Neurochemical Research

, Volume 18, Issue 9, pp 957–964 | Cite as

Effects of cell signaling on the development of GABA receptors in chick retina neurons

  • Bukhtiar H. Shah
  • Robert E. Hausman
Original Articles

Abstract

R-cognin, a cell recognition molecule, and insulin are known to play significant roles in GABAergic differentiation in the developing chick retina. In the present study, the effects of insulin and R-cognin on post-synaptic (GABAceptive) differentiation were investigated. In ovo binding of [3H]GABA and [3H]flunitrazepam ([3H]Flu) to the GABA and benzodiazepine (BZD) receptors, respectively, remained at low levels during early embryogenesis but increased sharply from mid-embryogenesis through hatching, increases which also occur in cultured neurons from early-embryonic (E7) and mid-embryonic (E11) chick retina. E7 neurons respond to insulin treatment (100 ng/ml) with increased [3H]Flu binding but no change in [3H]GABA binding. Cognin antibody (10 μg/ml) treatment of E7 neurons caused no significant inhibition of the developmental increases in binding of either radioligand. Insulin in E11 cultures led to greater developmental increases in binding sites for both radioligands, but exposure to cognin antibody was without significant effect. These data, along with previous studies, indicate that GABAergic differentiation in developing chick retina is regulated, in part, by insulin and cognin-mediated cell signaling. Insulin also regulates post-synaptic (GABAceptive) differentiation whereas cognin-mediated interactions are relatively insignificant.

Key Words

R-cognin cell contact insulin benzodiazepine 

Abbreviations

BZD

benzodiazepine

ChAT

choline acetyltransferase

Flu

flunitrazepam

GABA

γ-aminobutyric acid

GAD

glutamate decarboxylase (glutamic acid decarboxylase)

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References

  1. 1.
    Hausman, R. E., Sagar, G. D. V., and Shah, B. H. 1991. Initial cholinergic differentiation in embryonic chick retina is responsive to insulin and cell-cell interactions. Dev. Brain Res. 59:31–37.Google Scholar
  2. 2.
    Peterson, S. W., Kyriakis, J. M., and Hausman, R. E. 1986. Changes in insulin binding to developing embryonic chick neural retina cells. J. Neurochem. 47:851–855.PubMedGoogle Scholar
  3. 3.
    De Pablo, F., Scott, L. A., and Roth, J. 1990. Insulin and insulinlike growth factor I in early development: Peptides, receptors and biological events. Endocr. Rev., 11:558–577.PubMedGoogle Scholar
  4. 4.
    Meimaridis, D. G., Morse, D. E., Pansky, B., and Budd, G. C. 1990. Insulin immunoreactivity in the fetal and neonatal rat retina. Neurosci. Lett. 118:116–119.PubMedGoogle Scholar
  5. 5.
    Waldbillig, R. J., Arnold, D. R., Fletcher, R. T., and Chader, G. J. 1991. Insulin and IGF-I binding in developing chick neural retina and pigment epithelium: A characterization of binding and structural differences. Exp. Eye Res. 53:13–22.PubMedGoogle Scholar
  6. 6.
    Kyriakis, J. M., Hausman, R. E., and Peterson, S. W. 1987. Insulin stimulates choline acetyltransferase in the ganglion cell layer of developing chick neural retina. Proc. Natl. Acad. Sci. USA 84:7463–7467.PubMedGoogle Scholar
  7. 7.
    Shah, B. H., and Hausman, R. E. 1993. Effect of insulin on GABAergic development in the embryonic chick retina. Develop. Brain Res. (in press).Google Scholar
  8. 8.
    Hausman, R. E., and Moscona, A. A. 1975. Purification and characterization of the neural retina cell aggregating factor. Proc. Natl. Acad. Sci. USA 72:916–920.PubMedGoogle Scholar
  9. 9.
    Hausman, R. E., and Moscona, A. A. 1976. Isolation of retinaspecific cell aggregating factor from membranes of embryonic retina tissue. Proc. Natl. Acad. Sci. USA 73:3594–3598.PubMedGoogle Scholar
  10. 10.
    Dobi, E. T., Troccoli, N. M., and Hausman, R. E. 1986. Distribution of R-cognin in late embryonic and post-hatching chick retina. Invest. Ophthalmol. Vis. Sci. 27:323–329.PubMedGoogle Scholar
  11. 11.
    Dobi, E. T., Naya, F. J., and Hausman, R. E. 1988. Distribution of R-cognin and choline acetyltransferase in the ganglion cell layer of developing chick neural retina. Cell Differ. 22:115–124.PubMedGoogle Scholar
  12. 12.
    Sagar, G. D. V., Krishna Rao, A. S. M., Ren, Y., and Hausman, R. E. 1992. The cell recognition molecule, cognin, mediates choline acetyltransferase activity in embryonic chick retina. Brain Res. 585:63–70.PubMedGoogle Scholar
  13. 13.
    Shah, B. H., Krishna Rao, A. S. M., and Hausman, R. E. 1992. Role of the cell recognition molecule cognin, in GABAergic differentiation in chick retina. Brain Res. 589:268–274.PubMedGoogle Scholar
  14. 14.
    De Blas, A. L., Vitorica, J., and Friedrich, P. 1986. Localization of the GABA-A receptor in the rat brain with a monoclonal antibody to the 57,000 Mr peptide of the GABA-A receptor/benzodiazepine receptor/Cl channel complex. J. Neurosci. 8:602–614.Google Scholar
  15. 15.
    Vitorica, J., Park, D., Chin, G., and De Blas, A. L. 1988. Monoclonal antibodies and conventional antisera to the GABAA receptor/benzodiazepine receptor/Cl channel complex. J. Neurosci. 8:615–622.PubMedGoogle Scholar
  16. 16.
    Ewert, M., De Blas, A. L., Möhler, H., and Seeburg, P. H. 1992. A prominent epitope on GABAA receptors is recognized by two different monoclonal antibodies. Brain Res. 569:57–62.PubMedGoogle Scholar
  17. 17.
    Hausman, R. E., and Moscona, A. A. 1973. Cell surface interactions: Inhibition by proflavine of embryonic cell aggregation and the production of specific cell aggregating factor. Proc. Natl. Acad. Sci. USA. 70:3111–3114.PubMedGoogle Scholar
  18. 18.
    Hausman, R. E., Katz, M. S., Dobi, E. T., and Offermann, J. 1986. Cognin distribution during differentiation of embryonic chick retinal cells in vitro. Int. J. Devel. Neurosci. 4:537–544.Google Scholar
  19. 19.
    Hausman, R. E., and Moscona, A. A. 1979. Immunologic detection of retina cognin on the surface of embryonic cells. Exp. Cell. Res. 119:191–204.PubMedGoogle Scholar
  20. 20.
    Mehta, A. K., and Ticku, M. K. 1988. Developmental aspects of benzodiazepine receptors and GABA-gated chloride channels in primary cultures of spinal cord neurons. Brain Res. 454:156–163.PubMedGoogle Scholar
  21. 21.
    Hablitz, J. J., Tehrani, M. H. J., and Barnes, E. M. Jr. 1989. Chronic exposure of developing cortical neurons to GABA downregulates GABA/benzodiazepine receptors and GABA-gated chloride channels. Brain Res. 501:332–338.PubMedGoogle Scholar
  22. 22.
    Lloyd, K. G. 1986. GABA receptor binding, Pages 217–249,in A. A. Boulton, G. B. Baker, and P. D. Hrdina (eds), Neuromethods 4. Receptor Binding, Humana Press, Clifton, NJ.Google Scholar
  23. 23.
    Lewin, L., Mattsson, M.-O., and Sellström, Å. 1992. Inhibition of transporter mediated gamma-aminobutyric acid (GABA) release by SKF 89976-A, a GABA uptake inhibitor, studied in a primary neuronal culture from chicken. Neurochem. Res. 17:577–584.PubMedGoogle Scholar
  24. 24.
    Morgan, W. W. 1985. GABA: A potential neurotransmitter in retina, pp. 63–96,in W. W. Morgan (ed) Retinal transmitters and modulators: models for the brain. CRC Press, Boca Raton.Google Scholar
  25. 25.
    Scatchard, B. 1949. The attraction of proteins for small molecular ions. Ann. NY Acad. Sci. 51:660–672.Google Scholar
  26. 26.
    Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. R1-R4.Google Scholar
  27. 27.
    Tehrani, M. H. J., and Barnes, E. M. jr. 1986. Ontogeny of the GABA receptor complex in chick brain: studies in vivo and in vitro. Dev. Brain Res. 25:91–98.Google Scholar
  28. 28.
    Gravielle, M. C., and De Plazas, S. F. 1991. Benzodiazepine receptor sites in the chick optic lobe: development and pharmacological characterization. Neurochem. Res. 16:57–62.PubMedGoogle Scholar
  29. 29.
    Yazulla, S., Studholme, K. M., Vitorica, J., and De Blas, A. L. 1989. Immunocytochemical localization of GABAA receptors in goldfish and chicken retinas. J. Comp. Neurol. 280:15–26.PubMedGoogle Scholar
  30. 30.
    Jong, Y.-F., Thamphy, K. G., and Barnes, E. M. jr. 1986. Ontogeny of GABAergic neurons in chick brain. Dev. Brain Res. 25:83–90.Google Scholar
  31. 31.
    Kuriyama, K., Tomono, S., Kishi, M., Mukainaka, T., and Ohkuma, S. 1987. Development of γ-aminobutyric (GABA)ergic neurons in cerebral cortical neurons in primary culture. Brain Res. 416:7–21.PubMedGoogle Scholar
  32. 32.
    Barnes, E. M. jr. 1989. The biochemical development of GABA transmission, Pages 186–197,in P. Kellway and J. L. Noebels, (eds), Problems and Concepts in Developmental Neurophysiology, Johns Hopkins University Press, Baltimore.Google Scholar
  33. 33.
    Gonzàlez, N. N., Alfie, J., and De Plazas, S. F. 1990. Glutamic acid decarboxylase in different areas of the developing chick central nervous system. Neurochem. Res. 15:917–921.PubMedGoogle Scholar
  34. 34.
    Vitorica, J., Park, D., Chin, G., and De Blas, A. L. 1990. Characterization with antibodies of the γ-aminobutyric acidA/benzodiazepine receptor complex during development of the rat brain. J. Neurochem. 54:187–194.PubMedGoogle Scholar
  35. 35.
    Alstein, M., Dudai, Y., and Vogel, Z. 1981. Benzodiazepine receptors in chick retina: development and cellular localization. Brain Res. 206:198–202.PubMedGoogle Scholar
  36. 36.
    Coyle, J. T., and Enna, S. J. 1976. Neurochemical aspects of the ontogenesis of GABAergic neurons in the rat brain. Brain Res. 115:174–178.PubMedGoogle Scholar
  37. 37.
    Hausman, R. E. 1988. Retina cognin and cell differentiation, Pages 133–150,in S. R. Hilfer and J. B. Sheffield (eds), Cell interactions in visual development, Cell and Developmental Biology of the Eye. Proceedings of the 11th Symposium on Ocular Biology and Visual Development, Springer-Verlag, New York.Google Scholar
  38. 38.
    Sheffield, J. B., and Fischman, D. A. 1970. Intercellular junctions in the developing neural retina of chick embryos. Z. Zellforsch. 104:405–418.PubMedGoogle Scholar
  39. 39.
    Meinecke, D. L., and Rakic, P. 1990. Developmental expression of GABA and subunits of the GABAA receptor complex in an inhibitory synaptic circuit in the rat cerebellum. Dev. Brain Res. 55:73–86.Google Scholar
  40. 40.
    Gambarana, C., Pittman, R., and Siegel, R. E. 1990. Developmental expression of the GABAA receptor α1 subunit mRNA in the rat brain. J. Neurobiol. 21:1169–1179.PubMedGoogle Scholar
  41. 41.
    Frostholm, A., Zdilar, D., Chang, A., and Rotter, A. 1991. Stability of GABAA/benzodiazepine receptor α1 subunit mRNA expression in reeler mouse cerebellar Purkinje cells during postnatal development. Dev. Brain Res. 64:121–128.Google Scholar
  42. 42.
    Prichett, D., Sontheimer, H., Shivers, B. D., Ymer, S., Kettenman, H., Schofield, P. R., and Seeburg, P. 1989. Importance of a novel GABA-A receptor subunit for benzodiazepine pharmacology. Nature 338:582–585.PubMedGoogle Scholar
  43. 43.
    Zdilar, D., Rotter, A., and Frostholm, A. 1991. Expression of GABAA/benzodiazepine receptor α1-subunit nRNA and [3H] flunitrazepam binding sites during postnatal development of mouse cerebellum. Dev. Brain Res. 61:63–71.Google Scholar
  44. 44.
    Vitorica, J., Park, D., and De Blas, A. L. 1990. The GABAA/benzodiazepine receptor complex in rat brain neuronal cultures. Characterization by immunoprecipitation. Brain Res. 537:209–215.PubMedGoogle Scholar
  45. 45.
    De Mello, F. G., Bachrach, U., and Nirenberg, M. 1976. Ornithine and glutamic acid decarboxylase activities in the developing chick retina. J. Neurochem. 7:847–851.Google Scholar
  46. 46.
    Gleason, E., and Wilson, M. 1991. Chemical and electrical synapses formed by chick retinal neurons maintained in dissociated cell culture. Soc. Neurosci Abs. 1566.Google Scholar
  47. 47.
    Huba, R., and Hofmann, H.-D. 1990. Identification of GABAergic amacrine cell-like neurons developing in chick retinal monolayer cultures. Neurosci. Lett. 117:37–42.PubMedGoogle Scholar
  48. 48.
    Erdo, S. L., and Wolff, J. R. 1990. Gamma-aminobutyric acid outside the mammalian brain. J. Neurochem. 54:363–372.PubMedGoogle Scholar
  49. 49.
    Meier, E., Hertz, L., and Schousboe, A. 1991. Neurotransmitters as developmental signals. Neurochem. Int. 19:1–15.Google Scholar
  50. 50.
    Wolff, J. R., Joo, F., and Dames, W. 1978. Plasticity in dendrites shown by continuous GABA administration in superior cervical ganglion of adult rat. Nature 274:72–74.PubMedGoogle Scholar
  51. 51.
    Wolff, J. R., Joo, F., Dames, W., and Feher, O. 1979. Induction and maintenance of free postsynaptic membrane thickenings in the adult superior cervical ganglion. J. Neurocytol. 8:549–563.PubMedGoogle Scholar
  52. 52.
    Belhage, B., Damgaard, I., Saederup, E., Squires, R. F., and Schousboe, A. 1991. High- and low-affinity GABA-receptors in cultured cerebellar granule cells regulate transmitter release by different mechanisms. Neurochem. Int. 19:475–482.Google Scholar
  53. 53.
    Meier, E., Drejer, J., and Schousboe, A. 1984. The trophic effect of GABA on cerebellar granule cells is mediated by GABA-receptors. Int. J. Dev. Neurosci. 3:401–407.Google Scholar
  54. 54.
    Morgan, W. W., and Kamp, C. W. 1985. The demonstration of benzodiazepine binding sites and of pharmacologic effects of benzodiazepines in retina, Pages 97–106.in W. W. Morgan (ed), Retinal transmitters and modulators: models for the brain. CRC Press, Boca Raton.Google Scholar
  55. 55.
    Yazulla, S., and Brecha, N. 1981. Localized binding of 3H-muscimol to synapses in the chick retina. Proc. Natl. Acad. Sci. USA 78:643–647.PubMedGoogle Scholar
  56. 56.
    Young, W. S. III, and Kuhar, M. J. 1979. Autoradiographic localization of benzodiazepine receptors in the brains of humans and animals. Nature 280:393–396.Google Scholar
  57. 57.
    Brecha, N. C., Sternini, C., and Humphrey, M. F. 1991. Cellular distribution ofl-glutamate decarboxylase (GAD) and gamma-aminobutyric acidA (GABAA) receptor mRNAs in the retina. Cell. Mol. Neurobiol. 11:497–509.PubMedGoogle Scholar
  58. 58.
    Tehrani, M. H. J., and Barnes, E. M., Jr. 1991. Agonist-dependent internalization of gamma-aminobutyric acidA/benzodiazepine receptors in chick cortical neurons. J. Neurochem. 57:1307–1312.PubMedGoogle Scholar
  59. 59.
    Montpied, P., Ginns, E. I., Martin, B. M., Roca, D., Farb, D. H., and Paul, S. M. 1991. Gamma-aminobutyric acid (GABA) induces a receptor-mediated reduction in GABAA receptor α subunit messenger RNAs in embryonic chick neurons in culture. J. Biol. Chem. 266:6011–6014.PubMedGoogle Scholar
  60. 60.
    Tehrani, M. H. J., and Barnes, E. M., Jr. 1988. GABA downregulates the GABA/benzodiazepine receptor complex in developing cerebral neurons. Neurosci. Lett. 87:288–292.PubMedGoogle Scholar
  61. 61.
    Woods, J. D., and Davies, M. 1989. Regulation of the γ-aminobutyric acid receptor by γ-aminobutyric acid levels within the postsynaptic cell. J. Neurochem. 53:1648–1651.PubMedGoogle Scholar
  62. 62.
    Woods, J. D., and Davies, M. 1991. Regulation of the GABA-A receptor/ion channel complex by intracellular GABA levels. Neurochem. Res. 16:375–379.PubMedGoogle Scholar
  63. 63.
    Yang, C.-Y., Lin, Z.-S., and Yazulla, S. 1992. Localization of GABAA receptor subtypes in the tiger salamander retina. Visual Neurosci. 8:57–64.Google Scholar
  64. 64.
    Krishna Rao, A. S. M., and Hausman, R. E. 1991. Chiek retina cell recognition protein, cognin, is a multifunctional enzyme. J. Cell Biol. 115:70a.Google Scholar
  65. 65.
    Krishna Rao, A. S. M., and Hausman, R. E. 1992. Characterization of cDNA for the cell recognition molecule, R-cognin: homology with a multifunctional protein. Proc. Natl. Acad. Sci. USA 90 (in press).Google Scholar

Copyright information

© Plenum Publishing Corporation 1993

Authors and Affiliations

  • Bukhtiar H. Shah
    • 1
  • Robert E. Hausman
  1. 1.Department of BiologyBoston UniversityBoston

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