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Transcriptional regulation of nucleoredoxin-like genes takes place on a daily basis in the retina and pineal gland of rats

Published online by Cambridge University Press:  11 May 2015

TANJA WOLLOSCHECK ,
STEFANIE KUNST ,
DEBRA K. KELLEHER  and
RAINER SPESSERT
TANJA WOLLOSCHECK
Affiliation:
Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
STEFANIE KUNST
Affiliation:
Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
DEBRA K. KELLEHER
Affiliation:
Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
RAINER SPESSERT*
Affiliation:
Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany
*
*Address correspondence to: Rainer Spessert, Department of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg University Mainz, Saarstraße 19-21, 55099 Mainz, Germany. E-mail: [email protected]
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Abstract

The nucleoredoxin-like gene Nxnl1 (Txnl6) and its paralogue Nxnl2 encode the rod-derived cone viability factors (RdCVF and RdCVF2), which increase the resistance to photooxidative damage and have therapeutic potential for the survival of cones in retinitis pigmentosa. In this study, the transcription of Nxnl genes was investigated as a function of the day/night cycle in rats. The transcript levels of Nxnl1 and Nxnl2 were seen to display daily rhythms with steadily increasing values during the light phase and peak expression around dark onset in preparations of whole retina, photoreceptor cells and—but only in regard to Nxnl1—in photoreceptor-related pinealocytes. The cycling of Nxnl1 but not that of Nxnl2 persisted in constant darkness in the retina. This suggests that daily regulation of Nxnl1 is driven by a circadian clock, whereas that of Nxnl2 is promoted by environmental light. The present data indicate clock- and light-dependent regulations of nucleoredoxin-like genes that may be part of a protective shield against photooxidative damage.

Keywords

RatNucleoredoxin-like genesRod-derived cone viability factorRetinitis pigmentosaArylalkylamine N-Acetyltransferase
Type
Research Article
Information
Visual Neuroscience , Volume 32 , 2015 , E002
Copyright
Copyright © Cambridge University Press 2015 

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References

Bailey, M.J., Coon, S.L., Carter, D.A., Humphries, A., Kim, J.S., Shi, Q., Gaildrat, P., Morin, F., Ganguly, S., Hogenesch, J.B., Weller, J.L., Rath, M.F., Møller, M., Baler, R., Sugden, D., Rangel, Z.G., Munson, P.J. & Klein, D.C. (2009). Night/day changes in pineal expression of >600 genes: Central role of adrenergic/cAMP signaling. The Journal of Biological Chemistry 284, 7606–7622.CrossRefGoogle ScholarPubMed
Chalmel, F., Léveillard, T., Jaillard, C., Lardenois, A., Berdugo, N., Morel, E., Koehl, P., Lambrou, G., Holmgren, A., Sahel, J.A. & Poch, O. (2007). Rod-derived cone viability factor-2 is a novel bifunctional-thioredoxin-like protein with therapeutic potential. BMC Molecular Biology 8, 74.CrossRefGoogle ScholarPubMed
Cingolani, C., Rogers, B., Lu, L., Kachi, S., Shen, J. & Campochiaro, P.A. (2006). Retinal degeneration from oxidative damage. Free Radical Biology and Medicine 40, 660–669.CrossRefGoogle ScholarPubMed
Cornelissen, G. (2014). Cosinor based rhythmometry. Theoretical Biology and Medical Modelling 11, 16.CrossRefGoogle ScholarPubMed
Cronin, T., Léveillard, T. & Sahel, J.A. (2007). Retinal degenerations: From cell signaling to cell therapy; pre-clinical and clinical issues. Current Gene Therapy 7, 121–129.CrossRefGoogle ScholarPubMed
Cronin, T., Raffelsberger, W., Lee-Rivera, I., Jaillard, C., Niepon, M.L., Kinzel, B., Clérin, E., Petrosian, A., Picaud, S., Poch, O., Sahel, J.A. & Léveillard, T. (2010). The disruption of the rod-derived cone viability gene leads to photoreceptor dysfunction and susceptibility to oxidative stress. Cell Death and Differentiation 17, 1199–1210.CrossRefGoogle ScholarPubMed
Daiger, S.P., Sullivan, L.S. & Bowne, S.J. (2013). Genes and mutations causing retinitis pigmentosa. Clinical Genetics 84, 132–141.CrossRefGoogle ScholarPubMed
Fridlich, R., Delalande, F., Jaillard, C., Lu, J., Poidevin, L., Cronin, T., Perrocheau, L., Millet-Puel, G., Niepon, M.L., Poch, O., Holmgren, A., Van Dorsselaer, A., Sahel, J.A. & Léveillard, T. (2009). The thioredoxin-like protein rod-derived cone viability factor (RdCVFL) interacts with TAU and inhibits its phosphorylation in the retina. Molecular and Cellular Proteomics 8, 1206–1218.CrossRefGoogle ScholarPubMed
Goldmann, T., Burgemeister, R., Sauer, U., Loeschke, S., Lang, D.S., Branscheid, D., Zabel, P. & Vollmer, E. (2006). Enhanced molecular analyses by combination of the HOPE-technique and laser microdissection. Diagnostic Pathology 1, 2.CrossRefGoogle ScholarPubMed
Hastings, M.H., Maywood, E.S. & Reddy, A.B. (2008). Two decades of circadian time. Journal of Neuroendocrinology 20, 812–819.CrossRefGoogle ScholarPubMed
Hölter, P., Kunst, S., Wolloscheck, T., Kelleher, D.K., Sticht, C., Wolfrum, U. & Spessert, R. (2012). The retinal clock drives the expression of Kcnv2, a channel essential for visual function and cone survival. Investigative Ophthalmology and Visual Science 53, 6947–6954.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
Jaillard, C., Mouret, A., Niepon, M.L., Clérin, E., Yang, Y., Lee-Rivera, I., Aït-Ali, N., Millet-Puel, G., Cronin, T., Sedmak, T., Raffelsberger, W., Kinzel, B., Trembleau, A., Poch, O., Bennett, J., Wolfrum, U., Lledo, P.M., Sahel, J.A. & Léveillard, T. (2012). Nxnl2 splicing results in dual functions in neuronal cell survival and maintenance of cell integrity. Human Molecular Genetics 21, 2298–2311.CrossRefGoogle ScholarPubMed
Klein, D.C. (2007). Arylalkylamine n-acetyltransferase: “the Timezyme”. The Journal of Biological Chemistry 282, 4233–4237.CrossRefGoogle Scholar
Komeima, K., Rogers, B., Lu, L. & Campochiaro, P.A. (2006). Antioxidants reduce cone cell death in a model of retinitis pigmentosa. Proceedings of the National Academy of Sciences of the United States of America 103, 11300–11305.CrossRefGoogle Scholar
Kunst, S., Wolloscheck, T., Hölter, P., Wengert, A., Grether, M., Sticht, C., Weyer, V., Wolfrum, U. & Spessert, R. (2013). Transcriptional analysis of rat photoreceptor cells reveals daily regulation of genes important for visual signaling and light damage susceptibility. Journal of Neurochemistry 124, 757–769.CrossRefGoogle ScholarPubMed
Lambard, S., Reichman, S., Berlinicke, C., Niepon, M., Goureau, O., Sahel, J.A., Léveillard, T. & Zack, D.J. (2010). Expression of rod-derived cone viability factor: Dual role of CRX in regulating promoter activity and cell-type specificity. PLoS One 5, e13075.CrossRefGoogle ScholarPubMed
Léveillard, T., Mohand-Saïd, S., Lorentz, O., Hicks, D., Fintz, A.C., Clérin, E., Simonutti, M., Forster, V., Cavusoglu, N., Chalmel, F., Dollé, P., Poch, O., Lambrou, G. & Sahel, J.A. (2004). Identification and characterization of rod-derived cone viability factor. Nature Genetics 36, 755–759.CrossRefGoogle ScholarPubMed
Léveillard, T. & Sahel, J.A. (2010). Rod-derived cone viability factor for treating blinding diseases: From clinic to redox signaling. Science Translational Medicine 2, 26ps16.CrossRefGoogle ScholarPubMed
Maronde, E. & Stehle, J.H. (2007). The mammalian pineal gland: Known facts, unknown facets. Trends in Endocrinology and Metabolism 18, 142–149.CrossRefGoogle ScholarPubMed
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
Mohand-Said, S., Deudon-Combe, A., Hicks, D., Simonutti, M., Forster, V., Fintz, A.C., Léveillard, T., Dreyfus, H. & Sahel, J.A. (1998). Normal retina releases a diffusible factor stimulating cone survival in the retinal degeneration mouse. Proceedings of the National Academy of Sciences of the United States of America 95, 8357–8362.CrossRefGoogle ScholarPubMed
Mohand-Said, S., Hicks, D., Dreyfus, H. & Sahel, J.A. (2000). Selective transplantation of rods delays cone loss in a retinitis pigmentosa model. Archives of Ophthalmology 118, 807–811.CrossRefGoogle Scholar
Mohand-Said, S., Hicks, D., Simonutti, M., Tran-Minh, D., Deudon-Combe, A., Dreyfus, H., Silverman, M.S., Ogilvie, J.M., Tenkova, T. & Sahel, J. (1997). Photoreceptor transplants increase host cone survival in the retinal degeneration (rd) mouse. Ophthalmic Research 29, 290–297.CrossRefGoogle ScholarPubMed
Møller, M. & Baeres, F.M. (2002). The anatomy and innervation of the mammalian pineal gland. Cell and Tissue Research 309, 139–150.CrossRefGoogle ScholarPubMed
Niki, T., Hamada, T., Ohtomi, M., Sakamoto, K., Suzuki, S., Kako, K., Hosoya, Y., Horikawa, K. & Ishida, N. (1998). The localization of the site of arylalkylamine N-acetyltransferase circadian expression in the photoreceptor cells of mammalian retina. Biochemical and Biophysical Research Communications 248, 115–120.CrossRefGoogle ScholarPubMed
Rath, M.F., Bailey, M.J., Kim, J.S., Coon, S.L., Klein, D.C. & Møller, M. (2009 a). Developmental and daily expression of the Pax4 and Pax6 homeobox genes in the rat retina: Localization of Pax4 in photoreceptor cells. Journal of Neurochemistry 108, 285–294.CrossRefGoogle ScholarPubMed
Rath, M.F., Bailey, M.J., Kim, J.S., Ho, A.K., Gaildrat, P., Coon, S.L., Møller, M. & Klein, D.C. (2009 b). Developmental and diurnal dynamics of Pax4 expression in the mammalian pineal gland: Nocturnal down-regulation is mediated by adrenergic-cyclic adenosine 3',5'-monophosphate signaling. Endocrinology 150, 803–811.CrossRefGoogle ScholarPubMed
Rath, M.F., Rohde, K., Klein, D.C. & Møller, M. (2013). Homeobox genes in the rodent pineal gland: Roles in development and phenotype maintenance. Neurochemical Research 38, 1100–1112.CrossRefGoogle ScholarPubMed
Refinetti, R., Lissen, G.C. & Halberg, F. (2007). Procedures for numerical analysis of circadian rhythms. Biological Rhythm Research 38, 275–325.CrossRefGoogle ScholarPubMed
Reichman, S., Kalathur, R.K., Lambard, S., Aït-Ali, N., Yang, Y., Lardenois, A., Ripp, R., Poch, O., Zack, D.J., Sahel, J.A. & Léveillard, T. (2010). The homeobox gene CHX10/VSX2 regulates RdCVF promoter activity in the inner retina. Human Molecular Genetics 19, 250–261.CrossRefGoogle ScholarPubMed
Sahel, J.A., Leveillard, T., Picaud, S., Dalkara, D., Marazova, K., Safran, A., Paques, M., Duebel, J., Roska, B. & Mohand-Said, S. (2013). Functional rescue of cone photoreceptors in retinitis pigmentosa. Graefes Archive for Clinical and Experimental Ophthalmology 251, 1669–1677.CrossRefGoogle ScholarPubMed
Schneider, K., Tippmann, S., Spiwoks-Becker, I., Holthues, H., Wolloscheck, T., Spatkowski, G., Engel, L., Frederiksen, U. & Spessert, R. (2010). Unique clockwork in photoreceptor of rat. Journal of Neurochemistry 115, 585–594.CrossRefGoogle ScholarPubMed
Tosini, G., Pozdeyev, N., Sakamoto, K. & Iuvone, P.M. (2008). The circadian clock system in the mammalian retina. BioEssays 30, 624–633.CrossRefGoogle ScholarPubMed
Wang, X.W., Tan, B.Z., Sun, M., Ho, B. & Ding, J.L. (2008). Thioredoxin-like 6 protects retinal cell line from photooxidative damage by upregulating NF-kappaB activity. Free Radical Biology and Medicine 45, 336–344.CrossRefGoogle ScholarPubMed
Yang, Y., Mohand-Said, S., Danan, A., Simonutti, M., Fontaine, V., Clerin, E., Picaud, S., Léveillard, T. & Sahel, J.A. (2009). Functional cone rescue by RdCVF protein in a dominant model of retinitis pigmentosa. Molecular Therapy 17, 787–795.CrossRefGoogle Scholar