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Ontogeny of preproenkephalin mRNA expression in the rat retina

Published online by Cambridge University Press:  02 June 2009

Tomoki Isayama
Affiliation:
Department of Neuroscience and Anatomy, Milton S. Hershey Medical Center, Pennsylvania State University, College of Medicine, Hershey
Patricia J. McLaughlin
Affiliation:
Department of Neuroscience and Anatomy, Milton S. Hershey Medical Center, Pennsylvania State University, College of Medicine, Hershey
Ian S. Zagon
Affiliation:
Department of Neuroscience and Anatomy, Milton S. Hershey Medical Center, Pennsylvania State University, College of Medicine, Hershey

Abstract

Endogenous opioid systems (i.e. opioid peptides and opioid receptors) modulate developmental events in the neonatal mammalian retina. In the present study, the mRNA encoding preproenkephalin A (PPE), the prohormone for the opioid growth factor (OGF), [Met5]-enkephalin, was studied in the developing and the adult retinas of rats. Northern analysis indicated the presence of a 1.4-kb message in the developing and adult retinas corresponding to rat PPE mRNA. Quantitation showed that PPE message was present on postnatal day 1 at 5% of the adult level, and increased during development until the adult quantity was reached by postnatal day 27. In situ hybridization experiments first detected the presence of PPE mRNA in retinal tissues during late gestation. In late prenatal and neonatal retinas, PPE message was associated with areas of the developing retina containing proliferating neuroblasts and postmitotic cells. Later in development, message appeared to be located primarily within the inner retina, with abundant PPE mRNA associated with putative horizontal cells of the inner nuclear layer (INL). The adult retina showed a similar pattern of PPE gene expression in the cells of the INL. These findings document that the gene expression in the retina for PPE begins in the fetus, continues during retinal development, and coincides with the presence of a PPE mRNA derivative ([Met5]-enkephalin) that regulates DNA synthesis during retinal ontogeny. Our results are also the first to show the presence of PPE message in the adult mammalian retina, suggesting transcription of an opioid gene in the mature visual system.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Abe, H., Tooyama, I., Renda, T., Erspamer, V. & Kimura, H. (1994). Immunohistochemical demonstration of [D-Ala2]deltorphin-I in amacrine cells of rat retina. Peptides 15, 4954.Google Scholar
Altman, J. & Das, G.D. (1965). Postnatal origin of microneurones in the rat brain. Nature 207, 953956.CrossRefGoogle ScholarPubMed
Altschuler, R.A., Mosinger, J.L., Hoffman, D.W. & Parakkal, M.H. (1982). Immunocytochemical localization of enkephalin-like immunoreactivity in the retina of the guinea pig. Proceedings of the National Academy of Sciences of the U.S.A. 79, 23982400.CrossRefGoogle ScholarPubMed
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281302.CrossRefGoogle ScholarPubMed
Bugra, K., Oliver, L., Jacquemin, E., Laurent, M., Courtois, Y. & Hicks, D. (1993). Acidic fibroblast growth factor is expressed abundantly by photoreceptors within the developing and mature rat retina. European Journal of Neuroscience 5, 15861595.CrossRefGoogle ScholarPubMed
de la Rosa, E.J., Bondy, C.A., Hernandez-Sanchez, C., Wu, X., Zhou, J., Lopez-Carranza, A., Scavo, L.M. & de Pablo, F. (1994). Insulin and insulin-like growth factor system components gene expression in the chicken retina from early neurogenesis until late development and their effects on neuroepithelial cells. European Journal of Neuroscience 6, 18011810.CrossRefGoogle ScholarPubMed
Eldred, W.D. & Karten, H.J. (1983). Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin, and glucagon. Journal of Comparative Neurology 221, 371381.CrossRefGoogle ScholarPubMed
Grün, G. (1982). The development of the vertebrate retina: A comparative survey. Advances in Anatomy, Embryology, and Cell Biology 78, 183.Google ScholarPubMed
Hoffman, D.W. (1983). Chromatographic identification of enkephalins in the guinea pig retina. Neuroscience Letters 40, 6773.Google Scholar
Howells, R.D., Groth, J., Hiller, J.M. & Simon, E.J. (1980). Opiate binding sites in the retina: Properties and distribution. Journal of Pharmacology and Experimental Therapeutics 215, 6064.Google ScholarPubMed
Isayama, T., McLaughlin, P.J. & Zagon, I.S. (1991). Endogenous opioids regulate cell proliferation in the retina of developing rat. Brain Research 544, 7985.CrossRefGoogle ScholarPubMed
Isayama, T. & Zagon, I.S. (1991). Localization of preproenkephalin A mRNA in the neonatal rat retina. Brain Research Bulletin 27, 805808.Google Scholar
Isayama, T., Hurst, W.J., McLaughlin, P.J. & Zagon, I.S. (1995). Ontogeny of the opioid growth factor, [Met5]-Enkephalin, and its binding activity in the rat retina. Visual Neuroscience 12, 939950.Google Scholar
Keshet, E., Polakiewicz, R.D., Itin, A., Ornoy, A. & Rosen, H. (1989). Proenkephalin A is expressed in mesodermal lineages during organogenesis. EMBO Journal 8, 29172923.CrossRefGoogle ScholarPubMed
Kew, D. & Kilpatrick, D.L. (1990). Widespread organ expression of the rat proenkephalin gene during early postnatal development. Molecular Endocrinology 4, 337340.CrossRefGoogle ScholarPubMed
Koide, T., Takahashi, J.B., Hoshimaru, M., Kojima, M., Otsuka, T., Asahi, M. & Kikuchi, H. (1995). Localization of trkB and lowaffinity nerve growth factor receptor mRNA in the developing rat retina. Neuroscience Letters 185, 183186.CrossRefGoogle ScholarPubMed
LaGamma, E.F., Agarwal, B.L. & DeCristofaro, J.D. (1992). Regulation of adrenomedullary preproenkephalin mRNA: Effects of hypoglycemia during development. Molecular Brain Research 13, 189197.CrossRefGoogle Scholar
Meller, K. (1984). Morphological studies on the development of the retina. Progress in Retinal Research 3, 119.CrossRefGoogle Scholar
Meriney, S.D., Ford, M.J., Oliva, D. & Pilar, G. (1991). Endogenous opioids modulate neuronal survival in the developing avian ciliary ganglion. Journal of Neuroscience 11, 37053717.CrossRefGoogle ScholarPubMed
Molnar, M., Casini, G., Davis, B.M., Brecha, N.C. & Bagnoli, P. (1995). Preproenkephalin messenger RNA-containing amacrine cells in the chicken retina identified with in situ hybridization histochemistry. Visual Neuroscience 12, 185189.CrossRefGoogle ScholarPubMed
Polley, E.H., Zimmerman, R.P. & Fortney, R.L. (1989). Neurogenesis and maturation of cell morphology in the development of the mammalian retina. In Development of the Vertebrate Retina, ed. Finlay, B.L. & Sengelaub, D.R., pp. 329. New York: Plenum Press.CrossRefGoogle Scholar
Prada, C., Puga, J., Pérez-Méndez, L., López, R. & Ramírez, G. (1991). Spatial and temporal patterns of neurogenesis in the chick retina. European Journal of Neuroscience 3, 559569.CrossRefGoogle ScholarPubMed
Reese, B.E. & Colello, R.J. (1992). Neurogenesis in the retinal ganglion cell layer of the rat. Neuroscience 46, 419429.CrossRefGoogle ScholarPubMed
Rickman, D.W. & Brecha, N.C. (1995). Expression of the protooncogene, trk, receptors in the developing rat retina. Visual Neuroscience 12, 215222.CrossRefGoogle ScholarPubMed
Sidman, R.L. (1961). Histogenesis of mouse retina studied with thymidine-H3. In The Structure of the Eye, ed. Smelser, G.K., pp. 487506. New York: Academic Press.Google Scholar
Spence, S.G. & Robson, J.A. (1989). An autoradiographic analysis of neurogenesis in the chick retina in vitro and in vivo. Neuroscience 32, 801812.CrossRefGoogle ScholarPubMed
Stiene-Martin, A. & Hauser, K.F. (1990). Opioid-dependent growth of glial cultures: Suppression of astrocyte DNA synthesis by metenkephalin. Life Science 46, 9198.CrossRefGoogle ScholarPubMed
Tripathi, B.J., Tripathi, R.C., Livingston, A.M., & Borisuth, N.S.C. (1991). The role of growth factors in the embryogenesis and differentiation of the eye. American Journal of Anatomy 192, 442471.Google Scholar
Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1981). Autoradiographic localization of opioid receptors in the mammalian retina. Neuroscience Letters 27, 1924.CrossRefGoogle ScholarPubMed
Watt, C.B. (1989). Synaptic organization of enkephalinlike-immunoreactive amacrine cells in the goldfish retina. Journal of Comparative Neurology 283, 333341.CrossRefGoogle ScholarPubMed
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1985). Opioid pathways in an avian retina. II. Synaptic organization of enkephalin-immunoreactive amacrine cells. Journal of Neuroscience 5, 857865.CrossRefGoogle Scholar
Weisinger, G., DeCristofaro, J.D. & LaGamma, E.F. (1992). Tissueand treatment-specific usage of multiple preproenkephalin transcriptional start sites. Journal of Biological Chemistry 267, 45084512.CrossRefGoogle Scholar
Yoshikawa, K., Williams, C. & Sabol, S.L. (1984). Rat brain preproenkephalin mRNA. Journal of Biological Chemistry 259, 1430114308.CrossRefGoogle ScholarPubMed
Zagon, I.S., Isayama, T. & McLaughlin, P.J. (1994). Preproenkephalin mRNA expression in the developing and adult rat brain. Molecular Brain Research 21, 8598.Google Scholar
Zagon, I.S. & McLaughlin, P.J. (1993). Opioid growth factor receptor in the developing nervous system. In Receptors in the Developing Nervous System, Volume I. Growth Factors and Hormones, ed. Zagon, I.S. & McLaughlin, P.J., pp. 3962. London: Chapman and Hall.Google Scholar
Zagon, I.S. & McLaughlin, P.J. (1991). The role of endogenous opioids and opioid receptors in human and animal cancers. In Stress and Immunity, ed. Plotnikoff, N., Murgo, A., Faith, R. & Wybran, J., pp. 343355. Boca Raton, Florida: CRC Press, Inc.Google Scholar