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Circadian clock control of connexin36 phosphorylation in retinal photoreceptors of the CBA/CaJ mouse strain

Published online by Cambridge University Press:  20 May 2015

ZHIJING ZHANG ,
HONGYAN LI ,
XIAOQIN LIU ,
JOHN O'BRIEN  and
CHRISTOPHE P. RIBELAYGA
ZHIJING ZHANG
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Health Science Center at Houston, Medical School, Houston, Texas
HONGYAN LI
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Health Science Center at Houston, Medical School, Houston, Texas
XIAOQIN LIU
Affiliation:
Department of Neurobiology and Anatomy, University of Texas Health Science Center at Houston, Medical School, Houston, Texas
JOHN O'BRIEN
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Health Science Center at Houston, Medical School, Houston, Texas Graduate School of Biomedical Sciences, University of Texas Health Science Center at Houston, Houston, Texas Program in Neuroscience, Graduate School of Biomedical Sciences, The University of Texas Health Science Center at Houston, Houston, Texas Neuroscience Research Center, The University of Texas Health Science Center at Houston, Houston, Texas
CHRISTOPHE P. RIBELAYGA*
Affiliation:
Department of Ophthalmology and Visual Science, University of Texas Health Science Center at Houston, Medical School, Houston, Texas Graduate School of Biomedical Sciences, University of Texas Health Science Center at Houston, Houston, Texas Program in Neuroscience, Graduate School of Biomedical Sciences, The University of Texas Health Science Center at Houston, Houston, Texas Neuroscience Research Center, The University of Texas Health Science Center at Houston, Houston, Texas
*
*Address correspondence to: Christophe P. Ribelayga, Ruiz Department of Ophthalmology and Visual Science, The University of Texas Medical School, 6431 Fannin St., MSB 7.024, Houston, TX 77030. E-mail: Christophe.p.ribelayga@uth.tmc.edu
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Abstract

The gap-junction-forming protein connexin36 (Cx36) represents the anatomical substrate of photoreceptor electrical coupling in mammals. The strength of coupling is directly correlated to the phosphorylation of Cx36 at two regulatory sites: Ser110 and Ser293. Our previous work demonstrated that the extent of biotinylated tracer coupling between photoreceptor cells, which provides an index of the extent of electrical coupling, depends on the mouse strain. In the C57Bl/6J strain, light or dopamine reduces tracer coupling and Cx36 phosphorylation in photoreceptors. Conversely, darkness or a dopaminergic antagonist increases tracer coupling and Cx36 phosphorylation, regardless of the daytime. In the CBA/CaJ strain, photoreceptor tracer coupling is not only regulated by light and dopamine, but also by a circadian clock, a type of oscillator with a period close to 24 h and intrinsic to the retina, so that under prolonged dark-adapted conditions tracer coupling is broader at night compared to daytime. In the current study, we examined whether the modulation of photoreceptor coupling by a circadian clock in the CBA/CaJ mouse photoreceptors reflected a change in Cx36 protein expression and/or phosphorylation. We found no significant change in Cx36 expression or in the number of Cx36 gap junction among the conditions examined. However, we found that Cx36 phosphorylation is higher under dark-adapted conditions at night than in the daytime, and is the lowest under prolonged illumination at any time of the day/night cycle. Our observations are consistent with the view that the circadian clock regulation of photoreceptor electrical coupling is mouse strain-dependent and highlights the critical position of Cx36 phosphorylation in the control of photoreceptor coupling.

Keywords

RetinaGap junctionElectrical couplingPhotoreceptorsCircadian clock
Type
Brief Communication
Information
Visual Neuroscience , Volume 32 , 2015 , E009
Copyright
Copyright © Cambridge University Press 2015 

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References

Bloomfield, S.A. & Völgyi, B. (2009). The diverse functional roles and regulation of neuronal gap junctions in the retina. Nature Reviews. Neuroscience 10, 495–506.CrossRefGoogle ScholarPubMed
Dowling, J.E. (2012). The Retina: An Approachable Part of the Brain (Rev ed.). Cambridge: Harvard University Press.CrossRefGoogle Scholar
Heikkinen, H., Vinberg, F., Nymark, S. & Koskelainen, A. (2011). Mesopic background lights enhance dark-adapted cone ERG flash responses in the intact mouse retina: A possible role for gap junctional decoupling. Journal of Neurophysiology 105, 2309–2318.CrossRefGoogle ScholarPubMed
Huang, H., Wang, Z., Weng, S.J., Sun, X.H. & Yang, X.L. (2013). Neuromodulatory role of melatonin in retinal information processing. Progress in Retinal and Eye Research 32, 64–87.CrossRefGoogle ScholarPubMed
Iuvone, P.M., Tosini, G., Pozdeyev, N., Haque, R., Klein, D.C. & Chaurasia, S.S. (2005). Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Progress in Retinal and Eye Research 24, 433–456.CrossRefGoogle ScholarPubMed
Jin, N., Chuang, A.Z., Masson, P.J. & Ribelayga, C. (2015). Rod electrical coupling is controlled by a circadian clock and dopamine in mouse retina. The Journal of Physiology 593, 1597–1631.CrossRefGoogle ScholarPubMed
Kasahara, T., Abe, K., Mekada, K., Yoshiki, A. & Kato, T. (2010). Genetic variation of melatonin productivity in laboratory mice under domestication. Proceedings of the National Academy of Sciences of the United States of America 107, 6412–6417.CrossRefGoogle ScholarPubMed
Katti, C., Butler, R. & Sekaran, S. (2013). Diurnal and circadian regulation of connexin 36 transcript and protein in the mammalian retina. Investigative Ophthalmology & Visual Science 54, 821–829.CrossRefGoogle ScholarPubMed
Kolbinger, W. & Weiler, R. (1993). Modulation of endogenous dopamine release in the turtle retina: Effects of light, calcium, and neurotransmitters. Visual Neuroscience 10, 1035–1041.CrossRefGoogle ScholarPubMed
Kothmann, W.W., Li, X., Burr, G.S. & O'Brien, J. (2007). Connexin 35/36 is phosphorylated at regulatory sites in the retina. Visual Neuroscience 24, 363–375.CrossRefGoogle ScholarPubMed
Kothmann, W.W., Massey, S.C. & O'Brien, J. (2009). Dopamine-stimulated dephosphorylation of connexin 36 mediates AII amacrine cell uncoupling. The Journal of Neuroscience 29, 14903–14911.CrossRefGoogle ScholarPubMed
Kothmann, W.W., Trexler, E.B., Whitaker, C.M., Li, W., Massey, S.C. & O'Brien, J. (2012). Nonsynaptic NMDA receptors mediate activity-dependent plasticity of gap junctional coupling in the AII amacrine cell network. The Journal of Neuroscience 32, 6747–6759.CrossRefGoogle ScholarPubMed
Krizaj, D., Gabriel, R., Owen, W.G. & Witkovsky, P. (1998). Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. The Journal of Comparative Neurology 398, 529–538.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Li, H., Chuang, A.Z. & O'Brien, J. (2009). Photoreceptor coupling is controlled by connexin 35 phosphorylation in zebrafish retina. The Journal of Neuroscience 29, 15178–15186.CrossRefGoogle ScholarPubMed
Li, H., Chuang, A.Z. & O'Brien, J. (2014). Regulation of photoreceptor gap junctional phosphorylation by adenosine in zebrafish retina. Visual Neuroscience 31, 237–243.CrossRefGoogle ScholarPubMed
Li, H. & O'Brien, J. (2012). Regulation of gap junctional coupling in photoreceptors. In Photoreceptors: Physiology, Types and Abnormalities, ed. Akutagawa, E. & Ozaki, K., Hauppauge, NY: Nova Science.Google Scholar
Li, H., Zhang, Z., Blackburn, M.R., Wang, S.W., Ribelayga, C.P. & O'Brien, J. (2013). Adenosine and dopamine receptors coregulate photoreceptor coupling via gap junction phosphorylation in mouse retina. The Journal of Neuroscience 33, 3135–3150.CrossRefGoogle ScholarPubMed
Liu, X., Zhang, Z. & Ribelayga, C. (2012). Heterogeneous expression of the core circadian clock proteins among neuronal cell types in mouse retina. PLoS One 7, e50602.CrossRefGoogle ScholarPubMed
Mangel, S.C. & Ribelayga, C. (2010). Comparative eye: The circadian clock in the retina regulates rod and cone pathways. In The Encyclopedia of the Eye, Vol. 1, ed. Dartt, D.A., Besharse, J.C. & Dana, R., pp. 283–289, Oxford: Elsevier.CrossRefGoogle Scholar
McMahon, D.G., Iuvone, P.M. & Tosini, G. (2014). Circadian organization of the mammalian retina: From gene regulation to physiology and diseases. Progress in Retinal and Eye Research 39, 58–76.CrossRefGoogle ScholarPubMed
Ribelayga, C., Cao, Y. & Mangel, S.C. (2008). The circadian clock in the retina controls rod-cone coupling. Neuron 59, 790–801.CrossRefGoogle ScholarPubMed
Ribelayga, C. & Mangel, S.C. (2005). A circadian clock and light/dark adaptation differentially regulate adenosine in the mammalian retina. The Journal of Neuroscience 25, 215–222.CrossRefGoogle ScholarPubMed
Ribelayga, C. & Mangel, S.C. (2010). Identification of a circadian clock-controlled neural pathway in the rabbit retina. PLoS One 5, e11020.CrossRefGoogle ScholarPubMed
Ribelayga, C., Wang, Y. & Mangel, S.C. (2002). Dopamine mediates circadian clock regulation of rod and cone input to fish retinal horizontal cells. The Journal of Physiology 544, 801–816.CrossRefGoogle ScholarPubMed
Ribelayga, C., Wang, Y. & Mangel, S.C. (2004). A circadian clock in the fish retina regulates dopamine release via activation of melatonin receptors. The Journal of Physiology 554, 467–482.CrossRefGoogle ScholarPubMed
Wang, Y. & Mangel, S.C. (1996). A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. Proceedings of the National Academy of Sciences of the United States of America 93, 4655–4660.CrossRefGoogle ScholarPubMed
Yang, X.L. & Wu, S.M. (1989). Modulation of rod-cone coupling by light. Science 244, 352–354.CrossRefGoogle ScholarPubMed