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Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout

Published online by Cambridge University Press:  24 April 2006

KATHY VELDHOEN ,
W. TED ALLISON ,
NIK VELDHOEN ,
BRADLEY R. ANHOLT ,
CAREN C. HELBING  and
CRAIG W. HAWRYSHYN
KATHY VELDHOEN
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
W. TED ALLISON
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada Current address: University of Michigan, Department of Molecular, Cellular and Developmental Biology, 3008 Kraus Natural Sciences Building, Ann Arbor, Michigan.
NIK VELDHOEN
Affiliation:
Department of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada
BRADLEY R. ANHOLT
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
CAREN C. HELBING
Affiliation:
Department of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada
CRAIG W. HAWRYSHYN
Affiliation:
Department of Biology, University of Victoria, Victoria, British Columbia, Canada
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Abstract

The abundance and spatial distribution of retinal cone photoreceptors change during thyroid hormone (TH)-induced and natural development of rainbow trout (Oncorhynchus mykiss). These changes are thought to allow the fish to adapt to different photic environments throughout its life history. To date, the ontogeny of rainbow trout cone photoreceptors has been examined using physiological and morphological approaches. In this study, we extended these observations by measuring opsin gene expression in retinal quadrants during natural and TH-induced development. Gene expression during natural development was investigated in retinae from fish at both parr and smolt stages. The role of TH in modulating opsin gene expression was determined in TH-treated parr and control fish sampled after two, nine, and 22 days of treatment. Total RNA was isolated from each retinal quadrant and steady-state opsin mRNA levels were measured using reverse transcriptase real-time quantitative polymerase chain reaction (QPCR) analysis. Expression of ultraviolet-sensitive opsin (SWS1), rod opsin (RH1), middle wavelength-sensitive opsin (RH2), and long wavelength-sensitive opsin (LWS) transcripts vary spatially in the parr retina. Smolts, compared to parr, had downregulated SWS1 expression in all quadrants, lower LWS expression dorsally, higher RH1 expression nasally, and higher RH2 expression dorsally. In TH-treated parr, SWS1 opsin expression was downregulated in the nasal quadrants by two days. SWS1 displayed the greatest degree of downregulation in all quadrants after nine days of treatment, with an increase in short wavelength-sensitive (SWS2) and RH2 opsin mRNA expression in the temporal quadrants. This study reveals that opsin genes display spatially significant differences within rainbow trout retina in their level of mRNA expression, and that regulation of opsin expression is a dynamic process that is influenced by TH. This is particularly evident for SWS1 gene expression in parr following TH-induced and natural development.

Keywords

opsinOncorhynchus mykisscone photoreceptorthyroid hormonedevelopment
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 2 , March 2006 , pp. 169 - 179
Copyright
2006 Cambridge University Press

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References

REFERENCES

Allison, W.T., Dann, S.G., Helvik, J.V., Bradley, C., Moyer, H.D., & Hawryshyn C.W. (2003). Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). Journal of Comparative Neurology 461, 294–306.CrossRefGoogle Scholar
Allison, W.T., Dann, S.G., Veldhoen, K.M., & Hawryshyn, C.W. (2006). Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. Journal of Comparative Neurology. In Press.CrossRefGoogle Scholar
Andison, M.E. & Sivak, J.G. (1996). The naturally occurring accommodative response of the oscar, Astronotus ocellatus, to visual stimuli. Vision Research 36, 3021–3027.CrossRefGoogle Scholar
Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L.Y., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., & Robbins, J.T. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513–523.CrossRefGoogle Scholar
Beaudet, L., Browman, H.I., & Hawryshyn, C.W. (1993). Optic nerve response and retinal structure in rainbow trout of different sizes. Vision Research 33, 1739–1746.CrossRefGoogle Scholar
Beaudet, L. & Hawryshyn, C.W. (1999). Ecological aspects of vertebrate visual ontogeny. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, M.B.A., Lowe, E.R., Partridge, J.C. & Vallerga, S., pp. 413–437. Dordrecht, The Netherlands: Kluwer Academic Publishers.CrossRef
Beaudet, L., Novales Flamarique, I., & Hawryshyn, C.W. (1997). Cone photoreceptor topography in the retina of sexually mature pacific salmonid fishes. Journal of Comparative Neurology 383, 49–59.3.0.CO;2-L>CrossRefGoogle Scholar
Bender, K., Blattner, C., Knebel, A., Iordanov, M., Herrlich, P., & Rahmsdorf, H.J. (1997). UV-induced signal transduction. Journal of Photochemistry and Photobiolology B: Biology 37, 1–17.CrossRefGoogle Scholar
Bowmaker, J.K. (1995). The visual pigments of fish. Progress in Retinal and Eye Research 15, 1–31.CrossRefGoogle Scholar
Bridges, C.D.B. (1972). The rhodopsin-porphyropsin visual system. In Handbook of Sensory Physiology, ed. Dartnall, H.J.A., pp. 417–480. New York, NY: Springer-Verlag.CrossRef
Browman, H.I. & Hawryshyn, C.W. (1992). Thyroxine induces a precocial loss of ultraviolet sensitivity in rainbow trout (Oncorhynchus mykiss, Teleostei). Vision Research 32, 2303–2312.CrossRefGoogle Scholar
Browman, H.I. & Hawryshyn, C.W. (1994). The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxine. Vision Research 34, 1397–1406.CrossRefGoogle Scholar
Bunt, S.M. (1991). Evolution of vision in fishes. In Evolution of the Eye and Visual System Vol. 2 Vision and Visual Dysfunction, ed. Cronly-Dillon, J. & Gregory, R.L., pp. 398–420. Boca Raton, Florida: CRC Press, Inc.
Callery, E.M. & Elinson, R.P. (2000). Thyroid hormone-dependent metamorphosis in a direct developing frog. Proceedings of the National Academy of Sciences USA 97, 2615–2620.CrossRefGoogle Scholar
Carleton, K.L. & Kocher, T.D. (2001). Cone opsin genes of African cichlid fishes: tuning spectral sensitivity by differential gene expression. Molecular Biology and Evolution 18, 1540–1550.CrossRefGoogle Scholar
Cheng, C.L. & Novales Flamarique, I. (2004). New mechanisms for modulating colour vision. Nature 428, 279.Google Scholar
Collin, S.P. & Tresize, A.E.O. (2004). The origins of colour vision in vertebrates. Clinical and Experimental Optometry 87, 217–223.CrossRefGoogle Scholar
Crump, D., Werry, K., Veldhoen, N., Van Aggelen, G., & Helbing, C.C. (2002). Exposure to the herbicide acetochlor alters thyroid hormone-dependent gene expression and metamorphosis in Xenopus laevis. Environmental Health Perspectives 110, 1199–1205.CrossRefGoogle Scholar
Dann, S.G., Allison, W.T., Levin, D.B., Taylor, J.S., & Hawryshyn, C.W. (2004a). Salmonid opsin sequences undergo positive selection and indicate an alternate evolutionary relationship in Oncorhynchus. Journal of Molecular Evolution 58, 400–412.Google Scholar
Dann, S.G., Allison, W.T., Veldhoen, K., Johnson, T., & Hawryshyn, C.W. (2004b). Chromatin immunoprecipitation assay on the rainbow trout opsin proximal promoters illustrates binding of NF-κB and c-jun to the SWS1 promoter in the retina. Experimental Eye Research 78, 1015–1024.Google Scholar
Deutschlander, M.E., Greaves, D.K., Haimberger, T.J., & Hawryshyn, C.W. (2001). Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Oncorhynchus mykiss. Journal of Experimental Biology 204, 2401–2413.Google Scholar
Forrest, D., Reh, T.A., & Rüsch, A. (2002). Neurodevelopmental control by thyroid hormone receptors. Current Opinion in Neurobiology 12, 49–56.CrossRefGoogle Scholar
Grimm, C., Wenzel, A., Behrens, A., Hafezi, F., Wagner, E.F., & Remé, C.E. (2001). AP-1 mediated retinal photoreceptor apoptosis is independent of N-terminal phosphorylation of c-Jun. Cell Death and Differentiation 8, 859–867.CrossRefGoogle Scholar
Hafezi, F., Marti, A., Grimm, C., Wenzel, A., & Remé, C.E. (1999). Differential DNA binding activities of the transcription factors AP-1 and Oct-1 during light-induced apoptosis of photoreceptors. Vision Research 39, 2511–2518.CrossRefGoogle Scholar
Harpavat, S. & Cepko, C.L. (2003). Thyroid hormone and retinal development: an emerging field. Thyroid 13, 1013–1019.CrossRefGoogle Scholar
Hart, N.S. (2001). Variations in cone photoreceptor abundance and the visual ecology of birds. Journal of Comparative Physiology A 187, 685–698.CrossRefGoogle Scholar
Hawryshyn, C.W., Arnold, M.G., Chaisson, D.J., & Martin, P.C. (1989). The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri). Visual Neuroscience 2, 247–254.CrossRefGoogle Scholar
Hawryshyn, C.W., Haimberger, T.J., & Deutschlander, M.E. (2001). Microspectrophotometric measurements of vertebrate photoreceptors using CCD-based detection technology. Journal of Experimental Biology 204, 2431–2438.Google Scholar
Hawryshyn, C.W., Martens, G., Allison, W.T., & Anholt, B.R. (2003). Regeneration of ultraviolet-sensitive cones in the retinal cone mosaic of thyroxin-challenged post-juvenile rainbow trout (Oncorhynchus mykiss). Journal of Experimental Biology 206, 2665–2673.CrossRefGoogle Scholar
Helvik, J.V., Drivenes, Ø., Harboe, T., & Seo, H.-C. (2001). Topography of different photoreceptor cell types in the larval retina of the Atlantic halibut (Hippoglossus hippoglossus). Journal of Experimental Biology 204, 2553–2559.Google Scholar
Hoar, W.S. (1988). The physiology of smolting salmonids. In Fish Physiology, ed. Hoar, W.S. & Randall, D.J., pp. 275–343. San Diego, CA: Academic Press, Inc.CrossRef
Köhrle, J. (2002). Iodothyronine deiodinases. Methods in Enzymology 347, 125–167.CrossRefGoogle Scholar
Krishnamoorthy, R.R., Crawford, M.J., Chaturvedi, M.M., Jain, S.K., Aggarwal, B.B., Al-Ubaidi, M.R., & Agarwal N. (1999). Photo-oxidative stress down-modulates the activity of nuclear factor-κB via involvement of caspase-1, leading to apoptosis of photoreceptor cells. Journal of Biological Chemistry 274, 3734–3743.CrossRefGoogle Scholar
Kunz, Y.W., Wildenburg, G., Goodrich, L., & Callaghan, E. (1994). The fate of ultraviolet receptors in the retina of Atlantic salmon (Salmo salar). Vision Research 34, 1375–1383.CrossRefGoogle Scholar
Leatherland, J.F. (1994). Reflections of the thyroidology of fishes: from molecules to humankind. Guelph Ichthyology Reviews 2, 1–67.Google Scholar
Lee, S.-K., Kim, J.-H., Lee, Y.C., Cheong, J., & Lee, J.W. (2000). Silencing mediator of retinoic acid and thyroid hormone receptors, as a novel transcriptional corepressor molecule of activating protein-1, nuclear factor-κB, and serum response factor. Journal of Biological Chemistry 275, 12470–12474.CrossRefGoogle Scholar
Loew, E.R. & Lythgoe, J.N. (1978). The ecology of cone pigments in teleost fishes. Vision Research 18, 715–722.CrossRefGoogle Scholar
Makino, C.L. & Dodd, R.L. (1996). Multiple visual pigments in a photoreceptor of the salamander retina. Journal of General Physiology 108, 27–34.CrossRefGoogle Scholar
Marsh-Armstrong, N., Huang, H., Remo, B.F., Liu, T.T., & Brown, D.D. (1999). Asymmetric growth and development of the Xenopus laevis retina during metamorphosis is controlled by type III deiodinase. Neuron 24, 871–878.CrossRefGoogle Scholar
Minamoto, T. & Shimizu, I. (2005). Molecular cloning of cone opsin genes and their expression in the retina of a smelt, Ayu (Plecoglossus altivelis, Teleostei). Comparative Biochemistry and Physiology, Part B 140, 197–205.CrossRefGoogle Scholar
Nathans, J. (1987). Molecular biology of visual pigments. Annual Review of Neuroscience 10, 163–194.CrossRefGoogle Scholar
Ng, L., Hurley, J.B., Dierks, B., Srinivas, M., Saltó, C., Vennström, B., Reh, T.A., & Forrest, D. (2001). A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nature Genetics 27, 94–98.Google Scholar
Novales-Flamarique, I., Hendry, A., & Hawryshyn, C.W. (1992). The photic environment of a salmonid nursery lake. Journal of Experimental Biology 69, 121–141.Google Scholar
Oppenheimer, J.H., Schwartz, H.L., & Strait, K.A. (1995). An integrated view of thyroid hormone actions in vivo. In Molecular Endocrinology: Basic Concepts and Clinical Correlations, ed. Weintraub, B.E., pp. 249–269. New York, NY: Raven Press, Ltd.
Parry, J.W.L. & Bowmaker, J.K. (2002). Visual pigment coexpression in guinea pig cones: a microspectrophotometric study. Investigative Ophthalmology and Visual Science 43, 1662–1665.Google Scholar
Plate, E.M., Adams, B.A., Allison, W.T., Martens, G., Hawryshyn, C.W., & Eales, J.G. (2002). The effects of thyroxine or a GnRH analogue on thyroid hormone deiodination in the olfactory epithelimum and retina of the rainbow trout, Oncorhynchus mykiss, and sockeye salmon, Oncorhynchus nerka. General and Comparative Endocrinology 127, 59–65.CrossRefGoogle Scholar
Quinn, G.P. & Keough, M.J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge: Cambridge University Press.CrossRef
Rapp, L.M. & Ghalayini, A.J. (1999). Influence of UVA light stress on photoreceptor cell metabolism: decreased rates of rhodopsin regeneration and opsin synthesis. Experimental Eye Research 68, 757–764.CrossRefGoogle Scholar
Röhlich, P., van Veen, Th., & Szél, Á. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 1159–1166.CrossRefGoogle Scholar
Schmidt, E.D.L., Cramer, S.J., & Offringa, R. (1993). The thyroid hormone receptor interferes with transcriptional activation via the AP-1 complex. Biochemical and Biophysical Research Communications 192, 151–160.CrossRefGoogle Scholar
Shand, J., Partridge, J.C., Archer, S.N., Potts, G.W., & Lythgoe, J.N. (1988). Spectral absorbance changes in the violet/blue sensitive cones of the juvenile Pollack, Pollachius pollachius. J Comp Physiol A Sens Neural Behav Physiol 163, 699–703.CrossRefGoogle Scholar
Shi, Y. & Liang, V. (1994). Cloning and characterization of the ribosomal protein L8 gene from Xenopus laevis. Biochimica et Biophysica Acta 1217, 227–228.CrossRefGoogle Scholar
Shibusawa, N., Hashimoto, K., Nikrodhanond, A.A., Liberman, M.C., Applebury, M.L., Liao, X.H., Robbins, J.T., Refetoff, S., Cohen, R.N., & Wondisford, F.E. (2003). Thyroid hormone action in the absence of thyroid hormone receptor DNA-binding in vivo. Journal of Clinical Investigation 112, 588–597.CrossRefGoogle Scholar
Silvers, A.L. & Bowden, G.T. (2002). UVA irradiation-induced activation of activator protein-1 is correlated with induced expression of AP-1 family members in the human keratinocyte cell line HaCaT. Photochemistry and Photobiology 75, 302–310.2.0.CO;2>CrossRefGoogle Scholar
Smith, H.O. (1980). Recovery of DNA from gels. Methods in Enzymology 65, 371–380.CrossRefGoogle Scholar
Takechi, M. & Kawamura, S. (2005). Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. Journal of Experimental Biology 208, 1337–1345.CrossRefGoogle Scholar
Vile, G.F., Tanew-Iliitschew, A., & Tyrrell, R.M. (1995). Activation of NF-κB in human skin fibroblasts by the oxidative stress generated by UVA radiation. Photochemistry and Photobiology 62, 463–468.CrossRefGoogle Scholar
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. Journal of Neuroscience 10, 3390–3401.Google Scholar
Xiao, M. & Hendrickson, A. (2000). Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. Journal of Comparative Neurology 425, 545–559.3.0.CO;2-3>CrossRefGoogle Scholar
Yanagi, Y., Takezawa, S., & Kato, S. (2002). Distinct functions of photoreceptor cell-specific nuclear receptor, thyroid hormone receptor β2 and CRX in cone photoreceptor development. Investigative Ophthalmology and Visual Science 43, 3489–3494.Google Scholar
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19, 385–419.CrossRefGoogle Scholar
Zhang, J. & Lazar, M.A. (2000). The mechanism of action of thyroid hormones. Annual Review of Physiology 62, 439–66.CrossRefGoogle Scholar