Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T23:07:53.515Z Has data issue: false hasContentIssue false

Preproenkephalin messenger RNA-containing amacrine cells in the chicken retina identified with in situ hybridization histochemistry

Published online by Cambridge University Press:  02 June 2009

Margherita Molnar
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy
Giovanni Casini
Affiliation:
Department of Environmental Sciences, Tuscia University, 01100 Viterbo, Italy
Brian M. Davis
Affiliation:
Department of Anatomy and Neurobiology, University of KentuckyMedical Center, Lexington
Nicholas C. Brecha
Affiliation:
Departments of Anatomy & Cell Biology and Medicine, Brain Research Institute, CURE: VA/UCLA Gastroenteric Biology Center, UCLA School of Medicine, and VAMC-West Los Angeles, Los Angeles
Paola Bagnoli
Affiliation:
Department of Physiology and Biochemistry, University of Pisa, 56123 Pisa, Italy

Abstract

Enkephalin peptides are present in the retina of several vertebrate species. In the avian retina, enkephalin immunoreactivity is primarily localized to a population of amacrine cells. In the present study, we determined the localization of cells expressing preproenkephalin (PPE) mRNA, which encodes the precursor of enkephalin peptides, in adult as well as in embryonic chicken retinas. The localization of PPE mRNA-expressing cells to the proximal inner nuclear layer (INL) in the adult chicken retina is similar to that of enkephalin-immunoreactive cells observed in previous studies, indicating that amacrine cells expressing PPE mRNA synthesize Met5- and Leu5-enkephalin peptides and related extended forms. Specific hybridization signal is absent in retinas at embryonic day (E) 11, but it is detected in retinas at E 15 and at hatching. PPE mRNA-expressing cells at these ages are located in the proximal INL, and they can be classified as amacrine cells on the basis of their soma size and laminar position. These findings confirm and extend previous observations on the presence of opioid peptides in amacrine cells of the chicken retina. The presence of PPE mRNA at embryonic ages, together with the evidence that enkephalins influence developmental processes, suggests that these peptides modulate retinal maturation in birds.

Type
Short Communications
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschuler, R.A., Mostnger, J.W., Hoffman, D.W. & Parakkal, M.H. (1982). Immunocytochemical localization of enkephalin-like immunoreactivity in the retina of guinea pig. Proceedings of the National Academy of Sciences of the U.S.A. 78, 23982400.CrossRefGoogle Scholar
Boelen, M.K., Wellard, J., Dowton, M., Chubb, I.W. & Morgan, I.G. (1991). Glycinergic control of [Leu5] enkephalin levels in chicken retina. Brain Research 557, 221226.CrossRefGoogle ScholarPubMed
Boelen, M.K., Dowton, M. & Morgan, I.G. (1993). [Leu5] enkephalin-like immunoreactive amacrine cells are under nicotinic excitatory control during darkness in the chicken retina. Brain Research 624, 137142.CrossRefGoogle ScholarPubMed
Boelen, M.K., Wellard, J., Dowton, M. & Morgan, I.G. (1994). Endogenous dopamine inhibits the release of enkephalin-like immunoreactivity from amacrine cells in the chicken retina in the light. Brain Research 645, 240246.CrossRefGoogle ScholarPubMed
Brecha, N.C. (1983). Retinal neurotransmitters: histochemical and biochemical studies. In Chemical Neuroanatomy, ed. Emson, P.C., pp. 85129. New York: Raven Press.Google Scholar
Brecha, N., Karten, H.J. & Laverack, C. (1979). Enkephalin-containing amacrine cells in the avian retina: Immunohistochemical localization. Proceedings of the National Academy of Sciences of the U.S.A. 76, 30103014.CrossRefGoogle ScholarPubMed
Brecha, N.C., Eldred, W., Kullts, R.O. & Karten, H.J. (1984). Identification and localization of biologically active peptides in the vertebrate retina. In Progress in Retinal Research, Vol. 3, ed. Osborne, N. & Chader, J., pp. 185226. Oxford and New York: Pergamon Press.Google Scholar
Brecha, N.C., Sternini, C., Anderson, K. & Krause, J.E. (1989). Expression and cellular localization of substance P/neurokinin A and neurokinin B m RNAs in the rat retina. Visual Neuroscience 3, 527535.CrossRefGoogle Scholar
Britto, L.R.G. & Hamassaki-Britto, D.E. (1992). Enkephalin-immunoreactive ganglion cells in the pigeon retina. Visual Neuroscience 9, 389398.CrossRefGoogle ScholarPubMed
Coulombre, A.J. (1955). Correlations of structural and biochemical changes in the developing retina of the chick. American Journal of Anatomy 96, 153159.CrossRefGoogle ScholarPubMed
Davila-Garcia, M.I. & Azmitia, E.C. (1989). Effect of acute and chronic administration of Leu-enkephalin on cultured serotonergic neurons: Evidence for opioids as inhibitory neuronal growth factors. Developmental Brain Research 49, 97103.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A., Stell, W.K., Chin, C.A. & Lam, D.M.-K. (1981). An opiate system in the goldfish retina. Nature 292, 620623.CrossRefGoogle ScholarPubMed
Dowton, M., Boelen, M.K., Morgan, I.G. & Chubb, I.W. (1990). Light inhibits the release of both [Met5] enkephalin and [Met5] enkephalin-containing peptides in chicken retina, but not their synthesis. Neuroscience 38, 187193.CrossRefGoogle ScholarPubMed
Fisher, L.J. (1981). Synaptic development in chicken retina. Investigative Ophthalmology and Visual Science (Suppl.) 20, 203.Google Scholar
Gall, C., Brecha, N.C. & Parnavelas, J.G. (1984). Development of peptide immunoreactivity in the hippocampus, visual cortex and retina. In Organizing Principles of Neural Development, ed. Sharma, S.C., pp. 205249. New York: Plenum Press.CrossRefGoogle Scholar
Garner, L.K., Mendelson, B., Albers, K.M., Kindy, M., Overbeck, T.L. & Davis, B.M. (1994). Ontogeny and effect of activity on pro-enkephalin mRNA expression during development of the chick spinal cord. Journal of Comparative Neurology 347, 3646.CrossRefGoogle ScholarPubMed
Hauser, K.F., McLaughlin, P.J. & Zagon, I.S. (1989). Endogenous opioid system and the regulation of dendritic growth and spine formation. Journal of Comparative Neurology 281, 1322.CrossRefGoogle ScholarPubMed
Hughes, W.F. & La Velle, A. (1974). On the synaptogenesis sequence in the chick retina. Anatomical Record 179, 297302.CrossRefGoogle Scholar
Humbert, J., Pradelles, P., Gross, C. & Dray, F. (1979). Enkephalin-like products in embryonic chicken retina. Neuroscience Letters 12, 259263.CrossRefGoogle ScholarPubMed
Isayama, T., McLaughlin, P. & Zagon, I.S. (1991). Endogenous opioids regulate cell proliferation in the retina of developing rat. Brain Research 544, 7985.CrossRefGoogle ScholarPubMed
Millar, T.J., Saltpan, N., Oliver, J.O., Morgan, I.G. & Chubb, I.W. (1984). The concentration of enkephalin-like material in the chick retina is light dependent. Neuroscience 13, 221226.CrossRefGoogle ScholarPubMed
Prada, C., Puga, J., Perez-Méndez, L., Lopez, R. & Ramirez, G. (1991). Spatial and temporal patterns of neurogenesis in the chick retina. European Journal of Neuroscience 3, 559569.CrossRefGoogle ScholarPubMed
Slaughter, M.M., Mattler, J.A. & Gottlieb, D.I. (1985). Opiate binding sites in the chick, rabbit, and goldfish retina. Brain Research 339, 3947.CrossRefGoogle ScholarPubMed
Sternini, C., Anderson, K., Frantz, G., Krause, J.E. & Brecha, N.C. (1989). Expression of substance P/neurokinin A-encoding preprotachykinin messenger ribonucleic acids in the rat enteric nervous system. Gastroenterology 97, 348356.CrossRefGoogle ScholarPubMed
Su, Y.-Y.T., Watt, C.B. & Lam, D.M.-K. (1984). An enkephalin systern in an avian retina: Receptor binding and physiological studies. Investigative Ophthalmology and Visual Science (Suppl.) 25, 292.Google Scholar
Umino, O. & Dowlinc, J.E. (1991). Dopamine release from interplexiform cells in the retina: Effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity. Journal of Neuroscience 11, 30343046.CrossRefGoogle ScholarPubMed
Watt, C.B., Su, Y.Y.-T. & Lam, D.M.-K. (1984). Interaction between enkephalin and GABA in an avian retina. Nature (London) 311, 761763.CrossRefGoogle Scholar
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1985 a). Enkephalins in the vertebrate retina. In Progress in Retinal Research, Vol. 4, ed. Osborne, N. & Chader, J., pp. 221242. Oxford and New York: Pergamon Press.Google Scholar
Watt, C.B., Su, Y.-Y.T. & Lam, D.M.-K. (1985 b). Opioid pathways in an avian retina. II. Synaptic organization of enkephalin-immunoreactive amacrine cells. Journal of Neuroscience 5, 857865.CrossRefGoogle Scholar
Watt, C.B., Li, T., Lam, D.M.-K. & Wu, S.M. (1987). Interaction between enkephalin and -y-aminobutyric acid in the larval tiger salamander retina. Brain Research 408, 258262.CrossRefGoogle Scholar
Watt, C.B. & Su, Y.-Y.T. (1988). Enkephalinergic pathways in the retina. In Proceedings of the Retina Research Foundation Symposium, Vol. 1, ed. Lam, D.M.K., pp. 141161. Texas: Houston Portfolio Publishing Co.Google Scholar
Watt, C.B. & Florak, V.J. (1993). Colocalization of enkephalin and glycine in amacrine cells of the chicken retina. Brain Research 628, 349355.CrossRefGoogle ScholarPubMed
Watt, C.B. & Florak, V.J. (1994). A triple-label analysis demonstrating that enkephalin-, somatostatin-, and neurotensin-like immuno-reactivities are expressed by a single population of amacrine cells in the chicken retina. Brain Research 634, 310316.CrossRefGoogle Scholar
Watt, C.B. & Glazebrook, P.A. (1994). Interaction between enkephalin and -γ-aminobutyric acid in the chicken retina: A double-label immunoelectron microscopic analysis. Journal of Comparative Neurology 342, 378388.CrossRefGoogle Scholar
Zagon, I.S. & McLaughlin, P.J. (1987). Endogenous opioid systems regulate cell proliferation in the developing rat brain. Brain Research 412, 6872.CrossRefGoogle ScholarPubMed