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Midkine expression is regulated by the circadian clock in the retina of the zebrafish

  • ANDA-ALEXANDRA CALINESCU (a1) (a2), PAMELA A. RAYMOND (a2) (a3) and PETER F. HITCHCOCK (a1) (a2)

Abstract

The retina displays numerous processes that follow a circadian rhythm. These processes are coordinated through the direct action of light on photoreceptive molecules and, in the absence of light, through autocrine/paracrine actions of extracellular neuromodulators. We previously described the expression of the genes encoding the secreted heparin-binding growth factors, midkine-a (mdka) and midkine-b (mdkb), in the retina of the zebrafish. Here, we provide evidence that the expression of mdka and mdkb follows a daily rhythm, which is independent of the presence or absence of light, and we propose that the expression of mdka is regulated by the circadian clock. Both qualitative and quantitative measures show that for mdka, the levels of mRNA and protein decrease during the night and increase during the subjective day. Qualitative measures show that the expression of mdkb increases during the second half of the subjective night and decreases during the second half of the subjective day. Within horizontal cells, the two midkine paralogs show asynchronous circadian regulation. Though intensely studied in the contexts of physiology and disease, this is the first study to provide evidence for the circadian regulation of midkines in the vertebrate nervous system.

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Corresponding author

*Address correspondence and reprint requests to: Peter F. Hitchcock, Department of Ophthalmology and Visual Sciences, W. K. Kellogg Eye Center, 1000 Wall Street, University of Michigan, Ann Arbor, MI 48105-0714. E-mail: peterh@umich.edu

References

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Calinescu, A.A., Vihtelic, T.S., Hyde, D.R. & Hitchcock, P.F. (2009). The cellular expression of midkine-a and midkine-b during retinal development and photoreceptor regeneration in zebrafish. The Journal of Comparative Neurology 514, 110.
Dekens, M.P. & Whitmore, D. (2008). Autonomous onset of the circadian clock in the zebrafish embryo. European Molecular Biology Organization 27, 27572765.
Doyle, S. & Menaker, M. (2007). Circadian photoreception in vertebrates. Cold Spring Harbor Symposia on Quantitative Biology 72, 499508.
Falcón, J., Besseau, L., Fuentès, M., Sauzet, S., Magnanou, E. & Boeuf, G. (2009). Structural and functional evolution of the pineal melatonin system in vertebrates. Annals of the New York Academy of Sciences 1163, 101111.
Hitchcock, P.F. & Kakuk-Atkins, L. (2004). The basic helix-loop-helix transcription factor neuroD is expressed in the rod lineage of the teleost retina. The Journal of Comparative Neurology 477, 108117.
Kadomatsu, K., Huang, R.P., Suganuma, T., Murata, F. & Muramatsu, T. (1990). A retinoic acid responsive gene MK found in the teratocarcinoma system is expressed in spatially and temporally controlled manner during mouse embryogenesis. The Journal of Cell Biology 110, 607616.
Kadomatsu, K. & Muramatsu, T. (2004). Midkine and pleiotrophin in neural development and cancer. Cancer Letters 204, 127143.
Kadomatsu, K., Tomomura, M. & Muramatsu, T. (1998). cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochemical and Biophysical Research Communications 151, 13121318.
Korenbrodt, J.I. & Fernald, R.D. (1989). Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature 337, 454457.
LaVail, M.M. (1980). Circadian nature of rod outer segment disc shedding in the rat. Investigative Ophthalmology & Visual Sciences 19, 407411.
Li, L. & Dowling, J.E. (1998). Zebrafish visual sensitivity is regulated by a circadian clock. Visual Neuroscience 15, 851857.
Li, P., Chaurasia, S.S., Gao, Y., Carr, A.L., Iuvone, P.M. & Li, L. (2008). CLOCK is required for maintaining the circadian rhythms of opsin mRNA expression in photoreceptor cells. The Journal of Biological Chemistry 283, 3167331678.
Liedtke, D. & Winkler, C. (2008). Midkine-b regulates cell specification at the neural plate border in zebrafish. Developmental Dynamics 237, 6274.
Menger, G.J., Koke, J.R. & Cahill, G.M. (2005). Diurnal and circadian retinomotor movements in zebrafish. Visual Neuroscience 22, 203209.
Mitsiadis, T.A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M. & Thesleff, I. (1995). Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121, 3751.
Muramatsu, T. (2002). Midkine and pleiotrophin: Two related proteins involved in development, survival, inflammation and tumorigenesis. Journal of Biochemistry 132, 359371.
Obama, H., Matsubara, S., Guénet, J.L. & Muramatsu, T. (1994). The midkine (MK) family of growth/differentiation factors: Structure of an MK-related sequence in a pseudogene and evolutionary relationships among members of the MK family. Journal of Biochemsitry 115, 516522.
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RTPCR. Nucleic Acids Research 29, e45.
Pierce, M.E. & Besharse, J.C. (1985). Circadian regulation of retinomotor movements. Interaction of melatonin and dopamine in the control of cone length. The Journal of General Physiology 86, 671689.
Rajendran, R.R., Van Niel, E.E., Stenkamp, D.L., Cunningham, L.L., Raymond, P.A. & Gonzalez-Fernandez, F. (1996). Zebrafish interphotoreceptor retinoid-binding protein: Differential circadian expression among cone subtypes. The Journal of Experimental Biology 199, 27752787.
Ribelayga, C., Cao, Y. & Mangel, S.C. (2008). The circadian clock in the retina controls rod-cone coupling. Neuron 59, 790801.
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, 215222.
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, 801816.
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, 467482.
Schäfer, M., Rembold, M., Wittbrodt, J., Schartl, M. & Winkler, C. (2005). Medial floor plate formation in zebrafish consists of two phases and requires trunk-derived Midkine-a. Genes in Development 19, 897902.
Vallone, D., Lahiri, K., Dickmeis, T. & Foulkes, N.S. (2005). Zebrafish cell clocks feel the heat and see the light. Zebrafish 2, 171187.
Vuilleumier, R., Besseau, L., Boeuf, G., Piparelli, A., Gothilf, Y., Gehring, W.G., Klein, D.C. & Falcón, J. (2006). Starting the zebrafish pineal circadian clock with a single photic transition. Endocrinology 147, 22732279.
Vuilleumier, R., Boeuf, G., Fuentes, M., Gehring, W.J. & Falcón, J. (2007). Cloning and early expression pattern of two melatonin biosynthesis enzymes in the turbot (Scophthalmus maximus). The European Journal of Neuroscience 25, 30473057.
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, 46554660.
Whitmore, D., Cermakian, N., Crosio, C., Foulkes, N.S., Pando, M.P., Travnickova, Z., Sassone-Corsi, P. (2000). A clockwork organ. Biological Chemistry 381, 793800.
Winkler, C. & Moon, R.T. (2001). Zebrafish mdk2, a novel secreted midkine, participates in posterior neurogenesis. Developmental Biology 229, 102118.
Winkler, C., Schafer, M., Duschl, J., Schartl, M. & Volff, J.N. (2003). Functional divergence of two zebrafish midkine growth factors following fish-specific gene duplication. Genome Research 13, 10671081.

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Midkine expression is regulated by the circadian clock in the retina of the zebrafish

  • ANDA-ALEXANDRA CALINESCU (a1) (a2), PAMELA A. RAYMOND (a2) (a3) and PETER F. HITCHCOCK (a1) (a2)

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