Melatonin: An underappreciated player in retinal physiology and pathophysiology

Experimental Eye Research

Volumn 103, Issue , 2012, Pages 82-89

  Tosini, Gianluca ^a   Baba, Kenkichi ^a   Hwang, Christopher K ^b   Iuvone, P Michael ^b  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Circadian rhythms; Dopamine; Glaucoma; Melatonin; Photoreceptor degeneration; Retina

Indexed keywords

ARALKYLAMINE ACETYLTRANSFERASE; MELATONIN; N ACETYLSEROTONIN; TRYPTOPHAN HYDROXYLASE;

ANTIOXIDANT ACTIVITY; BIOSYNTHESIS; CIRCADIAN RHYTHM; ELECTRORETINOGRAM; GENE; GLAUCOMA; HORMONE ACTION; HORMONE SYNTHESIS; HUMAN; INTRAOCULAR PRESSURE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHOTORECEPTOR; PHOTOSENSITIVITY; PHYSIOLOGY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RETINA; RETINA DISEASE; RETINA GANGLION CELL; RETINA MACULA AGE RELATED DEGENERATION; RETINA NEUROEPITHELIAL LAYER; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

CIRCADIAN RHYTHM; HUMANS; MELATONIN; RECEPTORS, MELATONIN; RETINA; RETINAL DEGENERATION;

EID: 84866169882     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2012.08.009     Document Type: Review

References (145)

1. Alarma-Estrany P., Crooke A., Mediero A., Peláez T., Pintor J. Sympathetic nervous system modulates the ocular hypotensive action of MT2-melatonin receptors in normotensive rabbits. J. Pineal Res. 2008, 45:468-475.
2. Alarma-Estrany P., Crooke A., Pintor J. 5-MCA-NAT does not act through NQO2 to reduce intraocular pressure in New Zealand white rabbit. J. Pineal Res. 2009, 47:201-209.
3. Alcantara-Contreras S., Baba K., Tosini G. Removal of melatonin receptor type 1 increases intraocular pressure and retinal ganglion cells death in the mouse. Neurosci. Lett. 2011, 494:61-64.
4. Ayoub M.A., Couturier C., Lucas-Meunier E., Angers S., Fossier P., Bouvier M., Jockers R. Monitoring of ligand-independent dimerization and ligand-induced conformational changes of melatonin receptors in living cells by bioluminescence resonance energy transfer. J. Biol. Chem. 2002, 277:21522-21528.
5. Ayoub M.A., Levoye A., Delagrange P., Jockers R. Preferential formation of MT1/MT2 melatonin receptors heterodimers with distinct ligand interaction property compared with MT2 homodimers. Mol. Pharmacol. 2004, 66:312-321.
6. Baba K., Pozdeyev N., Mazzoni F., Contreras-Alcantara S., Liu C., Kasamatsu M., Martinez-Merlos T., Strettoi E., Iuvone P.M., Tosini G. Melatonin modulates visual function and cell viability in the mouse retina via the MT1 melatonin receptor. Proc. Natl. Acad. Sci. U S A 2009, 106:15043-15048.
7. Baba K., Mazzoni F., Owino S., Contreras-Alcantara S., Strettoi E., Tosini G. Age-related changes in the daily rhythm of photoreceptor functioning and circuitry in a melatonin-proficient mouse strain. PLoS One 2012, 7:e37799.
8. Baler R., Covington S., Klein D.C. The rat arylalkylamine N-acetyltransferase gene promoter. cAMP activation via a cAMP-responsive element-CCAAT complex. J. Biol. Chem. 1997, 272:6979-6985.
9. Baler R., Covington S., Klein D.C. Rat arylalkylamine N-acetyltransferase gene: upstream and intronic components of a bipartite promoter. Biol. Cell. 1999, 91:699-705.
10. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
11. Belforte N.A., Moreno M.C., de Zavalía N., Sande P.H., Chianelli M.S., Keller-Sarmiento M.I., Rosenstein R.E. Melatonin: a novel neuroprotectant for the treatment of glaucoma. J. Pineal Res. 2010, 48:353-364.
12. Besharse J.C., Dunis D.A. Methoxyindoles and photoreceptor metabolism: activation of rod shedding. Science 1983, 219:1341-1343.
13. Besharse J.C., Zhuang M., Freeman K., Fogerty J. Regulation of photoreceptor Per1 and Per2 by light, dopamine and a circadian clock. Eur. J. Neurosci. 2004 Jul, 20(1):167-174.
14. Besseau L., Benyassi A., Møller M., Coon S.L., Weller J.L., Boeuf G., Klein D.C., Falcón J. Melatonin pathway: breaking the 'high-at-night' rule in trout retina. Exp. Eye Res. 2006, 82:620-627.
15. Boatright J.H., Rubim N.M., Iuvone P.M. Regulation of endogenous dopamine release in amphibian retina by melatonin: the role of GABA. Vis. Neurosci. 1994, 11:1013-1018.
16. Bonnefond A., Clément N., Fawcett K., Yengo L., Vaillant E., Guillaume J.L., Dechaume A., Payne F., Roussel R., Czernichow S., Hercberg S., Hadjadj S., Balkau B., Marre M., Lantieri O., Langenberg C., Bouatia-Naji N., Meta-Analysis of Glucose and Insulin-Related Traits Consortium (MAGIC), Charpentier G., Vaxillaire M., Rocheleau G., Wareham N.J., Sladek R., McCarthy M.I., Dina C., Barroso I., Jockers R., Froguel P. Rare MTNR1B variants impairing melatonin receptor 1B function contribute to type 2 diabetes. Nat. Genet. 2012, 44:297-301.
17. Cahill G.M., Besharse J.C. Retinal melatonin is metabolized within the eye of Xenopus laevis. Proc. Natl. Acad. Sci. U S A 1989, 86:1098-1102.
18. Cahill G.M., Besharse J.C. Circadian regulation of melatonin in the retina of Xenopus laevis: limitation by serotonin availability. J. Neurochem. 1990, 54:716-719.
19. Cahill G.M., Besharse J.C. Resetting the circadian clock in cultured Xenopus eyecups: regulation of retinal melatonin rhythms by light and D2 dopamine receptors. J. Neurosci. 1991, 11:2959-2971.
20. Cahill G.M., Besharse J.C. Circadian clock functions localized in xenopus retinal photoreceptors. Neuron 1993, 10:573-577.
21. Celebi S., Dilsiz N., Yilmaz T., Kükner A.S. Effects of melatonin, vitamin E and octreotide on lipid peroxidation during ischemia-reperfusion in the guinea pig retina. Eur. J. Ophthalmol. 2002, 12:77-83.
22. Chaste P., Clement N., Mercati O., Guillaume J.L., Delorme R., Botros H.G., Pagan C., Périvier S., Scheid I., Nygren G., Anckarsäter H., Rastam M., Ståhlberg O., Gillberg C., Serrano E., Lemière N., Launay J.M., Mouren-Simeoni M.C., Leboyer M., Gillberg C., Jockers R., Bourgeron T. Identification of pathway-biased and deleterious melatonin receptor mutants in autism spectrum disorders and in the general population. PLoS One 2010, 5:e11495.
23. Chaurasia S.S., Pozdeyev N., Haque R., Visser A., Ivanova T.N., Iuvone P.M. Circadian clockwork machinery in neural retina: evidence for the presence of functional clock components in photoreceptor-enriched chick retinal cell cultures. Mol. Vis. 2006, 12:215-223.
24. Chaurasia S.S., Haque R., Pozdeyev N., Jackson C.R., Iuvone P.M. Temporal coupling of cyclic AMP and Ca/calmodulin-stimulated adenylyl cyclase to the circadian clock in chick retinal photoreceptor cells. J. Neurochem. 2006, 99:1142-1150.
25. Chen W., Baler R. The rat arylalkylamine N-acetyltransferase E-box: differential use in a master vs. a slave oscillator. Brain Res. Mol. Brain Res. 2000, 81:43-50.
26. Chong N.W., Cassone V.M., Bernard M., Klein D.C., Iuvone P.M. Circadian expression of tryptophan hydroxylase mRNA in the chicken retina. Brain Res. Mol. Brain Res. 1998, 61:243-250.
27. Chong N.W., Bernard M., Klein D.C. Characterization of the chicken serotonin N-acetyltransferase gene. Activation via clock gene heterodimer/E box interaction. J. Biol. Chem. 2000, 275:32991-32998.
28. Cohen A.I., Todd R.D., Harmon S., O'Malley K.L. Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. Proc. Natl. Acad. Sci. U S A 1992, 89:12093-12097.
29. Coon S.L., Mazuruk K., Bernard M., Roseboom P.H., Klein D.C., Rodriguez I.R. The human serotonin N-acetyltransferase (EC 2.3.1.87) gene (AANAT): structure, chromosomal localization, and tissue expression. Genomics 1996, 34:76-84.
30. Coon S.L., Del Olmo E., Young W.S., Klein D.C. Melatonin synthesis enzymes in Macaca mulatta: focus on arylalkylamine N-acetyltransferase (EC 2.3.1.87). J. Clin. Endocrinol. Metab. 2002, 87:4699-4706.
31. DeVries G.W., Cohen A.I., Hall I.A., Ferrendelli J.A. Cyclic nucleotide levels in normal and biologically fractionated mouse retina: effects of light and dark adaptation. J. Neurochem. 1978, 31:1345-1351.
32. Dinet V., Korf H.-W. Impact of melatonin receptors on pCREB and clock-gene protein levels in the murine retina. Cell. Tissue Res. 2007, 330:29-34.
33. Dinet V., Ansari N., Torres-Farfan C., Korf H.-W. Clock gene expression in the retina of melatonin-proficient (C3H) and melatonindeficient (C57BL) mice. J. Pineal Res. 2007, 42:83-91.
34. Doyle S.E., Grace M.S., McIvor W., Menaker M. Circadian rhythms of dopamine in mouse retina: the role of melatonin. Vis. Neurosci. 2002, 19:593-601.
35. Dubocovich M.L. Melatonin is a potent modulator of dopamine release in the retina. Nature 1983, 306:782-784.
36. Dubocovich M.L., Delagrange P., Krause D.N., Sugden D., Cardinali D.P., Olcese J. International Union of Basic and Clinical Pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacol. Rev. 2010, 62:343-380.
37. Fu Y., Tang M., Fan Y., Zou H., Sun X., Xu X. Anti-apoptotic effects of melatonin in retinal pigment epithelial cells. Front. Biosci. 2012, 17:1461-1468.
38. Fujieda H., Hamadanizadeh S.A., Wankiewicz E., Pang S.F., Brown G.M. Expression of mt1 melatonin receptor in rat retina: evidence for multiple cell targets for melatonin. Neuroscience 1999, 93:793-799.
39. Fujieda H., Scher J., Hamadanizadeh S.A., Wankiewicz E., Pang S.F., Brown G.M. Dopaminergic and GABAergic amacrine cells are direct targets of melatonin: immunocytochemical study of mt1 melatonin receptor in guinea pig retina. Vis. Neurosci. 2000, 17:63-70.
40. Fukuhara C., Dirden J.C., Tosini G. Photic regulation of melatonin in rat retina and the role of proteasomal proteolysis. Neuroreport 2001, 12:3833-3837.
41. Fukuhara C., Liu C., Ivanova T.N., Chan G.C.-K., Storm D.R., Iuvone P.M., Tosini G. Gating of the cAMP signaling cascade and melatonin synthesis by the circadian clock in mammalian retina. J. Neurosci. 2004, 24:1803-1811.
42. Gagne A.M., Danilenko K.V., Rosolen S.G., Herbert M. Impact of oral melatonin on the electroretinogram. J. Circadian Rhythms 2009, 7:14.
43. Ganguly S., Gastel J.A., Weller J.L., Schwartz C., Jaffe H., Namboodiri M.A., Coon S.L., Hickman A.B., Rollag M., Obsil T., Beauverger P., Ferry G., Boutin J.A., Klein D.C. Role of a pineal cAMP-operated arylalkylamine N-acetyltransferase/14-3-3-binding switch in melatonin synthesis. Proc. Natl. Acad. Sci. U S A 2001, 98:8083-8088.
44. Garbarino-Pico E., Carpentieri A.R., Contin M.A., Sarmiento M.I., Brocco M.A., Panzetta P., Rosenstein R.E., Caputto B.L., Guido M.E. Retinal ganglion cells are autonomous circadian oscillators synthesizing N-acetylserotonin during the day. J. Biol. Chem. 2004, 279:51172-51181.
45. Goto M., Oshima I., Tomita T., Ebihara S. Melatonin content of the pineal gland in different mouse strains. J. Pineal Res. 1989, 7:195-204.
46. Grace M.S., Cahill G.M., Besharse J.C. Melatonin deacetylation: retinal vertebrate class distribution and Xenopus laevis tissue distribution. Brain Res. 1991, 559:56-63.
47. Grace M.S., Wang L.M., Pickard G.E., Besharse J.C., Menaker M. The tau mutation shortens the period of rhythmic photoreceptor outer segment disk shedding in the hamster. Brain Res. 1996, 735:93-100.
48. Grace M.S., Chiba A., Menaker M. Circadian control of photoreceptor outer segment membrane turnover in mice genetically incapable of melatonin synthesis. Vis. Neurosci. 1999, 16:909-918.
49. Green C.B., Besharse J.C. Tryptophan hydroxylase expression is regulated by a circadian clock in Xenopus laevis retina. J. Neurochem. 1994, 62:2420-2428.
50. Green C.B., Besharse J.C. Retinal circadian clocks and control of retinal physiology. J. Biol. Rhythms 2004, 19:91-102.
51. Green C.B., Cahill G.M., Besharse J.C. Regulation of tryptophan hydroxylase expression by a retinal circadian oscillator in vitro. Brain Res. 1995, 677:283-290.
52. 2+ dependent lipid peroxidation of rod outer segment membranes of bovine retina. J. Pineal Res. 2003, 35:276-282.
53. Hamm H.E., Takahashi J.S., Menaker M. Light-induced decrease of serotonin N-acetyltransferase activity and melatonin in the chicken pineal gland and retina. Brain Res. 1983, 266:287-293.
54. Haque R., Ali F.G., Biscoglia R., Abey J., Weller J., Klein D., Iuvone P.M. CLOCK and NPAS2 have overlapping roles in the circadian oscillation of arylalkylamine N-acetyltransferase mRNA in chicken cone photoreceptors. J. Neurochem. 2010, 113:1296-1306.
55. Haque R., Chong N.W., Ali F., Chaurasia S.S., Sengupta T., Chun E., Howell J.C., Klein D.C., Iuvone P.M. Melatonin synthesis in retina: cAMP-dependent transcriptional regulation of chicken arylalkylamine N-acetyltransferase by a CRE-like sequence and a TTATT repeat motif in the proximal promoter. J. Neurochem. 2011, 119:6-17.
56. Hasegawa M., Cahill G.M. A role for cyclic AMP in entrainment of the circadian oscillator in Xenopus retinal photoreceptors by dopamine but not by light. J. Neurochem. 1999, 72:1812-1820.
57. Hsu L.L. Brain aryl acylamidase. Int. J. Biochem. 1982, 14:1037-1042.
58. Huang H., Lee S.C., Yang X.L. Modulation by melatonin of glutamatergic synaptic transmission in the carp retina. J. Physiol. 2005, 569:857-871.
59. Iigo M., Sánchez-Vázquez F.J., Madrid J.A., Zamora S., Tabata M. Unusual responses to light and darkness of ocular melatonin in European sea bass. Neuroreport 1997, 8:1631-1635.
60. Ismail S.A., Mowafi H.A. Melatonin provides anxiolysis, enhances analgesia, decreases intraocular pressure, and promotes better operating conditions during cataract surgery under topical anesthesia. Anesth. Analg. 2009, 108:1146-1151.
61. Iuvone P.M., Chong N.W., Bernard M., Brown A.D., Thomas K.B., Klein D.C. Melatonin biosynthesis in chicken retina. Regulation of tryptophan hydroxylase and arylalkylamine N-acetyltransferase. Adv. Exp. Med. Biol. 1999, 460:31-41.
62. Iuvone P.M., Brown A.D., Haque R., Weller J., Zawilska J.B., Chaurasia S.S., Ma M., Klein D.C. Retinal melatonin production: role of proteasomal proteolysis in circadian and photic control of arylalkylamine N-acetyltransferase. Invest. Ophthalmol. Vis. Sci. 2002, 43:564-572.
63. Iuvone P.M., Tosini G., Haque R., Klein D.C., Chaurasia S.S. Circadian clocks, clock-controlled genes and melatonin biosynthesis in the retina. Prog. Retin. Eye Res. 2005, 24:433-456.
64. Ivanova T.N., Iuvone P.M. Circadian rhythm and photic control of cAMP level in chick retinal cell cultures: a mechanism for coupling the circadian oscillator to the melatonin-synthesizing enzyme, arylalkylamine N-acetyltransferase, in photoreceptor cells. Brain Res. 2003, 991:96-103.
65. Ivanova T.N., Alonso-Gomez A.L., Iuvone P.M. Dopamine D4 receptors regulate intracellular calcium concentration in cultured chicken cone photoreceptor cells: relationship to dopamine receptor-mediated inhibition of cAMP formation. Brain Res. 2008, 1207:111-119.
66. Jang S.-W., Liu X., Pradoldej S., Tosini G., Chang Q., Iuvone P.M., Ye K. N-acetylserotonin activates TrkB receptor in a circadian rhythm. Proc. Natl. Acad. Sci. U S A 2010, 107:3876-3881.
67. Jockers R., Maurice P., Boutin J.A., Delagrange P. Melatonin receptors, heterodimerization, signal transduction and binding sites: what's new?. Br. J. Pharmacol. 2008, 154:1182-1195.
68. Klein D.C. The 2004 Aschoff/Pittendrigh lecture: theory of the origin of the pineal gland-a tale of conflict and resolution. J. Biol. Rhythms 2004, 19:264-279.
69. Klein D.C., Coon S.L., Roseboom P.H., Weller J.L., Bernard M., Gastel J.A., Zatz M., Iuvone P.M., Rodriguez I.R., Bégay V., Falcón J., Cahill G.M., Cassone V.M., Baler R. The melatonin rhythm-generating enzyme: molecular regulation of serotonin N-acetyltransferase in the pineal gland. Recent Prog. Horm. Res. 1997, 52:307-357.
70. La Vail M.M. Rod outer segment disk shedding in the rat retina: relationship to cyclic lighting. Science 1976, 194:1071-1073.
71. Leino M. 6-Methoxy-tetrahydro-beta-carboline and melatonin in the human retina. Exp. Eye Res. 1984, 38:325-330.
72. Li P., Pang S.F., Tsang C.W. Retinal 5-methoxytryptamine and 5-methoxyindole-3-acetic acid in the rat and quail: diurnal rhythms and interspecies differences. Biochem. Biophys. Res. Commun. 1997, 239:353-356.
73. Li C., Shi Y., You L., Wang L., Chen Z.J. Melatonin receptor 1A gene polymorphism associated with polycystic ovary syndrome. Gynecol. Obstet. Invest. 2011, 72:130-134.
74. Liang F.Q., Aleman T.S., Zaixin Y., Cideciyan A.V., Jacobson S.G., Bennett J. Melatonin delays photoreceptor degeneration in the rds/rds mouse. Neuroreport 2001, 12:1011-1014.
75. Liang F.Q., Green L., Wang C., Alssadi R., Godley B.F. Melatonin protects human retinal pigment epithelial (RPE) cells against oxidative stress. Exp. Eye Res. 2004, 78:1069-1075.
76. Liang J., Wessel J.H., Iuvone P.M., Tosini G., Fukuhara C. Diurnal rhythms of tryptophan hydroxylase 1 and 2 mRNA expression in the rat retina. Neuroreport 2004, 15:1497-5100.
77. Liu C., Fukuhara C., Wessel J.H., Iuvone P.M., Tosini G. Localization of Aa-nat mRNA in the rat retina by fluorescence in situ hybridization and laser capture microdissection. Cell. Tissue Res. 2004, 315:197-201.
78. Lu J., Zoran M.J., Cassone V.M. Daily and circadian variation in the electroretinogram of the domestic fowl: effects of melatonin. J. Comp. Physiol. A. 1995, 177:299-306.
79. Lundmark P.O., Pandi-Perumal S.R., Srinivasan V., Cardinali D.P., Rosenstein R.E. Melatonin in the eye: implications for glaucoma. Exp. Eye Res. 2007, 84:1021-1030.
80. Marchiafava P.L., Longoni B. Melatonin as an antioxidant in retinal photoreceptors. J. Pineal Res. 1999, 26:184-189.
81. McGoogan J.M., Cassone V.M. Circadian regulation of chick electroretinogram: effects of pinealectomy and exogenous melatonin. Am. J. Phys. 1999, 277:R1418-R1427.
82. Menaker M., Moreira L.F., Tosini G. The Evolution of vertebrate circadian organization. Braz. J. Med. Biol. Res. 1997, 30:305-313.
83. Meyer P., Pache M., Loeffler K.U., Brydon L., Jockers R., Flammer J., Wirz-Justice A., Savaskan E. Melatonin MT-1-receptor immunoreactivity in the human eye. Br. J. Ophthalmol. 2002, 86:1053-1057.
84. Nguyen-Legros J., Chanut E., Versaux-Botteri C., Simon A., Trouvin J.H. Dopamine inhibits melatonin synthesis in photoreceptor cells through a D2-like receptor subtype in the rat retina: biochemical and histochemical evidence. J. Neurochem. 1996, 67:2514-2520.
85. Nir I., Haque R., Iuvone P.M. Diurnal metabolism of dopamine in dystrophic retinas of homozygous and heterozygous retinal degeneration slow (rds) mice. Brain Res. 2000, 884:13-22.
86. Nir I., Harrison J.M., Haque R., Low M.J., Grandy D.K., Rubinstein M., Iuvone P.M. Dysfunctional light-evoked regulation of cAMP in photoreceptors and abnormal retinal adaptation in mice lacking dopamine D4 receptors. J. Neurosci. 2002, 22:2063-2273.
87. Nowak J.Z., Zurawska E., Zawilska J. Melatonin and its generating system in vertebrate retina: circadian rhythm, effect of environmental lighting and interaction with dopamine. Neurochem. Int. 1989, 14:397-406.
88. Obsil T., Ghirlando R., Klein D.C., Ganguly S., Dyda F. Crystal structure of the 14-3-3zeta: serotonin N-acetyltransferase complex. A role for scaffolding in enzyme regulation. Cell 2001, 105:257-267.
89. Organisciak D.T., Darrow R.M., Barsalou L., Kutty R.K., Wiggert B. Circadian-dependent retinal light damage in rats. Invest. Ophthalmol. Vis. Sci. 2000, 41:3694-3701.
90. Orr H.T., Lowry O.H., Cohen A.I., Ferrendelli J.A. Distribution of 3':5'-cyclic AMP and 3':5'-cyclic GMP in rabbit retina in vivo: selective effects of dark and light adaptation and ischemia. Proc. Natl. Acad. Sci. U S A 1976, 73:4442-4445.
91. Osborne N.N., Chidlow G. The presence of functional melatonin receptors in the iris-ciliary processes of the rabbit eye. Exp. Eye Res. 1994, 59:3-9.
92. Osborne N.N., Nash M.S., Wood J.P. Melatonin counteracts ischemia-induced apoptosis in human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 1998, 39:2374-2383.
93. Ping Y., Huang H., Zhang X.J., Yang X.L. Melatonin potentiates rod signals to ON type bipolar cells in fish retina. J. Physiol. 2008, 586:2683-2694.
94. Pintor J., Martin L., Pelaez T., Hoyle C.H., Peral A. Involvement of melatonin MT(3) receptors in the regulation of intraocular pressure in rabbits. Eur. J. Pharmacol. 2001, 416:251-254.
95. 3 receptor. Br. J. Pharmacol. 2003, 138:831-836.
96. Pozdeyev N., Taylor C., Haque R., Chaurasia S.S., Visser A., Thazyeen A., Du Y., Fu H., Weller J., Klein D.C., Iuvone P.M. Photic regulation of arylalkylamine N-acetyltransferase binding to 14-3-3 proteins in retinal photoreceptor cells. J. Neurosci. 2006, 26:9153-9161.
97. Pozdeyev N.K., Tosini G., Ali F., Rozov S., Lee R.H., Iuvone P.M. Dopamine modulates diurnal and circadian rhythms of protein phosphorylation in photoreceptor cells of mouse retina. Eur. J. Neurosci. 2008, 27:26691-26700.
98. Pulido O., Clifford J. Age-associated changes in the circadian rhythm of retinal N-acetylserotonin and melatonin in rats with pigmented eyes. Exp. Gerontol. 1986, 21:23-30.
99. Reiter R.J., Paredes S.D., Manchester L.C., Tan D.X. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit. Rev. Biochem. Mol. Biol. 2009, 44:175-200.
100. Reppert S.M. Melatonin receptors: molecular biology of a new family of G-protein-coupled receptors. J. Biol. Rhythms 1997, 12:528-531.
101. Reppert S.M., Godson C., Mahle C.D., Weaver D.R., Slaugenhaupt S.A., Gusella J.F. Molecular characterization of a second melatonin receptor expressed in human retina and brain: the Mel1b melatonin receptor. Proc. Natl. Acad. Sci. U S A 1995, 92:8734-8738.
102. Ribelayga C., Wang Y., Mangel S.C. A circadian clock in the fish retina regulates dopamine release via activation of melatonin receptors. J. Physiol. 2004, 554:467-482.
103. Ribelayga C., Wang Y., Mangel S.C. Dopamine mediates circadian clock regulation of rod and cone input to fish retinal horizontal cells. J. Physiol. 2004, 544:801-816.
104. Rodriguez I.R., Mazuruk K., Schoen T.J., Chader G.J. Structural analysis of the human hydroxyindole-O-methyltransferase gene. Presence of two distinct promoters. J. Biol. Chem. 1994, 269:31969-31977.
105. Rogawski M.A., Roth R.H., Aghajanian G.K. Melatonin: deacetylation to 5-methoxytryptamine by liver but not brain aryl acylamidase. J. Neurochem. 1979, 32:1219-1226.
106. Rosen R., Hu D.N., Perez V., Tai K., Yu G.P., Chen M., Tone P., McCormick S.A., Walsh J. Urinary 6-sulfatoxymelatonin level in age-related macular degeneration patients. Mol. Vis. 2009, 15:1673-1679.
107. Rufiange M., Dumont M., Lachappelle P. Correlating retinal function with melatonin secretion in subject with an early or late circadian phase. Invest. Ophthalmol. Vis. Sci. 2002, 43:2491-2499.
108. Sakamoto K., Oishi K., Shiraishi M., Hamano S., Otsuka H., Miyake Y., Ishida N. Two circadian oscillatory mechanisms in the mammalian retina. Neuroreport 2000, 11:3995-3997.
109. Sakamoto K., Liu C., Tosini G. Circadian rhythms in the retina of rats with photoreceptor degeneration. J. Neurochem. 2004, 90:1019-1024.
110. Sakamoto K., Liu C., Kasamatsu M., Iuvone P.M., Tosini G. Intraocular injection of kainic acid does not abolish the circadian rhythm of arylalkylamine N-acetyltransferase mRNA in rat photoreceptors. Mol. Vis. 2006, 12:117-124.
111. Samples J.R., Krause G., Lewy A.J. Effect of melatonin on intraocular pressure. Curr. Eye Res. 1988, 7:649-653.
112. Savaskan E., Wirz-Justice A., Olivieri G., Pache M., Kräuchi K., Brydon L., Jockers R., Müller-Spahn F., Meyer P. Distribution of melatonin MT1 receptor immunoreactivity in human retina. J. Histochem. Cytochem. 2002, 50:519-526.
113. Savaskan E., Jockers R., Ayoub M., Angeloni D., Fraschini F., Flammer J., Eckert A., Müller-Spahn F., Meyer P. The MT2 melatonin receptor subtype is present in human retina and decreases in Alzheimer's disease. Curr. Alzheimer Res. 2007, 4:47-51.
114. Scher J., Wankiewicz E., Brown G.M., Fujieda H. MT1 melatonin receptor in the human retina: expression and localization. Invest. Ophthalmol. Vis. Sci. 2002, 43:889-897.
115. Schmid-Kubista K.E., Glittenberg C.G., Cezanne M., Holzmann K., Neumaier-Ammerer B., Binder S. Daytime levels of melatonin in patients with age-related macular degeneration. Acta Ophthalmol. 2009, 87:89-93.
116. Sengupta A., Baba K., Mazzoni F., Pozdeyev N.V., Strettoi E., Iuvone P.M., Tosini G. Localization of melatonin receptor 1 in mouse retina and its role in the circadian regulation of the electroretinogram and dopamine levels. PLoS One 2011, 6:e24483.
117. 3 receptor agonist, on intraocular pressure in glaucomatous monkey eyes. J. Glaucoma 2004, 13:385-388.
118. Siu A.W., Reiter R.J., To C.H. Pineal indoleamines and vitamin E reduce nitric oxide-induced lipid peroxidation in rat retinal homogenates. J. Pineal. Res. 1999, 27:122-128.
119. Steenhard B.M., Besharse J.C. Phase shifting the retinal circadian clock: xPer2 mRNA induction by light and dopamine. J. Neurosci. 2000, 20:8572-8577.
120. Sugawara T., Sieving P.A., luvone P.M., Bush R.A. The melatonin antagonist luzindole protects retinal photoreceptors from light damage in the rat. Invest. Ophthalmol. Vis. Sci. 1998, 39:2458-2465.
121. Teirstein P.S., Goldman A.I., O'Brien P.J. Evidence for both local and central regulation of rat rod outer segment disc shedding. Invest. Ophthalmol. Vis. Sci. 1980, 19:1268-1273.
122. Terman J.S., Remé C.E., Wirz-Justice A. Rod outer segment disk shedding in rats with lesions of the suprachiasmatic nucleus. Brain Res. 1993, 605:256-264.
123. Thomas K.B., Iuvone P.M. Circadian rhythm of tryptophan hydroxylase activity in chicken retina. Cell. Mol. Neurobiol. 1991, 11:511-527.
124. Thomas K.B., Tigges M., Iuvone P.M. Melatonin synthesis and circadian tryptophan hydroxylase activity in chicken retina following destruction of serotonin immunoreactive amacrine and bipolar cells by kainic acid. Brain Res. 1993, 601:303-307.
125. Tosini G., Dirden J.C. Dopamine inhibits melatonin release in the mammalian retina: in vitro evidence. Neurosci. Lett. 2000, 286:119-122.
126. Tosini G., Menaker M. Circadian rhythms in cultured mammalian retina. Science 1996, 272:419-421.
127. Tosini G., Menaker M. The clock in the mouse retina: melatonin synthesis and photoreceptor degeneration. Brain Res. 1998, 789:221-228.
128. Tosini G., Chaurasia S.S., Iuvone P.M. Regulation of AANAT in the retina. Chronobiol. Int. 2006, 23:381-391.
129. Tosini G., Davidson A.J., Fukuhara C., Kasamatsu M., Castanon-Cervantes O. Localization of a circadian clock in mammalian photoreceptors. FASEB J. 2007, 21:3866-3871.
130. Tosini G., Pozdeyev N., Sakamoto K., Iuvone P.M. The circadian clock system in mammalian retina. BioEssays 2008, 30:624-633.
131. Tosini, G., Ye, K., Iuvone, P.M. N-acetylserotonin: neuroprotection, neurogenesis, and the sleepy brain. Neuroscientist, http://dx.doi.org/10.1177/1073858412446634.
132. Underwood H., Binkley S., Siopes T., Mosher K. Melatonin rhythms in the eyes, pineal bodies, and blood of Japanese quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol. 1984, 56:70-81.
133. Valenciano A.I., Alonso-Gómez A.L., Iuvone P.M. Diurnal rhythms of tryptophan hydroxylase activity in Xenopus laevis retina: opposing phases in photoreceptors and inner retinal neurons. Neuroreport 1999, 10:2131-2135.
134. Vaughan D.K., Nemke J.L., Fliesler S.J., Darrow R.M., Organisciak D.T. Evidence for a circadian rhythm of susceptibility to retinal light damage. Photochem. Photobiol. 2002, 75:547-553.
135. Von Gall C., Garabette M.L., Kell C.A., Frenzel S., Dehghani F., Schumm-Draeger P.M., Weaver D.R., Korf H.-W., Hastings M.H., Stehle J.H. Rhythmic gene expression in pituitary depends on heterologous sensitization by the neurohormone melatonin. Nat. Neurosci. 2002, 5:234-238.
136. White M.P., Fisher L.J. Effects of exogenous melatonin on circadian disc shedding in the albino rat retina. Vis. Res. 1989, 29:167-179.
137. Wiechmann A.F., O'Steen W.K. Melatonin increases photoreceptor susceptibility to light-induced damage. Invest. Ophthalmol. Vis. Sci. 1992, 33:1894-1902.
138. Wiechmann A.F., Summers J.A. Circadian rhythms in the eye: the physiological significance of melatonin receptors in ocular tissues. Prog. Retin. Eye Res. 2008, 27:137-160.
139. Wiechmann A.F., Wirsig-Wiechmann C.R. Melatonin receptor mRNA and protein expression in Xenopus laevis nonpigmented ciliary epithelial cells. Exp. Eye Res. 2001, 73:617-623.
140. Wiechmann A.F., Yang X.L., Wu S.M., Hollyfield J.G. Melatonin enhances horizontal cell sensitivity in salamander retina. Brain Res. 1988, 453:377-380.
141. Wiechmann A.F., Vrieze M.J., Dighe R., Hu Y. Direct modulation of rod photoreceptor responsiveness through a Mel(1c) melatonin receptor in transgenic Xenopus laevis retina. Invest. Ophthalmol. Vis. Sci. 2003, 44:4522-4531.
142. Yi C., Pan X., Yan H., Guo M., Pierpaoli W. Effects of melatonin in age-related macular degeneration. Ann. N. Y. Acad. Sci. 2005, 1057:384-392.
143. Yuan H., Lu Y., Pang S.F. Binding characteristics and regional distribution of [125I]iodomelatonin binding sites in the brain of the human fetus. Neurosci. Lett. 1991, 130:229-232.
144. Zawilska J.B., Iuvone P.M. Melatonin synthesis in chicken retina: effect of kainic acid-induced lesions on the diurnal rhythm and D2-dopamine receptor-mediated regulation of serotonin N-acetyltransferase activity. Neurosci. Lett. 1992, 135:71-74.
145. Zawilska J.B., Derbiszewska T., Nowak J.Z. Clozapine and other neuroleptic drugs antagonize the light-evoked suppression of melatonin biosynthesis in chick retina: involvement of the D4-like dopamine receptor. J. Neural Transm. Gen. Sect. 1994, 97:107-117.