Circadian rhythmicity in dopamine content of mammalian retina: role of the photoreceptors

Doyle, Susan E.; McIvor, Wilson; Menaker, Michael

doi:10.1046/j.1471-4159.2002.01149.x

Cited by 102 publications

(92 citation statements)

References 49 publications

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“…In rat retinas, dopamine release is lowest at night and highest during the day, even in constant darkness and in animals without photoreceptors, adult RCS/N-rdy rats homozygous for the rdy (retinal dystrophy) allele of photoreceptors (Doyle et al, 2002b). These rhythms might be maintained by melatonin release from the pineal gland (Doyle et al, 2002a) or by endogenous oscillations in the dopaminergic amacrine cells themselves (Gustincich et al, 2004;Witkovsky, 2004), but histaminergic retinopetal axons, which remained intact in these experiments, might also play an important role.…”

Section: Hr1 In Rat Retinasmentioning

confidence: 99%

Histamine receptors in mammalian retinas

Gastinger

Barber

Vardi

et al. 2006

J of Comparative Neurology

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Mammalian retinas are innervated by histaminergic axons that originate from perikarya in the posterior hypothalamus. To identify the targets of these retinopetal axons, we localized histamine receptors (HR) in monkey and rat retinas by light and electron microscopy. In monkeys, puncta containing HR3 were found at the tips of ON-bipolar cell dendrites in cone pedicles and rod spherules, closer to the photoreceptors than the other neurotransmitter receptors. This is the first ultrastructural localization of any histamine receptor and the first direct evidence that HR3 is present on postsynaptic membranes in the central nervous system. In rat retinas, most HR1 were localized to dopaminergic amacrine cells. The differences in histamine receptor localization may reflect the differences in the activity patterns of the two species. Indexing termsretinopetal; centrifugal; bipolar; amacrine; primate; dopamine Vertebrate retinas receive input from the brain via retinopetal axons, and this pathway has important modulatory effects on retinal neurons in birds and fish, the groups that have been studied most intensively. The functions of retinopetal axons in mammalian retinas are not well understood, however (Uchiyama, 1989). Histamine has been localized to retinopetal axons in the guinea pig (Airaksinen and Panula, 1988), monkey (Gastinger et al., 1999), and rat (Gastinger et al., 2001) retinas. These axons originate from perikarya in the tuberomammillary nucleus of the posterior hypothalamus (Manning et al., 1996;Panula et al., 1989). Mast cells, another possible source of histamine, are not present in the retina (Smelser and Silver, 1963). With the identification of the neurotransmitter of these retinopetal axons, it is now possible to predict how these inputs contribute to information processing in mammalian retinas.These retinopetal axons are expected to be active at night in rats and during the day in monkeys. Histaminergic neurons play an important role in the ascending arousal system (Saper et al., 2001), firing at a steady rate during waking and becoming silent during sleep (Steininger et al., 1999;Vanni-Mercier et al., 2003). In rats, a nocturnal species, histaminergic neurons are most active at night, and the rate of histamine release in the posterior hypothalamus is higher at night than during the day (Prast et al., 1992). In macaques, a diurnal species, levels of histamine metabolites in the third ventricular cerebral spinal fluid are higher during the day than at night (Prell et al., 1989).In the central nervous system, histamine acts on three types of G-protein-coupled receptors: histamine receptor 1 (HR1), histamine receptor 2 (HR2) and histamine receptor 3 (HR3). Among these, only HR1 has been characterized previously in mammalian retinas (Nowak, 1993;Sawai et al., 1988). However, there is indirect evidence that HR2 and HR3 are also present in mammalian retinas. Histamine inhibits a forskolin-induced increase in cAMP in the rabbit retina via HR2 (Nowak, 1991;Nowak et al., 1989). Histamine also increa...

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Section: Hr1 In Rat Retinasmentioning

confidence: 99%

Histamine receptors in mammalian retinas

Gastinger

Barber

Vardi

et al. 2006

J of Comparative Neurology

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“…In that regard it may be significant that the tyrosine hydroxylase-positive neurons have a circadian rhythm of dopamine production (Doyle et al, 2002a), a rhythm that persists in dystrophic rats showing severe photoreceptor degeneration. Melatonin is known to play an important role in the release of dopamine, and Niki et al (1998) provided evidence that in the rat retina AA-NAT, the ratelimiting enzyme for melatonin synthesis, was found in the photoreceptor layer.…”

Section: Biological Clock Genes In the Retinamentioning

confidence: 99%

“…Melatonin is known to play an important role in the release of dopamine, and Niki et al (1998) provided evidence that in the rat retina AA-NAT, the ratelimiting enzyme for melatonin synthesis, was found in the photoreceptor layer. Doyle et al (2002a) have used these data to argue that photoreceptors influence the amount of dopamine, but not the rhythm of its synthesis. On the other hand, retinal dopamine rhythms are blunted in a mouse strain lacking melatonin, suggesting a possible interdependence of dopamine and melatonin rhythms (Doyle et al, 2002b).…”

Section: Biological Clock Genes In the Retinamentioning

confidence: 99%

Cellular Location and Circadian Rhythm of Expression of the Biological Clock GenePeriod 1in the Mouse Retina

et al. 2003

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The cellular location and rhythmic expression of Period 1 (Per1) circadian clock gene were examined in the retina of a Per1::GFP transgenic mouse. Mouse Per1 (mPer1) RNA was localized to inner nuclear and ganglion cell layers but was absent in the outer nuclear (photoreceptor) layer. Green fluorescent protein (GFP), which was shown to colocalize with PER1 protein, was found in a few subtypes of amacrine neuron, including those containing tyrosine hydroxylase, calbindin, and calretinin, but not in cholinergic amacrine cells. A small subset of ganglion cells also contained GFP immunoreactivity (GFP-IR), but the melanopsin-containing subtype, which projects to the suprachiasmatic nuclei (SCN), lacked GFP-IR. Although the intensity of GFP-IR varied among the populations of amacrine cells at each time point that was examined, both diurnal and circadian rhythms were found for the fraction of neurons showing strong GFP-IR, with peak expression between Zeitgeber/circadian (ZT/CT) times 10 and 14. In SCNs that were examined in the same mice used for the retinal measures, the peak in GFP-IR also occurred at approximately ZT/CT 10. Our results are the first to demonstrate a circadian rhythm of a biological clock component in identified neurons of a mammalian retina.

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“…T he mammalian retinal circadian clock exerts extensive control over retinal physiology and function, regulating a wide variety of retinal circadian rhythms, including rod disk shedding (1)(2)(3), melatonin release (4-6), dopamine synthesis (7,8), electroretinogram (ERG) b-wave amplitude (9), extracellular pH (10), visual sensitivity (11,12), and intraocular pressure (13,14). The retinal circadian clock and its dopamine-and melatonin-signaling molecules also influence pathological processes in the eye, including the susceptibility of photoreceptors to degeneration from light damage (15,16), photoreceptor survival in animal models of retinal degeneration (17), and the degree of refractive errors in primate models of myopia (18).…”

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confidence: 99%

Circadian organization of the mammalian retina

Ruan

Zhang

Zhou

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

148

185

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The mammalian retina contains an endogenous circadian pacemaker that broadly regulates retinal physiology and function, yet the cellular origin and organization of the mammalian retinal circadian clock remains unclear. Circadian clock neurons generate daily rhythms via cell-autonomous autoregulatory clock gene networks, and, thus, to localize circadian clock neurons within the mammalian retina, we have studied the cell type-specific expression of six core circadian clock genes in individual, identified mouse retinal neurons, as well as characterized the clock gene expression rhythms in photoreceptor degenerate rd mouse retinas. Individual photoreceptors, horizontal, bipolar, dopaminergic (DA) amacrines, catecholaminergic (CA) amacrines, and ganglion neurons were identified either by morphology or by a tyrosine hydroxylase (TH) promoter-driven red fluorescent protein (RFP) fluorescent reporter. Cells were collected, and their transcriptomes were subjected to multiplex single-cell RT-PCR for the core clock genes Period (Per) 1 and 2, Cryptochrome (Cry) 1 and 2, Clock, and Bmal1. Individual horizontal, bipolar, DA, CA, and ganglion neurons, but not photoreceptors, were found to coordinately express all six core clock genes, with the lowest proportion of putative clock cells in photoreceptors (0%) and the highest proportion in DA neurons (30%). In addition, clock gene rhythms were found to persist for >25 days in isolated, cultured rd mouse retinas in which photoreceptors had degenerated. Our results indicate that multiple types of retinal neurons are potential circadian clock neurons that express key elements of the circadian autoregulatory gene network and that the inner nuclear and ganglion cell layers of the mammalian retina contain functionally autonomous circadian clocks.circadian clock ͉ clock gene ͉ mouse retina ͉ photoreceptor ͉ real-time PCR T he mammalian retinal circadian clock exerts extensive control over retinal physiology and function, regulating a wide variety of retinal circadian rhythms, including rod disk shedding (1-3), melatonin release (4-6), dopamine synthesis (7, 8), electroretinogram (ERG) b-wave amplitude (9), extracellular pH (10), visual sensitivity (11, 12), and intraocular pressure (13,14). The retinal circadian clock and its dopamine-and melatonin-signaling molecules also influence pathological processes in the eye, including the susceptibility of photoreceptors to degeneration from light damage (15, 16), photoreceptor survival in animal models of retinal degeneration (17), and the degree of refractive errors in primate models of myopia (18). Despite its widespread influence, the cellular origin and organization of the circadian clock in the mammalian retina remain unclear.Neural circadian clocks generate endogenous circadian rhythms through cell-autonomous autoregulatory transcriptiontranslation feedback loops comprised of a defined set of ''clock genes'' in subsets of circadian pacemaker neurons. Gene targeting has demonstrated that, in mammals, the genes Period (Per) 1 and 2 and Cr...

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Circadian rhythmicity in dopamine content of mammalian retina: role of the photoreceptors

Cited by 102 publications

References 49 publications

Histamine receptors in mammalian retinas

Histamine receptors in mammalian retinas

Cellular Location and Circadian Rhythm of Expression of the Biological Clock GenePeriod 1in the Mouse Retina

Circadian organization of the mammalian retina

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