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. 1989 Nov;418:379–396. doi: 10.1113/jphysiol.1989.sp017847

Calcium channels in solitary retinal ganglion cells from post-natal rat.

A Karschin 1, S A Lipton 1
PMCID: PMC1189978  PMID: 2559971

Abstract

1. Calcium currents from identified, post-natal retinal ganglion cell neurones from rat were studied with whole-cell and single-channel patch-clamp techniques. Na+ and K+ currents were suppressed with pharmacological agents, allowing isolation of current carried by either 10 mM-Ca2+ or Ba2- during whole-cell recordings. For cell-attached patch recordings, the recording pipette contained 96-110 mM-BaCl2 while the bath solution consisted of isotonic potassium aspartate in order to zero the neuronal membrane potential. 2. A transient component, present in approximately one-third of the whole-cell recordings resembles closely the T-type calcium current observed previously in other tissues. This component activates at low voltages (-40 to -50 mV from holding potentials negative to -80 mV), inactivates with a time constant of 10-30 ms at 35 degrees C, and is carried equally well by Ba2+ or Ca2+. In single-channel recordings small (8 pS) channels are observed whose aggregate microscopic kinetics correspond well to the macroscopic current obtained during whole-cell measurements. 3. During whole-cell recordings, a more prolonged component activates in all retinal ganglion cells at -40 to -20 mV from a holding potential of -90 mV. This component is substantially larger when equimolar Ba2+ replaces Ca2+ as the charge carrier, and is sensitive to the dihydropyridine agonist Bay K8644 (5 microM) and antagonists nifedipine (1-10 microM) and nimodipine (1-10 microM). Thus, the dihydropyridine pharmacology of this prolonged component resembles that of the L-type calcium current found in dorsal root ganglion neurones and in heart cells. Also reminiscent of the L-current, the prolonged component in this preparation is less inactivated at depolarized holding potentials (-60 to -40 mV) than the transient component. In cell-attached recordings, large (20 pS) channels are observed with activation properties similar to those of the prolonged portion of the whole-cell current. 4. omega-Conotoxin fraction GVIA (omega-CgTX VIA), a peptide from the venom of the snail Conus geographus, produces a readily reversible blockade of all components of the calcium current in these central mammalian neurones. This finding is in contrast to that of other preparations in which this toxin is responsible for an ephemeral block of T-current but a long-lasting block of other components of calcium current. 5. In summary, at least two components of calcium current with discrete underlying unitary events are present in post-natal retinal ganglion cells from rat. One component closely resembles the T or transient current observed in other cell types.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Bean B. P. Classes of calcium channels in vertebrate cells. Annu Rev Physiol. 1989;51:367–384. doi: 10.1146/annurev.ph.51.030189.002055. [DOI] [PubMed] [Google Scholar]
  2. Bean B. P. Nitrendipine block of cardiac calcium channels: high-affinity binding to the inactivated state. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6388–6392. doi: 10.1073/pnas.81.20.6388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown A. M., Kunze D. L., Yatani A. Dual effects of dihydropyridines on whole cell and unitary calcium currents in single ventricular cells of guinea-pig. J Physiol. 1986 Oct;379:495–514. doi: 10.1113/jphysiol.1986.sp016266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Byerly L., Yazejian B. Intracellular factors for the maintenance of calcium currents in perfused neurones from the snail, Lymnaea stagnalis. J Physiol. 1986 Jan;370:631–650. doi: 10.1113/jphysiol.1986.sp015955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carbone E., Lux H. D. A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys J. 1984 Sep;46(3):413–418. doi: 10.1016/S0006-3495(84)84037-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carbone E., Lux H. D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature. 1984 Aug 9;310(5977):501–502. doi: 10.1038/310501a0. [DOI] [PubMed] [Google Scholar]
  7. Carbone E., Lux H. D. Kinetics and selectivity of a low-voltage-activated calcium current in chick and rat sensory neurones. J Physiol. 1987 May;386:547–570. doi: 10.1113/jphysiol.1987.sp016551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cruz L. J., Olivera B. M. Calcium channel antagonists. Omega-conotoxin defines a new high affinity site. J Biol Chem. 1986 May 15;261(14):6230–6233. [PubMed] [Google Scholar]
  9. Fishman M. C., Spector I. Potassium current suppression by quinidine reveals additional calcium currents in neuroblastoma cells. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5245–5249. doi: 10.1073/pnas.78.8.5245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fox A. P., Krasne S. Two calcium currents in Neanthes arenaceodentatus egg cell membranes. J Physiol. 1984 Nov;356:491–505. doi: 10.1113/jphysiol.1984.sp015479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fox A. P., Nowycky M. C., Tsien R. W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol. 1987 Dec;394:149–172. doi: 10.1113/jphysiol.1987.sp016864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fox A. P., Nowycky M. C., Tsien R. W. Single-channel recordings of three types of calcium channels in chick sensory neurones. J Physiol. 1987 Dec;394:173–200. doi: 10.1113/jphysiol.1987.sp016865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hagiwara N., Irisawa H., Kameyama M. Contribution of two types of calcium currents to the pacemaker potentials of rabbit sino-atrial node cells. J Physiol. 1988 Jan;395:233–253. doi: 10.1113/jphysiol.1988.sp016916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hagiwara S., Ozawa S., Sand O. Voltage clamp analysis of two inward current mechanisms in the egg cell membrane of a starfish. J Gen Physiol. 1975 May;65(5):617–644. doi: 10.1085/jgp.65.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Hess P., Lansman J. B., Tsien R. W. Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists. Nature. 1984 Oct 11;311(5986):538–544. doi: 10.1038/311538a0. [DOI] [PubMed] [Google Scholar]
  17. Hirning L. D., Fox A. P., McCleskey E. W., Olivera B. M., Thayer S. A., Miller R. J., Tsien R. W. Dominant role of N-type Ca2+ channels in evoked release of norepinephrine from sympathetic neurons. Science. 1988 Jan 1;239(4835):57–61. doi: 10.1126/science.2447647. [DOI] [PubMed] [Google Scholar]
  18. Kasai H., Aosaki T., Fukuda J. Presynaptic Ca-antagonist omega-conotoxin irreversibly blocks N-type Ca-channels in chick sensory neurons. Neurosci Res. 1987 Feb;4(3):228–235. doi: 10.1016/0168-0102(87)90014-9. [DOI] [PubMed] [Google Scholar]
  19. Kostyuk P. G., Shuba YaM, Savchenko A. N. Three types of calcium channels in the membrane of mouse sensory neurons. Pflugers Arch. 1988 Jun;411(6):661–669. doi: 10.1007/BF00580863. [DOI] [PubMed] [Google Scholar]
  20. Leifer D., Lipton S. A., Barnstable C. J., Masland R. H. Monoclonal antibody to Thy-1 enhances regeneration of processes by rat retinal ganglion cells in culture. Science. 1984 Apr 20;224(4646):303–306. doi: 10.1126/science.6143400. [DOI] [PubMed] [Google Scholar]
  21. Lester H. A. Heterologous expression of excitability proteins: route to more specific drugs? Science. 1988 Aug 26;241(4869):1057–1063. doi: 10.1126/science.2457947. [DOI] [PubMed] [Google Scholar]
  22. Lipton S. A. Bursting of calcium-activated cation-selective channels is associated with neurite regeneration in a mammalian central neuron. Neurosci Lett. 1987 Nov 10;82(1):21–28. doi: 10.1016/0304-3940(87)90165-0. [DOI] [PubMed] [Google Scholar]
  23. Lipton S. A., Tauck D. L. Voltage-dependent conductances of solitary ganglion cells dissociated from the rat retina. J Physiol. 1987 Apr;385:361–391. doi: 10.1113/jphysiol.1987.sp016497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lipton S. A., Wagner J. A., Madison R. D., D'Amore P. A. Acidic fibroblast growth factor enhances regeneration of processes by postnatal mammalian retinal ganglion cells in culture. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2388–2392. doi: 10.1073/pnas.85.7.2388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Matteson D. R., Armstrong C. M. Properties of two types of calcium channels in clonal pituitary cells. J Gen Physiol. 1986 Jan;87(1):161–182. doi: 10.1085/jgp.87.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McCleskey E. W., Fox A. P., Feldman D. H., Cruz L. J., Olivera B. M., Tsien R. W., Yoshikami D. Omega-conotoxin: direct and persistent blockade of specific types of calcium channels in neurons but not muscle. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4327–4331. doi: 10.1073/pnas.84.12.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Narahashi T., Tsunoo A., Yoshii M. Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol. 1987 Feb;383:231–249. doi: 10.1113/jphysiol.1987.sp016406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nilius B., Hess P., Lansman J. B., Tsien R. W. A novel type of cardiac calcium channel in ventricular cells. Nature. 1985 Aug 1;316(6027):443–446. doi: 10.1038/316443a0. [DOI] [PubMed] [Google Scholar]
  29. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
  30. Olivera B. M., Gray W. R., Zeikus R., McIntosh J. M., Varga J., Rivier J., de Santos V., Cruz L. J. Peptide neurotoxins from fish-hunting cone snails. Science. 1985 Dec 20;230(4732):1338–1343. doi: 10.1126/science.4071055. [DOI] [PubMed] [Google Scholar]
  31. Perry V. H. The ganglion cell layer of the retina of the rat: a Golgi study. Proc R Soc Lond B Biol Sci. 1979 May 23;204(1156):363–375. doi: 10.1098/rspb.1979.0033. [DOI] [PubMed] [Google Scholar]
  32. Plummer M. R., Logothetis D. E., Hess P. Elementary properties and pharmacological sensitivities of calcium channels in mammalian peripheral neurons. Neuron. 1989 May;2(5):1453–1463. doi: 10.1016/0896-6273(89)90191-8. [DOI] [PubMed] [Google Scholar]
  33. Sanguinetti M. C., Kass R. S. Voltage-dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ Res. 1984 Sep;55(3):336–348. doi: 10.1161/01.res.55.3.336. [DOI] [PubMed] [Google Scholar]
  34. Schramm M., Thomas G., Towart R., Franckowiak G. Novel dihydropyridines with positive inotropic action through activation of Ca2+ channels. Nature. 1983 Jun 9;303(5917):535–537. doi: 10.1038/303535a0. [DOI] [PubMed] [Google Scholar]
  35. Scott R. H., Dolphin A. C. Activation of a G protein promotes agonist responses to calcium channel ligands. Nature. 1987 Dec 24;330(6150):760–762. doi: 10.1038/330760a0. [DOI] [PubMed] [Google Scholar]
  36. Scott R. H., Dolphin A. C. The agonist effect of Bay K 8644 on neuronal calcium channel currents is promoted by G-protein activation. Neurosci Lett. 1988 Jun 29;89(2):170–175. doi: 10.1016/0304-3940(88)90376-x. [DOI] [PubMed] [Google Scholar]
  37. Swandulla D., Armstrong C. M. Fast-deactivating calcium channels in chick sensory neurons. J Gen Physiol. 1988 Aug;92(2):197–218. doi: 10.1085/jgp.92.2.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Wada K., Ballivet M., Boulter J., Connolly J., Wada E., Deneris E. S., Swanson L. W., Heinemann S., Patrick J. Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor. Science. 1988 Apr 15;240(4850):330–334. doi: 10.1126/science.2832952. [DOI] [PubMed] [Google Scholar]
  39. Yaari Y., Hamon B., Lux H. D. Development of two types of calcium channels in cultured mammalian hippocampal neurons. Science. 1987 Feb 6;235(4789):680–682. doi: 10.1126/science.2433765. [DOI] [PubMed] [Google Scholar]

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