Circadian regulation of lodopsin gene expression in embryonic photoreceptors in retinal cell culture

Pierce, Mary E.; Sheshberadaran, Hooshmand; Zhang, Zhang Zhe; Fox, Lyle E.; Applebury, Meredithe L.; Takahashi, Joseph S.

doi:10.1016/0896-6273(93)90161-j

Cited by 161 publications

(131 citation statements)

References 25 publications

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“…Diurnal and circadian rhythms are cyclic processes that occur with a 24-h periodicity; diurnal rhythms depend on light while circadian rhythms persist in the absence of light. Previous work has demonstrated that circadian rhythms can be generated within photoreceptors (Cahill and Besharse 1993;Pierce et al 1993), and regulated by neurotransmitters such as dopamine (McCormack and Burnside 1992). In addition, dopamine can (a) Northern blots with 2.5 lg of total retinal RNA showed two major opsin mRNA bands, opsin I (6.4 kb) and opsin II (2.1 kb), as described previously .…”

Section: Discussionsupporting

confidence: 70%

Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Alfinito

Alli

Townes‐Anderson

2002

Journal of Neurochemistry

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The neuromodulator adenosine mediates dark-adaptive changes in retinal photoreceptors through A 2a receptors. In cold-blooded vertebrates, opsin mRNA expression is lower at night than during the day. In the present study, we tested whether adenosine could inhibit opsin mRNA expression in cultured rod cells and if endogenous adenosine acts to suppress opsin mRNA in the intact retina at night. Semi-quantitative in situ hybridization showed that treatment with 100 nM of the A 2a /A 2b agonist N 6 -[2-(3,5-dimethoxyphenyl)-2-(2-methylphenyl)-ethyl]adenosine (DPMA) reduced opsin mRNA 41% in cultured rod cells. The effect of DPMA was blocked by 10 lM of the A 2a antagonist 8-(3-chlorostyryl)caffeine (CSC) but not by 10 lM of the A 2b antagonist alloxazine. One micromolar adenosine alone had no effect on opsin mRNA.However, in the presence of the adenosine deaminase inhibitor erythro-9-(2-hydroxy-3-nonyl)adenine hydrochloride (EHNA), 1 lM adenosine reduced opsin mRNA 61%. EHNA alone reduced opsin mRNA by 26%. Consistent with an A 2a receptor mechanism, 100 nM forskolin (adenylate cyclase agonist) decreased opsin mRNA 34%. Finally, northern blots showed that intravitreal injection of 10 lM CSC at night increased opsin I mRNA 38%. Thus, endogenous adenosine suppresses rod opsin I mRNA expression at night; in vitro results indicate this reduction occurs through A 2a -like receptor binding and stimulation of adenylate cyclase activity. Keywords: A 2a receptor, adenosine, mRNA expression, opsin, retina, rod photoreceptor. The rod visual pigment, rhodopsin, is composed of the chromophore 11-cis-retinal and the integral membrane glycoprotein opsin. Absorption of light by rhodopsin initiates vision through a G-protein linked signal transduction cascade which ultimately inhibits neurotransmitter release. While the importance of opsin to rod cell function has been well established, its importance to rod cell survival has only recently been uncovered. Studies using transgenic and knockout mice have shown that single point mutations in the opsin gene as well as overexpression or deletion of normal opsin can result in rod cell death and retinal degenerative disease (Dryja et al. 1991;Olsson et al. 1992;Li et al. 1996;Humphries et al. 1997;Lem et al. 1999). Therefore, understanding the mechanisms that regulate opsin gene expression is critical to our knowledge of rod cell biology and to the development of strategies for treating retinal disease.Previous reports have provided details of the rod opsin promoter and have demonstrated its activation by the transacting factors Nrl and Crx (Ahmad 1995;Chen and Zack 1996;Rehemtulla et al. 1996;Chen et al. 1997). Other studies have shown that rod opsin mRNA exhibits rhythmic Abbreviations used: AP, alkaline phosphatase; BCIP, 5-bromo-4-chloro-3-indolyl phosphate; CSC, 8-(3-chlorostyryl)caffeine; DABCO, 1,4-diazabicyclo[2.2.2]octane; DMSO, dimethylsulfoxide; DPMA, N 6 -[2-(3,5-dimethoxyphenyl)-2-(2-methylphenyl)-ethyl]adenosine; EHNA, erythro-9-(2-hydroxy-3-nonyl)adenine hydrochloride...

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Section: Discussionsupporting

confidence: 70%

Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Alfinito

Alli

Townes‐Anderson

2002

Journal of Neurochemistry

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“…photoreceptor cells (rods and cones), bipolar cells, ganglion cells, amacrine cells, and horizontal cells, have been extensively characterized [4]. From the view point of circadian biology, a wealth of data exist on cellular, molecular, and system level retinal events that are regulated by local circadian clocks, such as the rhythms in rod disc shedding [5], melatonin release [6], dopamine synthesis [7], electroretinogram b-wave amplitude [8], extracellular pH [9], phototransduction events including iodopsin expression [10] and cGMP-gated channel sensitivity [11,12], and intraocular pressure [13,14]. Many of these rhythms are thought to allow the retina to anticipate day-night variation and to detect light signals even in the dynamic variation of light intensity over 6-log units between day and night.…”

Section: Introductionmentioning

confidence: 99%

Circadian proteomics of the mouse retina

et al. 2007

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The circadian clock in the retina regulates a variety of physiological phenomena such as disc shedding and melatonin release. Although these events are critical for retinal functions, it is almost unknown how the circadian clock controls the physiological rhythmicity. To gain insight into the processes, we performed a proteomic analysis using 2-DE to find proteins whose levels show circadian changes. Among 415 retinal protein spots, 11 protein spots showed circadian rhythmicity in their intensities. We performed MALDI-TOF MS and NanoLC-MS/MS analyses and identified proteins contained in the 11 spots. The proteins were related to vesicular transport, calcium-binding, protein degradation, metabolism, RNA-binding, and protein foldings, suggesting the clock-regulation of neurotransmitter release, transportation of the membrane proteins, calcium-binding capability, and so on. We also found a rhythmic phosphorylation of N-ethylmaleimide-sensitive fusion protein and identified one of the amino acid residues modified by phosphorylation. These findings provide a new perspective on the relationship between the physiological functions of the retina and the circadian clock system.

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“…The circadian oscillators in photoreceptors are endogenous and able to function independently in the absence of other retinal inputs (Cahill and Besharse 1993;Thomas et al 1993;Ko et al 2001). Photoreceptor circadian oscillators regulate retinomotor movement (Pierce and Besharse 1985;Burnside 2001), outer segment disc shedding and membrane renewal (LaVail 1980;Besharse and Dunis 1983), morphological changes at synaptic ribbons (Adly et al 1999), gene expression (Korenbrot and Fernald 1989;Pierce et al 1993;Haque et al 2002), and the gating behavior of ion channels (Ko et al 2001) among other photoreceptor activities. Importantly, photoreceptors are more sensitive to intense light damage at night than during the day, even in animals that have been maintained in constant darkness (DD) for several days after circadian lightdark (LD) cycle entrainment (Vaughan et al 2002).…”

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confidence: 99%

The expression of L‐type voltage‐gated calcium channels in retinal photoreceptors is under circadian control

Ko¹,

Liu²,

Dryer³

et al. 2007

Journal of Neurochemistry

202

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Photoreceptors are non-spiking neurons, and their synapses mediate the continuous release of neurotransmitters under the control of L-type voltage-gated calcium channels (VGCCs). Photoreceptors express endogenous circadian oscillators that play important roles in regulating photoreceptor physiology and function. Here, we report that the L-type VGCCs in chick cone photoreceptors are under circadian control. The L-type VGCC currents are greater when measured during the subjective night than during the subjective day. Using antibodies against the VGCCa1C and VGCCa1D subunits, we found that the immunofluorescence intensities of both VGCCa1C and VGCCa1D in photoreceptors are higher during the subjective night. However, the mRNA levels of VGCCa1D, but not VGCCa1C, are rhythmic. Nocturnal increases in L-type VGCCs are blocked by manumycin A, PD98059, and KN93, which suggest that the circadian output pathway includes Ras, Erk, and calcium-calmodulin dependent kinase II. In summary, four independent lines of evidence show that the L-VGCCs in cone photoreceptors are under circadian control. Keywords: avian, circadian, photoreceptor, retina, voltagegated calcium channel. Visual systems must anticipate daily changes in ambient illumination over 10-12 orders of magnitude. Circadian oscillators in the retina provide a mechanism for visual systems to initiate more sustained adaptive changes throughout the course of the day (Cahill and Besharse 1995;Green and Besharse 2004). The circadian oscillators in photoreceptors are endogenous and able to function independently in the absence of other retinal inputs (Cahill and Besharse 1993;Thomas et al. 1993;Ko et al. 2001). Photoreceptor circadian oscillators regulate retinomotor movement (Pierce and Besharse 1985;Burnside 2001), outer segment disc shedding and membrane renewal (LaVail 1980;Besharse and Dunis 1983), morphological changes at synaptic ribbons (Adly et al. 1999), gene expression (Korenbrot and Fernald 1989;Pierce et al. 1993;Haque et al. 2002), and the gating behavior of ion channels (Ko et al. 2001) among other photoreceptor activities. Importantly, photoreceptors are more sensitive to intense light damage at night than during the day, even in animals that have been maintained in constant darkness (DD) for several days after circadian lightdark (LD) cycle entrainment (Vaughan et al. 2002).Photoreceptors are non-spiking neurons, and they release glutamate continuously in the darkness as a result of depolarization-evoked activation of L-type voltage-gated calcium channels (VGCCs) (Barnes and Kelly 2002). The synthesis and release of the neurohormone melatonin in photoreceptors is also under circadian control (Cahill and Besharse 1993;Bernard et al. 1997;Ivanova and Iuvone 2003b), and melatonin synthesis and release can be blocked by dihydropyridine inhibitors of L-type VGCCs (Iuvone and Besharse 1986;Ivanova and Iuvone 2003a). In this regard, we previously showed that there is a circadian regulation of the apparent affinity of cGMP-gated ion channels (CNGCs) for cG...

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Circadian regulation of lodopsin gene expression in embryonic photoreceptors in retinal cell culture

Cited by 161 publications

References 25 publications

Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Circadian proteomics of the mouse retina

The expression of L‐type voltage‐gated calcium channels in retinal photoreceptors is under circadian control

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Circadian regulation of lodopsin gene expression in embryonic photoreceptors in retinal cell culture

Cited by 161 publications

References 25 publications

Adenosine A2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Adenosine A2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Circadian proteomics of the mouse retina

The expression of L‐type voltage‐gated calcium channels in retinal photoreceptors is under circadian control

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Product

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Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander

Adenosine A_2a receptor‐mediated inhibition of rod opsin mRNA expression in tiger salamander