AMP in photoreceptor cells. J Neurochem 109:148-157. CrossRef Medline
23. Jackson CR, Chaurasia SS, Hwang CK, Iuvone PM (2011) Dopamine D(4) receptor activation controls circadian timing of the adenylyl cyclase 1/cyclic AMP signaling system in mouse retina. Eur J Neurosci 34:57-64. CrossRef Medline
24. Jackson CR, Ruan GX, Aseem F, Abey J, Gamble K, Stanwood G, Palmiter RD, Iuvone PM, McMahon DG (2012) Retinal dopamine mediates multiple dimensions of light-adapted vision. J Neurosci 32:9359-9368. CrossRef Medline
25. Jeon CJ, Strettoi E, Masland RH (1998) The major cell populations of the mouse retina. J Neurosci 18:8936-8946. Medline
26. Kerrison JB, Duh EJ, Yu Y, Otteson DC, Zack DJ (2005) A system for inducible gene expression in retinal ganglion cells. Invest Ophthalmol Vis Sci 46:2932-2939. CrossRef Medline
27. King DP, Zhao Y, Sangoram AM, Wilsbacher LD, Tanaka M, Antoch MP, Steeves TD, Vitaterna MH, Kornhauser JM, Lowrey PL, Turek FW, Takahashi JS (1997) Positional cloning of the mouse circadian clock gene. Cell 89:641-653. CrossRef Medline
28. Knapp AG, Dowling JE (1987) Dopamine enhances excitatory amino acidgated conductances in cultured retinal horizontal cells. Nature 325:437-439. CrossRef Medline
29. Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM (1999) mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98:193-205. CrossRef Medline
30. Li L, Dowling JE (1998) Zebrafish visual sensitivity is regulated by a circadian clock. Vis Neurosci 15:851-857. Medline
31. Liman ER, Knapp AG, Dowling JE (1989) Enhancement of kainate-gated currents in retinal horizontal cells by cyclic AMP-dependent protein kinase. Brain Res 481:399-402. CrossRef Medline
32. Liu AY, Mathur R, Mei N, Langhammer CG, Babiarz B, Firestein BL (2011) Neuroprotective drug riluzole amplifies the heat shock factor 1 (HSF1)- and glutamate transporter 1 (GLT1)-dependent cytoprotective mechanisms for neuronal survival. J Biol Chem 286:2785-2794. CrossRef Medline
33. Liu X, Zhang Z, Ribelayga CP (2012) Heterogeneous expression of the core circadian clock proteins among neuronal cell types in mouse retina. PLoS One 7:e50602. CrossRef Medline
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408. CrossRef Medline
35. Mills SL, Xia XB, Hoshi H, Firth SI, Rice ME, Frishman LJ, Marshak DW (2007) Dopaminergic modulation of tracer coupling in a ganglionamacrine cell network. Vis Neurosci 24:593-608. CrossRef Medline
36. Nadal-Nicolás FM, Jiménez-López M, Sobrado-Calvo P, Nieto-López L, Cánovas-Martínez I, Salinas-Navarro M, Vidal-Sanz M, Agudo M (2009) Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50:3860-3868. CrossRef Medline
37. Oak JN, Lavine N, Van Tol HH (2001) Dopamine D(4) and D(2L) receptor stimulation of the mitogen-activated protein kinase pathway is dependent on trans-activation of the platelet-derived growth factor receptor. Mol Pharmacol 60:92-103. Medline
38. Oldenhof J, Vickery R, Anafi M, Oak J, Ray A, Schoots O, Pawson T, von Zastrow M, Van Tol HH (1998) SH3 binding domains in the dopamine D4 receptor. Biochemistry 37:15726-15736. CrossRef Medline
39. O'Neill JS, Maywood ES, Chesham JE, Takahashi JS, Hastings MH (2008) cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320:949-953. CrossRef Medline
40. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45:4611-4616. CrossRef Medline
41. Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia A-S, White LE (2012) In: Neuroscience, Ed 5, pp 277-288. Sunderland, MA: Sinauer Associates.
42. Reick M, Garcia JA, Dudley C, McKnight SL (2001) NPAS2: an analog of clock operative in the mammalian forebrain. Science 293:506-509. CrossRef Medline
43. Ribelayga C, Wang Y, Mangel SC (2004) A circadian clock in the fish retina regulates dopamine release via activation of melatonin receptors. J Physiol 554:467-482. CrossRef Medline
44. Ruan GX, Zhang DQ, Zhou T, Yamazaki S, McMahon DG (2006) Circadian organization of the mammalian retina. Proc Natl Acad Sci U S A 103: 9703-9708. CrossRef Medline
45. Ruan GX, Allen GC, Yamazaki S, McMahon DG (2008) An autonomous circadian clock in the inner mouse retina regulated by dopamine and GABA. PLoS Biol 6:e249. CrossRef Medline
46. Rubinstein M, Phillips TJ, Bunzow JR, Falzone TL, Dziewczapolski G, Zhang G, Fang Y, Larson JL, McDougall JA, Chester JA, Saez C, Pugsley TA, Gershanik O, Low MJ, Grandy DK (1997) Mice lacking dopamine D4 receptors are supersensitive to ethanol, cocaine, and methamphetamine. Cell 90:991-1001. CrossRef Medline
47. Salinas-Navarro M, Mayor-Torroglosa S, Jiménez-López M, Avilés- Trigueros M, Holmes TM, Lund RD, Villegas-Pérez MP, Vidal-Sanz M (2009) A computerized analysis of the entire retinal ganglion cell population and its spatial distribution in adult rats. Vis Res 49:115-126. CrossRef Medline
48. Solessio E, Scheraga D, Engbretson GA, Knox BE, Barlow RB (2004) Circadian modulation of temporal properties of the rod pathway in larval Xenopus. J Neurophysiol 92:2672-2684. CrossRef Medline
49. Storch KF, Paz C, Signorovitch J, Raviola E, Pawlyk B, Li T, Weitz CJ (2007) Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information. Cell 130:730-741. CrossRef Medline
50. Stradleigh TW, Ogata G, Partida GJ, Oi H, Greenberg KP, Krempely KS, Ishida AT (2011) Colocalization of hyperpolarization-activated, cyclic nucleotide-gated channel subunits in rat retinal ganglion cells. J Comp Neurol 519:2546-2573. CrossRef Medline
51. Sun W, Deng Q, Levick WR, He S (2006) ON direction-selective ganglion cells in the mouse retina. J Physiol 576:197-202. CrossRef Medline
52. Takeuchi Y, Yamamoto H, Miyakawa T, Miyamoto E (2000) Increase of brain-derived neurotrophic factor gene expression in NG108-15 cells by the nuclear isoforms of Ca2+/calmodulin-dependent protein kinase II. J Neurochem 74:1913-1922. CrossRef Medline
53. Tassi P, Pellerin N, Moessinger M, Eschenlauer R, Muzet A (2000) Variation of visual detection over the 24-hour period in humans. Chronobiol Int 17:795-805. CrossRef Medline
54. van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Wit J, Verkerk A, Eker AP, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JH, Yasui A (1999) Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398:627-630. CrossRef Medline
55. Vaney DI, Sivyer B, Taylor WR (2012) Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci 13:194-208. CrossRef Medline
56. Veruki ML, Yeh HH (1994) Vasoactive intestinal polypeptide modulates GABAAreceptor function through activation of cyclic AMP. Vis Neurosci 11:899-908. CrossRef Medline
57. Wan DC, Choi RC, Siow NL, Tsim KW (2000) The promoter of human acetylcholinesterase is activated by a cyclic adenosine 3′,5′-monophosphatedependent pathway in cultured NG108-15 neuroblastoma cells. Neurosci Lett 288:81-85. CrossRef Medline
58. Wang H, Ferguson GD, Pineda VV, Cundiff PE, Storm DR (2004) Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Nat Neurosci 7:635-642. CrossRef Medline
59. Weng S, Sun W, He S (2005) Identification of ON-OFF direction-selective ganglion cells in the mouse retina. J Physiol 562:915-923. CrossRef Medline
60. Wu ZL, Thomas SA, Villacres EC, Xia Z, Simmons ML, Chavkin C, Palmiter RD, Storm DR (1995) Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc Natl Acad Sci U S A 92:220-224. CrossRef Medline
61. Yu CJ, Gao Y, Li P, Li L (2007) Synchronizing multiphasic circadian rhythms of rhodopsin promoter expression in rod photoreceptor cells. J Exp Biol 210:676-684. CrossRef Medline
62. Yujnovsky I, Hirayama J, Doi M, Borrelli E, Sassone-Corsi P (2006) Signaling mediated by the dopamine D2 receptor potentiates circadian regulation by CLOCK:BMAL1. Proc Natl Acad Sci U S A 103:6386-6391. CrossRef Medline
63. Zhang DQ, Wong KY, Sollars PJ, Berson DM, Pickard GE, McMahon DG (2008) Intraretinal signaling by ganglion cell photoreceptors to dopaminergic amacrine neurons. Proc Natl Acad Sci U S A 105:14181-14186. CrossRef Medline
64. Zheng B, Albrecht U, Kaasik K, Sage M, Lu W, Vaishnav S, Li Q, Sun ZS, Eichele G, Bradley A, Lee CC (2001) Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105:683-694. CrossRef Medline
65. Zhou YD, Barnard M, Tian H, Li X, Ring HZ, Francke U, Shelton J, Richardson J, Russell DW, McKnight SL (1997) Molecular characterization of two mammalian bHLH-PAS domain proteins selectively expressed in the central nervous system. Proc Natl Acad Sci U S A 94:713-718. CrossRef Medline