Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1995 Nov 1;488(Pt 3):565–576. doi: 10.1113/jphysiol.1995.sp020990

GABA transport and calcium dynamics in horizontal cells from the skate retina.

L Haugh-Scheidt 1, R P Malchow 1, H Ripps 1
PMCID: PMC1156724  PMID: 8576848

Abstract

1. Changes in intracellular calcium concentration [Ca2+]i in response to extracellularly applied gamma-aminobutyric acid (GABA) were studied in isolated horizontal cells from the all-rod skate retina. 2. Calcium measurements were made using fura-2 AM, both with and without whole-cell voltage clamp. Superfusion with GABA, in the absence of voltage clamp, resulted in an increase in [Ca2+]i; the threshold for detection was approximately 50 microM GABA, and a maximal response was elicited by 500 microM GABA. 3. The rise in [Ca2+]i was not mimicked by baclofen nor was it blocked by phaclofen, picrotoxin or bicuculline. However, the GABA-induced [Ca2+]i increase was completely abolished when extracellular sodium was replaced with N-methyl-D-glucamine. 4. With the horizontal cell voltage clamped at -70 mV, GABA evoked a large inward current, but there was no concomitant change in [Ca2+]i. Nifedipine, which blocks L-type voltage-gated Ca2+ channels, suppressed the GABA-induced increase in [Ca2+]i. These findings suggest that the calcium response was initiated by GABA activation of sodium dependent electrogenic transport, and that the resultant depolarization led to the opening of voltage-gated Ca2+ channels, and a rise in [Ca2+]i. 5. The GABA-induced influx of calcium appears not to have been the sole source of the calcium increase. The GABA-induced rise in [Ca2+]i was reduced by dantrolene, indicating that internal Ca2+ stores contributed to the GABA-mediated Ca2+ response. 6. These observations demonstrate that activation of the GABA transporter induces changes in [Ca2+]i which may have important implications for the functional properties of horizontal cells.

Full text

PDF
566

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Agardh E., Bruun A., Ehinger B., Ekström P., van Veen T., Wu J. Y. Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. J Comp Neurol. 1987 Apr 22;258(4):622–630. doi: 10.1002/cne.902580411. [DOI] [PubMed] [Google Scholar]
  2. Brunken W. J., Witkovsky P., Karten H. J. Retinal neurochemistry of three elasmobranch species: an immunohistochemical approach. J Comp Neurol. 1986 Jan 1;243(1):1–12. doi: 10.1002/cne.902430102. [DOI] [PubMed] [Google Scholar]
  3. Cammack J. N., Schwartz E. A. Ions required for the electrogenic transport of GABA by horizontal cells of the catfish retina. J Physiol. 1993 Dec;472:81–102. doi: 10.1113/jphysiol.1993.sp019938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carvalho A. P., Bandeira-Duarte C., Ferreira I. L., Coutinho O. P., Carvalho C. M. Sodium-calcium exchange in nerve terminals. Influence on internal Ca2+ and neurosecretion. Ann N Y Acad Sci. 1991;639:300–311. doi: 10.1111/j.1749-6632.1991.tb17318.x. [DOI] [PubMed] [Google Scholar]
  5. Crow J. M., Atkinson M. M., Johnson R. G. Micromolar levels of intracellular calcium reduce gap junctional permeability in lens cultures. Invest Ophthalmol Vis Sci. 1994 Jul;35(8):3332–3341. [PubMed] [Google Scholar]
  6. De Erausquin G., Brooker G., Costa E., Wojcik W. J. Stimulation of high affinity gamma-aminobutyric acidB receptors potentiates the depolarization-induced increase of intraneuronal ionized calcium content in cerebellar granule neurons. Mol Pharmacol. 1992 Sep;42(3):407–414. [PubMed] [Google Scholar]
  7. Desmedt J. E., Hainaut K. Inhibition of the intracellular release of calcium by Dantrolene in barnacle giant muscle fibres. J Physiol. 1977 Feb;265(2):565–585. doi: 10.1113/jphysiol.1977.sp011731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Grynkiewicz G., Poenie M., Tsien R. Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985 Mar 25;260(6):3440–3450. [PubMed] [Google Scholar]
  9. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  10. Heidelberger R., Matthews G. Inhibition of calcium influx and calcium current by gamma-aminobutyric acid in single synaptic terminals. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7135–7139. doi: 10.1073/pnas.88.16.7135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hua S. Y., Nohmi M., Kuba K. Characteristics of Ca2+ release induced by Ca2+ influx in cultured bullfrog sympathetic neurones. J Physiol. 1993 May;464:245–272. doi: 10.1113/jphysiol.1993.sp019633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Keynan S., Kanner B. I. gamma-Aminobutyric acid transport in reconstituted preparations from rat brain: coupled sodium and chloride fluxes. Biochemistry. 1988 Jan 12;27(1):12–17. doi: 10.1021/bi00401a003. [DOI] [PubMed] [Google Scholar]
  13. Lamb T. D. Spatial properties of horizontal cell responses in the turtle retina. J Physiol. 1976 Dec;263(2):239–255. doi: 10.1113/jphysiol.1976.sp011630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lasater E. M., Dowling J. E., Ripps H. Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. J Neurosci. 1984 Aug;4(8):1966–1975. doi: 10.1523/JNEUROSCI.04-08-01966.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Leblanc N., Hume J. R. Sodium current-induced release of calcium from cardiac sarcoplasmic reticulum. Science. 1990 Apr 20;248(4953):372–376. doi: 10.1126/science.2158146. [DOI] [PubMed] [Google Scholar]
  16. Levi A. J., Brooksby P., Hancox J. C. A role for depolarisation induced calcium entry on the Na-Ca exchange in triggering intracellular calcium release and contraction in rat ventricular myocytes. Cardiovasc Res. 1993 Sep;27(9):1677–1690. doi: 10.1093/cvr/27.9.1677. [DOI] [PubMed] [Google Scholar]
  17. Linn C. P., Christensen B. N. Excitatory amino acid regulation of intracellular Ca2+ in isolated catfish cone horizontal cells measured under voltage- and concentration-clamp conditions. J Neurosci. 1992 Jun;12(6):2156–2164. doi: 10.1523/JNEUROSCI.12-06-02156.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Malchow R. P., Qian H. H., Ripps H., Dowling J. E. Structural and functional properties of two types of horizontal cell in the skate retina. J Gen Physiol. 1990 Jan;95(1):177–198. doi: 10.1085/jgp.95.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Malchow R. P., Ripps H. Effects of gamma-aminobutyric acid on skate retinal horizontal cells: evidence for an electrogenic uptake mechanism. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8945–8949. doi: 10.1073/pnas.87.22.8945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marshak D. W., Dowling J. E. Synapses of cone horizontal cell axons in goldfish retina. J Comp Neurol. 1987 Feb 15;256(3):430–443. doi: 10.1002/cne.902560310. [DOI] [PubMed] [Google Scholar]
  21. Naka K. I., Rushton W. A. The generation and spread of S-potentials in fish (Cyprinidae). J Physiol. 1967 Sep;192(2):437–461. doi: 10.1113/jphysiol.1967.sp008308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Naka K. I., Witkovsky P. Dogfish ganglion cell discharge resulting from extrinsic polarization of the horizontal cells. J Physiol. 1972 Jun;223(2):449–460. doi: 10.1113/jphysiol.1972.sp009857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Qian H., Dowling J. E. Novel GABA responses from rod-driven retinal horizontal cells. Nature. 1993 Jan 14;361(6408):162–164. doi: 10.1038/361162a0. [DOI] [PubMed] [Google Scholar]
  24. Qian H., Malchow R. P., Ripps H. Gap-junctional properties of electrically coupled skate horizontal cells in culture. Vis Neurosci. 1993 Mar-Apr;10(2):287–295. doi: 10.1017/s0952523800003680. [DOI] [PubMed] [Google Scholar]
  25. Qian H., Ripps H. Receptive field properties of rod-driven horizontal cells in the skate retina. J Gen Physiol. 1992 Sep;100(3):457–478. doi: 10.1085/jgp.100.3.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Reichling D. B., Kyrozis A., Wang J., MacDermott A. B. Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J Physiol. 1994 May 1;476(3):411–421. doi: 10.1113/jphysiol.1994.sp020142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rose B., Loewenstein W. R. Permeability of a cell junction and the local cytoplasmic free ionized calcium concentration: a study with aequorin. J Membr Biol. 1976 Aug 27;28(1):87–119. doi: 10.1007/BF01869692. [DOI] [PubMed] [Google Scholar]
  28. Sakai H. M., Naka K. Synaptic organization of the cone horizontal cells in the catfish retina. J Comp Neurol. 1986 Mar 1;245(1):107–115. doi: 10.1002/cne.902450108. [DOI] [PubMed] [Google Scholar]
  29. Schwartz E. A. Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. Science. 1987 Oct 16;238(4825):350–355. doi: 10.1126/science.2443977. [DOI] [PubMed] [Google Scholar]
  30. Slaughter M. M., Pan Z. H. The physiology of GABAB receptors in the vertebrate retina. Prog Brain Res. 1992;90:47–60. doi: 10.1016/s0079-6123(08)63608-0. [DOI] [PubMed] [Google Scholar]
  31. Sullivan J. M., Lasater E. M. Sustained and transient calcium currents in horizontal cells of the white bass retina. J Gen Physiol. 1992 Jan;99(1):85–107. doi: 10.1085/jgp.99.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Williams D. A., Fay F. S. Intracellular calibration of the fluorescent calcium indicator Fura-2. Cell Calcium. 1990 Feb-Mar;11(2-3):75–83. doi: 10.1016/0143-4160(90)90061-x. [DOI] [PubMed] [Google Scholar]
  33. Wu S. M. Synaptic transmission in the outer retina. Annu Rev Physiol. 1994;56:141–168. doi: 10.1146/annurev.ph.56.030194.001041. [DOI] [PubMed] [Google Scholar]
  34. Yau K. W., Nakatani K. Electrogenic Na-Ca exchange in retinal rod outer segment. Nature. 1984 Oct 18;311(5987):661–663. doi: 10.1038/311661a0. [DOI] [PubMed] [Google Scholar]
  35. Yazulla S., Kleinschmidt J. Carrier-mediated release of GABA from retinal horizontal cells. Brain Res. 1983 Mar 14;263(1):63–75. doi: 10.1016/0006-8993(83)91201-5. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES