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Ontogeny of the opioid growth factor, [Met5]-enkephalin, and its binding activity in the rat retina

Published online by Cambridge University Press:  02 June 2009

Tomoki Isayama ,
W. Jeffrey Hurst ,
Patricia J. McLaughlin  and
Ian S. Zagon
Tomoki Isayama
Affiliation:
Department of Neuroscience and Anatomy, The Pennsylvania State University, The Milton S. Hershey Medical Center, Hershey
W. Jeffrey Hurst
Affiliation:
Department of Comparative Medicine, The Pennsylvania State University, The Milton S. Hershey Medical Center, Hershey
Patricia J. McLaughlin
Affiliation:
Department of Neuroscience and Anatomy, The Pennsylvania State University, The Milton S. Hershey Medical Center, Hershey
Ian S. Zagon
Affiliation:
Department of Neuroscience and Anatomy, The Pennsylvania State University, The Milton S. Hershey Medical Center, Hershey
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Abstract

The endogenous opioid peptide [Met5]-enkephalin is a tonically active opioid growth factor (OGF) with an inhibitory action on DNA synthesis in the developing rat retina. In this study, the ontogeny of the spatial and temporal expression of OGF and its binding activity was examined. OGF-like immunoreactivity was detected in the retina at gestation day (E) 20, but not at E18, and was localized to ganglion cell and neuroblast layers; immunochemical reaction was no longer seen in the retina by postnatal day 6. Native OGF was further identified and characterized by high-performance liquid chromatography (HPLC) studies and immunodot assays, which revealed that [Met5]-enkephalin was present in the neonatal, but not adult, rat retina. OGF binding activity was detected as early as E18 using [125I]-[Met5]-enkephalin and in vitro receptor autoradiography. Little OGF binding activity was noted for prenatal retinas, but appreciable activity was observed from birth to postnatal day 4; no OGF binding could be detected after postnatal day 5 or in the adult. These results reveal the transient appearance of the OGF, [Met5]-enkephalin, and its receptor binding activity in the developing mammalian retina, and show that their ontogeny coincides with the timetable of DNA synthesis of retinal neuroblasts.

Keywords

DevelopmentGrowth factorOpioidOpioid receptorRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 939 - 950
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

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, 2398–2400.CrossRefGoogle ScholarPubMed
Anchan, R.M., Reh, T.A., Angello, J., Balliet, A. & Walker, M. (1991). EGF and TGF-α stimulate retinal neuroepithelial cell proliferation in vitro. Neuron 6, 923–936.Google Scholar
Ault, S.J. & Leventhal, A.G. (1994). Postnatal development of different classes of cat retinal ganglion cells. Journal of Comparative Neurology 339, 106–116.Google Scholar
Bassnett, S. & Beebe, D.C. (1990). Localization of insulin-like growth factor-1 binding sites in the embryonic chicken eye. Investigative Ophthalmology and Visual Science 31, 1637–1643.Google ScholarPubMed
Braekevelt, C.R. & Hollenberg, M.J. (1970). The development of the retina of the albino rat. American Journal of Anatomy 127, 281–302.Google Scholar
Carmignoto, G., Comelli, M.C., Candeo, P., Cavicchioli, L., Yan, Q., Merighi, A. & Maffei, L. (1991). Expression of NGF receptor and NGF receptor mRNA in the developing and adult rat retina. Experimental Neurology 111, 302–311.CrossRefGoogle ScholarPubMed
Connolly, S.E., Hjelmeland, L.M. & LaVail, M.M. (1992). Immuno-histochemical localization of basic fibroblast growth factor in mature and developing retinas of normal and RCS rats. Current Eye Research 11, 1005–1017.CrossRefGoogle Scholar
Consigli, S.A., Lyser, K.M. & Joseph-Silverstein, J. (1993). The temporal and spatial expression of basic fibroblast growth factor during ocular development in the chicken. Investigative Ophthalmology and Visual Science 34, 559–566.Google ScholarPubMed
Dunlop, S.A. (1990). Early development of retinal ganglion cell dendrites in the marsupial Setonix brachyurus, Quokka. Journal of Comparative Neurology 293, 425–447.Google Scholar
Ebendal, T. & Persson, H. (1988). Detection of nerve growth factor mRNA in the developing chicken embryo. Development 102, 101–106.CrossRefGoogle ScholarPubMed
Gao, H. & Hollyfield, J.G. (1992). Basic fibroblast growth factor (bFGF) immunolocalization in the rodent outer retina demonstrated with an anti-rodent bFGF antibody. Brain Research 585, 355–360.CrossRefGoogle ScholarPubMed
Grün, G. (1982). The development of the vertebrate retina: A comparative survey. Advances in Anatomy, Embryology, and Cell Biology 78, 1–83.CrossRefGoogle ScholarPubMed
Hansson, H.-A., Holmgren, A., Norstedt, G. & Rozell, B. (1989). Changes in the distribution of insulin-like growth factor I, thioredoxin, thioredoxin reductase and ribonucleotide reductase during the development of the retina. Experimental Eye Research 48, 411–420.Google Scholar
Harman, A.M. & Ferguson, J. (1994). Morphology and birth dates of horizontal cells in the retina of a marsupial. Journal of Comparative Neurology 340, 392–404.Google Scholar
Hendrickson, A. & Drucker, D. (1992). The development of parafoveal and mid-peripheral human retina. Behavioral Brain Research 49, 21–31.Google Scholar
Hermes, B., Reuss, S. & Vollrath, L. (1992). Synaptic ribbons, spheres and intermediate structures in the developing rat retina. International Journal of Developmental Neuroscience 10, 215–223.Google Scholar
Heuer, J.G., von Bartheld, C.S., Kinoshita, Y., Evers, P.C. & Both-well, M. (1990). Alternating phases of FGF receptor and NGF receptor expression in the developing chicken nervous system. Neuron 5, 283–296.CrossRefGoogle ScholarPubMed
Hicks, D. & Courtois, Y. (1992). Fibroblast growth factor stimulates photoreceptor differentiation in vitro. Journal of Neuroscience 12, 2022–2033.CrossRefGoogle ScholarPubMed
Hoffman, D.W. (1983). Chromatographic identification of enkephalins in the guinea pig retina. Neuroscience Letters 40, 67–73.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, 60–64.Google Scholar
Isayama, T., McLaughlin, P.J. & Zagon, I.S. (1991). Endogenous opioids regulate cell proliferation in the retina of developing rat. Brain Research 544, 79–85.CrossRefGoogle ScholarPubMed
Isayama, T. & Zagon, I.S. (1991). Localization of preproenkephalin A mRNA in the neonatal rat retina. Brain Research Bulletin 27, 805–808.CrossRefGoogle ScholarPubMed
LaVail, M.M., Rapaport, D.H. & Rakic, P. (1991). Cytogenesis in the monkey retina. Journal of Comparative Neurology 309, 86–114.Google Scholar
Layer, P.G., Alber, R., Mansky, P., Vollmer, G. & Willbold, E. (1990). Regeneration of a chimeric retina from single cells in vitro: Cell-lineage-dependent formation of radial cell columns by segregated chick and quail cells. Cell and Tissue Research 259, 187–198.Google Scholar
Lee, W.-H., Javedan, S. & Bondy, C.A. (1992). Coordinate expression of insulin-like growth factor system components by neurons and neuroglia during retinal and cerebellar development. Journal of Neuroscience 12, 4737–4744.CrossRefGoogle ScholarPubMed
Lillien, L. & Cepko, C. (1992). Control of proliferation in the retina: Temporal changes in responsiveness to FGF and TGFα. Development 115, 253–266.CrossRefGoogle Scholar
Mascarelli, F, Raulais, D., Counis, M.F. & Courtois, Y. (1987). Characterization of acidic and basic fibroblast growth factors in brain, retina and vitreous chick embryo. Biochemical and Biophysical Research Communications 146, 478–486.CrossRefGoogle ScholarPubMed
Meller, K. (1984). Morphological studies on the development of the retina. Progress in Retinal Research 3, 1–19.CrossRefGoogle Scholar
Morest, D.K. (1970). The pattern of neurogenesis in the retina of the rat. Zeitschrift fur Anatomie und Entwicklungs-Geschichte 131, 45–67.Google Scholar
Park, C.M. & Hollenberg, M.J. (1989). Basic fibroblast growth factor induces retinal regeneration in vivo. Developmental Biology 134, 201–205.CrossRefGoogle ScholarPubMed
Park, C.M. & Hollenberg, M.J. (1993). Growth factor-induced retinal regeneration in vivo. International Review of Cytology 146, 49–74.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. 3–29. New York: Plenum Press.CrossRefGoogle Scholar
Prada, C, Medina, J.I., López Génis-Gálvez, J.M. & Prada, F.A. (1992). Development of retinal displaced ganglion cells in the chick: Neurogenesis and morphogenesis. Journal of Neuroscience 12, 3781–3788.CrossRefGoogle ScholarPubMed
Rapaport, D.H. & Vietri, A.J. (1991). Identity of cells produced by two stages of cytogenesis in the postnatal cat retina. Journal of Comparative Neurology 312, 341–352.Google Scholar
Reese, B.E. & Colello, R.J. (1992). Neurogenesis in the retinal ganglion cell layer of the rat. Neuroscience 46, 419–429.Google Scholar
Reese, B.E., Thompson, W.F. & Peduzzi, J.D. (1994). Birthdates of neurons in the retinal ganglion cell layer of the ferret. Journal of Comparative Neurology 341, 464–475.Google Scholar
Reichenbach, A., Schnitzer, J., Friedrich, A., Ziegert, W., Brückner, G. & Schober, W. (1991). Development of the rabbit retina. I. Size of eye and retina, and postnatal cell proliferation. Anatomy and Embryology 183, 287–297.Google ScholarPubMed
Rhodes, R.H. (1979). A light microscopic study of the developing human neural retina. American Journal of Anatomy 154, 195–210.Google Scholar
Sanyal, S. & Bal, A.K. (1973). Comparative light and electron microscopic study of retinal histogenesis in normal and rd mutant mice. Zeitschrift fur Anatomie und Entwicklungs-Geschichte 142, 219–238.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. 487–506. 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, 801–812.CrossRefGoogle ScholarPubMed
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: An autoradiographic study. Journal of Embryology and Experimental Morphology 26, 67–79.Google ScholarPubMed
Tcheng, M., Oliver, L., Courtois, Y. & Jeanny, J.-C. (1994). Effects of exogenous FGFs on growth, differentiation, and survival of chick neural retina cells. Experimental Cell Research 212, 30–35.Google Scholar
Tesoriere, G., Vento, R., Calvaruso, G., Taibi, G. & Giuliano, M. (1992). Identification of insulin in chick embryo retina during development and its inhibitory effect on DNA synthesis. Journal of Neurochemistry 58, 1353–1359.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, 442–471.CrossRefGoogle ScholarPubMed
Turner, D.L., Snyder, E.Y. & Cepko, C.L. (1990). Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4, 833–845.Google Scholar
Van Driel, D., Provis, J.M. & Billson, F.A. (1990). Early differentiation of ganglion, amacrine, bipolar, and Muller cells in the developing fovea of human retina. Journal of Comparative Neurology 291, 203–219.CrossRefGoogle ScholarPubMed
Wamsley, J.K., Palacios, J.M. & Kuhar, M.J. (1981). Autoradiographic localization of opioid receptors in the mammalian retina. Neuroscience Letters 27, 19–24.CrossRefGoogle ScholarPubMed
Wanaka, A., Milbrandt, J. & Johnson, E.M. (1991). Expression of FGF receptor gene in rat development. Development 111, 455–468.CrossRefGoogle ScholarPubMed
Weidman, T.A. & Kuwabara, T. (1969). Development of the rat retina. Investigative Ophthalmology 8, 60–69.Google ScholarPubMed
Williams, R.W. & Goldowitz, D. (1992). Structure of clonal and polyclonal arrays in chimeric mouse retina. Proceedings of the National Academy of Sciences of the U.S.A. 89, 1184–1188.CrossRefGoogle ScholarPubMed
Yew, D.T., Luo, C.B., Zheng, D.R., Guan, Y.L., Tsang, D. & Stadlin, A. (1991). Immunohistochemical localization of substance P, enkephalin and serotonin in the developing human retina. Journal fur Hirnforschung 32, 61–67.Google ScholarPubMed
Young, R.W. (1983). Cell differentiation in the retina of the mouse. Anatomical Record 212, 199–205.Google Scholar
Zagon, I.S., Goodman, S.R. & McLaughlin, P.J. (1989). Characterization of zeta (ζ): A new opioid receptor involved in growth. Brain Research 482, 297–305.CrossRefGoogle ScholarPubMed
Zagon, I.S., Goodman, S.R. & McLaughlin, P.J. (1990). Demonstration and characterization of zeta (ζ), a growth-related opioid receptor, in a neuroblastoma cell line. Brain Research 511, 181–186.CrossRefGoogle Scholar
Zagon, I.S., Isayama, T. & McLaughlin, P.J. (1994). Preproenkeph-alin mRNA expression in the developing and adult rat brain. Molecular Brain Research 21, 85–98.Google Scholar
Zagon, I.S. & McLaughlin, P.J. (1983). Increased brain size and cellular content in infant rats treated with an opiate antagonist. Science 221, 1179–1180.CrossRefGoogle ScholarPubMed
Zagon, l.S. & McLaughlin, P.J. (1991). Identification of opioid peptides regulating proliferation of neurons and glia in the developingnervous system. Brain Research 542, 318–323.Google Scholar
Zagon, I.S. & McLaughlin, P.J. (1992). An opioid growth factor regulates the replication of microorganisms. Life Sciences 50, 1179–1187.CrossRefGoogle ScholarPubMed
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. 39–62. London, England: Chapman and Hall.Google Scholar
Zagon, I.S., Rhodes, R.E. & McLaughlin, P.J. (1985). Localization of enkephalin immunoreactivity in germinative cells of developingrat cerebellum. Science 227, 1049–1051.CrossRefGoogle Scholar
Zanellato, A., Comelli, M.C., Toso, R.D. & Carmignoto, G. (1993). Developing rat retinal ganglion cells express the functional NGF receptor p140lrkA. Developmental Biology 159, 105–113.Google Scholar