Abstract
Telomerase, a specialized reverse transcriptase that maintains telomere during cell division, is commonly associated with cell proliferation. Increasing evidence suggests that telomerase may bear functions other than telomere elongation. We investigated whether telomerase is expressed in the continuously growing goldfish retina. Telomeric repeat amplification protocol (TRAP) assay reveals telomerase activity in goldfish retina. Reverse transcription-polymerase chain reaction (RT-PCR) and western blot show that telomerase catalytic subunit (TERT) is expressed at both mRNA and protein levels. Localization of TERT by immunohistochemistry indicates prominent expression of TERT in the outer nuclear layer, the inner nuclear layer, and, in a small population of cells, in the ganglion cell layer. Coexpression of TERT with proliferative cell nuclear antigen (PCNA) immunoreactivity is found in rod progenitor cells. These results suggest the role of telomerase in vertebrate central nervous system (CNS) other than telomere maintenance, such as regulation of cell cycle progression and maintenance of retinal cell phenotypes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Braisted, J. E., & Raymond, P. A. (1993). Continued search for the cellular signals that regulate regeneration of dopaminergic neurons in goldfish retina. Brain Research Developmental Brain Research, 76, 221–232.
Fernald, R. D. (1990). Teleost vision: Seeing while growing. Journal of Experimental Zoology Supplement, 5, 167–180.
Fu, W., Begley, J. G., Killen, M. W., & Mattson, M. P. (1999). Anti-apoptotic role of telomerase in pheochromocytoma cells. Journal of Biological Chemistry, 274, 7264–7271.
Fu, W., Lu, C., Mattson, M. P. (2002). Telomerase mediates the cell survival-promoting actions of brain-derived neurotrophic factor and secreted amyloid precursor protein in developing hippocampal neurons. Journal of Neuroscience, 22, 10710–10719.
Hitchcock, P. F., Lindsey Myhr, K. J., Easter Jr., S. S., Mangione-Smith, R., & Jones, D. D. (1992). Local regeneration in the retina of the goldfish. Journal of Neurobiology, 23, 187–203.
Johns, P. R. (1977). Growth of the adult goldfish eye. III. Source of the new retinal cells. Journal of Comparative Neurology, 176, 343–357.
Johns, P. R. (1982). Formation of photoreceptors in larval and adult goldfish. Journal of Neuroscience, 2, 178–198.
Johns, P. R., & Fernald, R. D. (1981). Genesis of rods in teleost fish retina. Nature, 293, 141–142.
Julian, D., Ennis, K., & Korenbrot, J. I. (1998). Birth and fate of proliferative cells in the inner nuclear layer of the mature fish retina. Journal of Comparative Neurology, 394, 271–282.
Kang, H. J., Choi, Y. S., Hong, S. B., Kim, K. W., Woo, R. S., Won, S. J., et al. (2004). Ectopic expression of the catalytic subunit of telomerase protects against brain injury resulting from ischemia and NMDA-induced neurotoxicity. Journal of Neuroscience, 24, 1280–1287.
Klapper, W., Heidorn, K., Kuhne, K., Parwaresch, R., & Krupp, G. (1998a). Telomerase activity in ‘immortal’ fish. FEBS Letters, 434, 409–412.
Klapper, W., Kuhne, K., Singh, K. K., Heidorn, K., Parwaresch, R., & Krupp, G. (1998b). Longevity of lobsters is linked to ubiquitous telomerase expression. FEBS Letters, 439, 143–146.
Kuramoto, M., Ohsumi, K., Kishimoto, T., & Ishikawa, F. (2001). Identification and analyses of the Xenopus TERT gene that encodes the catalytic subunit of telomerase. Gene, 277, 101–110.
Lamond, A. I. (1989). Tetrahymena telomerase contains an internal RNA template. Trends in Biochemical Sciences, 14, 202–204.
Mack, A. F., & Fernald, R. D. (1995). New rods move before differentiating in adult teleost retina. Developments in Biologicals, 170, 136–141.
Mattson, M. P., & Klapper, W. (2001). Emerging roles for telomerase in neuronal development and apoptosis. Journal of Neuroscience Research, 63, 1–9.
Meyer, R. L. (1978). Evidence from thymidine labeling for continuing growth of retina and tectum in juvenile goldfish. Experimental Neurology, 59, 99–111.
Morin, G. B. (1989). The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell, 59, 521–529.
Otteson, D. C., D’Costa, A. R., & Hitchcock, P. F. (2001). Putative stem cells and the lineage of rod photoreceptors in the mature retina of the goldfish. Developments in Biologicals, 232, 62–76.
Otteson, D. C., & Hitchcock, P. F. (2003). Stem cells in the teleost retina: Persistent neurogenesis and injury-induced regeneration. Vision Research, 43, 927–936.
Reh, T. A., & Fischer, A. J. (2001). Stem cells in the vertebrate retina. Brain, Behavavior and Evolution, 58, 296–305.
Shay, J. W., & Bacchetti, S. (1997). A survey of telomerase activity in human cancer. European Journal of Cancer, 33, 787–791.
Shay, J. W., Werbin, H., & Wright, W. E. (1997). Telomerase assays in the diagnosis and prognosis of cancer. Ciba Foundation Symposium, 211, 148–155.
Tao, M., Miyano-Kurosaki, N., Takai, K., & Takaku, H. (1999). Specific inhibition of human telomerase activity by transfection reagent, FuGENE6-antisense phosphorothioate oligonucleotide complex in HeLa cells. FEBS Letters, 454, 312–316.
Urquidi, V., Tarin, D., & Goodison, S. (2000). Role of telomerase in cell senescence and oncogenesis. Annual Review of Medicine, 51, 65–79.
Wright, W. E., & Shay, J. W. (1992). Telomere positional effects and the regulation of cellular senescence. Trends in Genetics, 8, 193–197.
Yasumoto, S., Kunimura, C., Kikuchi, K., Tahara, H., Ohji, H., Yamamoto, H., et al. (1996). Telomerase activity in normal human epithelial cells. Oncogene, 13, 433–439.
Zhu, H., Fu, W., & Mattson, M. P. (2000). The catalytic subunit of telomerase protects neurons against amyloid beta-peptide-induced apoptosis. Journal of Neurochemistry, 75, 117–124.
Acknowledgements
This study was supported in part by grants from The University of Hong Kong (Seed Funding Programme for Basic Research) and the Research Grants Council of Hong Kong (7651/05M).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lau, B.W.M., Tsao, G.S.W., So, K.F. et al. Expression of Telomerase Reverse Transcriptase in Adult Goldfish Retina. J Mol Neurosci 32, 160–167 (2007). https://doi.org/10.1007/s12031-007-0031-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12031-007-0031-6