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. 1999 Jan 4;18(1):131–144. doi: 10.1093/emboj/18.1.131

Ca2+ permeation in cyclic nucleotide-gated channels.

C Dzeja 1, V Hagen 1, U B Kaupp 1, S Frings 1
PMCID: PMC1171109  PMID: 9878057

Abstract

Cyclic nucleotide-gated (CNG) channels conduct Na+, K+ and Ca2+ currents under the control of cGMP and cAMP. Activation of CNG channels leads to depolarization of the membrane voltage and to a concomitant increase of the cytosolic Ca2+ concentration. Several polypeptides were identified that constitute principal and modulatory subunits of CNG channels in both neurons and non-excitable cells, co-assembling to form a variety of heteromeric proteins with distinct biophysical properties. Since the contribution of each channel type to Ca2+ signaling depends on its specific Ca2+ conductance, it is necessary to analyze Ca2+ permeation for each individual channel type. We have analyzed Ca2+ permeation in all principal subunits of vertebrates and for a principal subunit from Drosophila melanogaster. We measured the fractional Ca2+ current over the physiological range of Ca2+ concentrations and found that Ca2+ permeation is determined by subunit composition and modulated by membrane voltage and extracellular pH. Ca2+ permeation is controlled by the Ca2+-binding affinity of the intrapore cation-binding site, which varies profoundly between members of the CNG channel family, and gives rise to a surprising diversity in the ability to generate Ca2+ signals.

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Selected References

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  1. Ahmad I., Leinders-Zufall T., Kocsis J. D., Shepherd G. M., Zufall F., Barnstable C. J. Retinal ganglion cells express a cGMP-gated cation conductance activatable by nitric oxide donors. Neuron. 1994 Jan;12(1):155–165. doi: 10.1016/0896-6273(94)90160-0. [DOI] [PubMed] [Google Scholar]
  2. Altenhofen W., Ludwig J., Eismann E., Kraus W., Bönigk W., Kaupp U. B. Control of ligand specificity in cyclic nucleotide-gated channels from rod photoreceptors and olfactory epithelium. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9868–9872. doi: 10.1073/pnas.88.21.9868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baumann A., Frings S., Godde M., Seifert R., Kaupp U. B. Primary structure and functional expression of a Drosophila cyclic nucleotide-gated channel present in eyes and antennae. EMBO J. 1994 Nov 1;13(21):5040–5050. doi: 10.1002/j.1460-2075.1994.tb06833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Biel M., Zong X., Distler M., Bosse E., Klugbauer N., Murakami M., Flockerzi V., Hofmann F. Another member of the cyclic nucleotide-gated channel family, expressed in testis, kidney, and heart. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3505–3509. doi: 10.1073/pnas.91.9.3505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biel M., Zong X., Ludwig A., Sautter A., Hofmann F. Molecular cloning and expression of the Modulatory subunit of the cyclic nucleotide-gated cation channel. J Biol Chem. 1996 Mar 15;271(11):6349–6355. doi: 10.1074/jbc.271.11.6349. [DOI] [PubMed] [Google Scholar]
  6. Bradley J., Li J., Davidson N., Lester H. A., Zinn K. Heteromeric olfactory cyclic nucleotide-gated channels: a subunit that confers increased sensitivity to cAMP. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8890–8894. doi: 10.1073/pnas.91.19.8890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bradley J., Zhang Y., Bakin R., Lester H. A., Ronnett G. V., Zinn K. Functional expression of the heteromeric "olfactory" cyclic nucleotide-gated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons. J Neurosci. 1997 Mar 15;17(6):1993–2005. doi: 10.1523/JNEUROSCI.17-06-01993.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Burnashev N., Zhou Z., Neher E., Sakmann B. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainate receptor subtypes. J Physiol. 1995 Jun 1;485(Pt 2):403–418. doi: 10.1113/jphysiol.1995.sp020738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bönigk W., Altenhofen W., Müller F., Dose A., Illing M., Molday R. S., Kaupp U. B. Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron. 1993 May;10(5):865–877. doi: 10.1016/0896-6273(93)90202-3. [DOI] [PubMed] [Google Scholar]
  10. Bönigk W., Müller F., Middendorff R., Weyand I., Kaupp U. B. Two alternatively spliced forms of the cGMP-gated channel alpha-subunit from cone photoreceptor are expressed in the chick pineal organ. J Neurosci. 1996 Dec 1;16(23):7458–7468. doi: 10.1523/JNEUROSCI.16-23-07458.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chen T. Y., Illing M., Molday L. L., Hsu Y. T., Yau K. W., Molday R. S. Subunit 2 (or beta) of retinal rod cGMP-gated cation channel is a component of the 240-kDa channel-associated protein and mediates Ca(2+)-calmodulin modulation. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11757–11761. doi: 10.1073/pnas.91.24.11757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Coburn C. M., Bargmann C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron. 1996 Oct;17(4):695–706. doi: 10.1016/s0896-6273(00)80201-9. [DOI] [PubMed] [Google Scholar]
  14. Colamartino G., Menini A., Torre V. Blockage and permeation of divalent cations through the cyclic GMP-activated channel from tiger salamander retinal rods. J Physiol. 1991;440:189–206. doi: 10.1113/jphysiol.1991.sp018703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dang T. X., McCleskey E. W. Ion channel selectivity through stepwise changes in binding affinity. J Gen Physiol. 1998 Feb;111(2):185–193. doi: 10.1085/jgp.111.2.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. De Waard M., Gurnett C. A., Campbell K. P. Structural and functional diversity of voltage-activated calcium channels. Ion Channels. 1996;4:41–87. doi: 10.1007/978-1-4899-1775-1_2. [DOI] [PubMed] [Google Scholar]
  17. Dhallan R. S., Yau K. W., Schrader K. A., Reed R. R. Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature. 1990 Sep 13;347(6289):184–187. doi: 10.1038/347184a0. [DOI] [PubMed] [Google Scholar]
  18. Distler M., Biel M., Flockerzi V., Hofmann F. Expression of cyclic nucleotide-gated cation channels in non-sensory tissues and cells. Neuropharmacology. 1994 Nov;33(11):1275–1282. doi: 10.1016/0028-3908(94)90027-2. [DOI] [PubMed] [Google Scholar]
  19. Dryer S. E., Henderson D. A cyclic GMP-activated channel in dissociated cells of the chick pineal gland. Nature. 1991 Oct 24;353(6346):756–758. doi: 10.1038/353756a0. [DOI] [PubMed] [Google Scholar]
  20. Eismann E., Müller F., Heinemann S. H., Kaupp U. B. A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1109–1113. doi: 10.1073/pnas.91.3.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ellinor P. T., Yang J., Sather W. A., Zhang J. F., Tsien R. W. Ca2+ channel selectivity at a single locus for high-affinity Ca2+ interactions. Neuron. 1995 Nov;15(5):1121–1132. doi: 10.1016/0896-6273(95)90100-0. [DOI] [PubMed] [Google Scholar]
  22. Finn J. T., Grunwald M. E., Yau K. W. Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu Rev Physiol. 1996;58:395–426. doi: 10.1146/annurev.ph.58.030196.002143. [DOI] [PubMed] [Google Scholar]
  23. Finn J. T., Krautwurst D., Schroeder J. E., Chen T. Y., Reed R. R., Yau K. W. Functional co-assembly among subunits of cyclic-nucleotide-activated, nonselective cation channels, and across species from nematode to human. Biophys J. 1998 Mar;74(3):1333–1345. doi: 10.1016/S0006-3495(98)77846-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Frings S. Cyclic nucleotide-gated channels and calcium: an intimate relation. Adv Second Messenger Phosphoprotein Res. 1997;31:75–82. doi: 10.1016/s1040-7952(97)80010-9. [DOI] [PubMed] [Google Scholar]
  25. Frings S., Lynch J. W., Lindemann B. Properties of cyclic nucleotide-gated channels mediating olfactory transduction. Activation, selectivity, and blockage. J Gen Physiol. 1992 Jul;100(1):45–67. doi: 10.1085/jgp.100.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Frings S., Seifert R., Godde M., Kaupp U. B. Profoundly different calcium permeation and blockage determine the specific function of distinct cyclic nucleotide-gated channels. Neuron. 1995 Jul;15(1):169–179. doi: 10.1016/0896-6273(95)90074-8. [DOI] [PubMed] [Google Scholar]
  27. Fujita Y., Mynlieff M., Dirksen R. T., Kim M. S., Niidome T., Nakai J., Friedrich T., Iwabe N., Miyata T., Furuichi T. Primary structure and functional expression of the omega-conotoxin-sensitive N-type calcium channel from rabbit brain. Neuron. 1993 Apr;10(4):585–598. doi: 10.1016/0896-6273(93)90162-k. [DOI] [PubMed] [Google Scholar]
  28. Garaschuk O., Schneggenburger R., Schirra C., Tempia F., Konnerth A. Fractional Ca2+ currents through somatic and dendritic glutamate receptor channels of rat hippocampal CA1 pyramidal neurones. J Physiol. 1996 Mar 15;491(Pt 3):757–772. doi: 10.1113/jphysiol.1996.sp021255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Hagen V., Dzeja C., Bendig J., Baeger I., Kaupp U. B. Novel caged compounds of hydrolysis-resistant 8-Br-cAMP and 8-Br-cGMP: photolabile NPE esters. J Photochem Photobiol B. 1998 Jan;42(1):71–78. doi: 10.1016/s1011-1344(97)00125-5. [DOI] [PubMed] [Google Scholar]
  31. Hagen V., Dzeja C., Frings S., Bendig J., Krause E., Kaupp U. B. Caged compounds of hydrolysis-resistant analogues of cAMP and cGMP: synthesis and application to cyclic nucleotide-gated channels. Biochemistry. 1996 Jun 18;35(24):7762–7771. doi: 10.1021/bi952895b. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Haynes L. W., Kay A. R., Yau K. W. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 1986 May 1;321(6065):66–70. doi: 10.1038/321066a0. [DOI] [PubMed] [Google Scholar]
  34. Haynes L. W. Permeation of internal and external monovalent cations through the catfish cone photoreceptor cGMP-gated channel. J Gen Physiol. 1995 Sep;106(3):485–505. doi: 10.1085/jgp.106.3.485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Hess P., Lansman J. B., Tsien R. W. Calcium channel selectivity for divalent and monovalent cations. Voltage and concentration dependence of single channel current in ventricular heart cells. J Gen Physiol. 1986 Sep;88(3):293–319. doi: 10.1085/jgp.88.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Karpen J. W., Zimmerman A. L., Stryer L., Baylor D. A. Gating kinetics of the cyclic-GMP-activated channel of retinal rods: flash photolysis and voltage-jump studies. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1287–1291. doi: 10.1073/pnas.85.4.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kaupp U. B. Family of cyclic nucleotide gated ion channels. Curr Opin Neurobiol. 1995 Aug;5(4):434–442. doi: 10.1016/0959-4388(95)80002-6. [DOI] [PubMed] [Google Scholar]
  38. Kaupp U. B., Koch K. W. Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu Rev Physiol. 1992;54:153–175. doi: 10.1146/annurev.ph.54.030192.001101. [DOI] [PubMed] [Google Scholar]
  39. Kaupp U. B., Niidome T., Tanabe T., Terada S., Bönigk W., Stühmer W., Cook N. J., Kangawa K., Matsuo H., Hirose T. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature. 1989 Dec 14;342(6251):762–766. doi: 10.1038/342762a0. [DOI] [PubMed] [Google Scholar]
  40. Kim M. S., Morii T., Sun L. X., Imoto K., Mori Y. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett. 1993 Mar 1;318(2):145–148. doi: 10.1016/0014-5793(93)80009-j. [DOI] [PubMed] [Google Scholar]
  41. Kingston P. A., Zufall F., Barnstable C. J. Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10440–10445. doi: 10.1073/pnas.93.19.10440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Kleene S. J. Block by external calcium and magnesium of the cyclic-nucleotide-activated current in olfactory cilia. Neuroscience. 1995 Jun;66(4):1001–1008. doi: 10.1016/0306-4522(94)00634-h. [DOI] [PubMed] [Google Scholar]
  43. Kleene S. J., Gesteland R. C., Bryant S. H. An electrophysiological survey of frog olfactory cilia. J Exp Biol. 1994 Oct;195:307–328. doi: 10.1242/jeb.195.1.307. [DOI] [PubMed] [Google Scholar]
  44. Koch K. W. Control of photoreceptor proteins by Ca2+. Cell Calcium. 1995 Oct;18(4):314–321. doi: 10.1016/0143-4160(95)90027-6. [DOI] [PubMed] [Google Scholar]
  45. Korenbrot J. I. Ca2+ flux in retinal rod and cone outer segments: differences in Ca2+ selectivity of the cGMP-gated ion channels and Ca2+ clearance rates. Cell Calcium. 1995 Oct;18(4):285–300. doi: 10.1016/0143-4160(95)90025-x. [DOI] [PubMed] [Google Scholar]
  46. Körschen H. G., Illing M., Seifert R., Sesti F., Williams A., Gotzes S., Colville C., Müller F., Dosé A., Godde M. A 240 kDa protein represents the complete beta subunit of the cyclic nucleotide-gated channel from rod photoreceptor. Neuron. 1995 Sep;15(3):627–636. doi: 10.1016/0896-6273(95)90151-5. [DOI] [PubMed] [Google Scholar]
  47. Leinders-Zufall T., Greer C. A., Shepherd G. M., Zufall F. Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J Neurosci. 1998 Aug 1;18(15):5630–5639. doi: 10.1523/JNEUROSCI.18-15-05630.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Leinders-Zufall T., Rand M. N., Shepherd G. M., Greer C. A., Zufall F. Calcium entry through cyclic nucleotide-gated channels in individual cilia of olfactory receptor cells: spatiotemporal dynamics. J Neurosci. 1997 Jun 1;17(11):4136–4148. doi: 10.1523/JNEUROSCI.17-11-04136.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Leinders-Zufall T., Rosenboom H., Barnstable C. J., Shepherd G. M., Zufall F. A calcium-permeable cGMP-activated cation conductance in hippocampal neurons. Neuroreport. 1995 Sep 11;6(13):1761–1765. doi: 10.1097/00001756-199509000-00013. [DOI] [PubMed] [Google Scholar]
  50. Li J., Zagotta W. N., Lester H. A. Cyclic nucleotide-gated channels: structural basis of ligand efficacy and allosteric modulation. Q Rev Biophys. 1997 May;30(2):177–193. doi: 10.1017/s0033583597003326. [DOI] [PubMed] [Google Scholar]
  51. Liman E. R., Buck L. B. A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP. Neuron. 1994 Sep;13(3):611–621. doi: 10.1016/0896-6273(94)90029-9. [DOI] [PubMed] [Google Scholar]
  52. Ludwig J., Margalit T., Eismann E., Lancet D., Kaupp U. B. Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett. 1990 Sep 17;270(1-2):24–29. doi: 10.1016/0014-5793(90)81226-e. [DOI] [PubMed] [Google Scholar]
  53. McCleskey E. W. Calcium channels: cellular roles and molecular mechanisms. Curr Opin Neurobiol. 1994 Jun;4(3):304–312. doi: 10.1016/0959-4388(94)90090-6. [DOI] [PubMed] [Google Scholar]
  54. Menini A. Currents carried by monovalent cations through cyclic GMP-activated channels in excised patches from salamander rods. J Physiol. 1990 May;424:167–185. doi: 10.1113/jphysiol.1990.sp018061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Misaka T., Kusakabe Y., Emori Y., Gonoi T., Arai S., Abe K. Taste buds have a cyclic nucleotide-activated channel, CNGgust. J Biol Chem. 1997 Sep 5;272(36):22623–22629. doi: 10.1074/jbc.272.36.22623. [DOI] [PubMed] [Google Scholar]
  56. Nakatani K., Yau K. W. Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. J Physiol. 1988 Jan;395:695–729. doi: 10.1113/jphysiol.1988.sp016942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Nawy S., Jahr C. E. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature. 1990 Jul 19;346(6281):269–271. doi: 10.1038/346269a0. [DOI] [PubMed] [Google Scholar]
  58. Neher E., Augustine G. J. Calcium gradients and buffers in bovine chromaffin cells. J Physiol. 1992 May;450:273–301. doi: 10.1113/jphysiol.1992.sp019127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Nizzari M., Sesti F., Giraudo M. T., Virginio C., Cattaneo A., Torre V. Single-channel properties of cloned cGMP-activated channels from retinal rods. Proc Biol Sci. 1993 Oct 22;254(1339):69–74. doi: 10.1098/rspb.1993.0128. [DOI] [PubMed] [Google Scholar]
  60. Park C. S., MacKinnon R. Divalent cation selectivity in a cyclic nucleotide-gated ion channel. Biochemistry. 1995 Oct 17;34(41):13328–13333. doi: 10.1021/bi00041a008. [DOI] [PubMed] [Google Scholar]
  61. Perry R. J., McNaughton P. A. Response properties of cones from the retina of the tiger salamander. J Physiol. 1991 Feb;433:561–587. doi: 10.1113/jphysiol.1991.sp018444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Picones A., Korenbrot J. I. Permeability and interaction of Ca2+ with cGMP-gated ion channels differ in retinal rod and cone photoreceptors. Biophys J. 1995 Jul;69(1):120–127. doi: 10.1016/S0006-3495(95)79881-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Prasher D. C., Eckenrode V. K., Ward W. W., Prendergast F. G., Cormier M. J. Primary structure of the Aequorea victoria green-fluorescent protein. Gene. 1992 Feb 15;111(2):229–233. doi: 10.1016/0378-1119(92)90691-h. [DOI] [PubMed] [Google Scholar]
  64. Reuter D., Zierold K., Schröder W. H., Frings S. A depolarizing chloride current contributes to chemoelectrical transduction in olfactory sensory neurons in situ. J Neurosci. 1998 Sep 1;18(17):6623–6630. doi: 10.1523/JNEUROSCI.18-17-06623.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rieke F., Schwartz E. A. A cGMP-gated current can control exocytosis at cone synapses. Neuron. 1994 Oct;13(4):863–873. doi: 10.1016/0896-6273(94)90252-6. [DOI] [PubMed] [Google Scholar]
  66. Root M. J., MacKinnon R. Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel. Neuron. 1993 Sep;11(3):459–466. doi: 10.1016/0896-6273(93)90150-p. [DOI] [PubMed] [Google Scholar]
  67. Root M. J., MacKinnon R. Two identical noninteracting sites in an ion channel revealed by proton transfer. Science. 1994 Sep 23;265(5180):1852–1856. doi: 10.1126/science.7522344. [DOI] [PubMed] [Google Scholar]
  68. Sautter A., Biel M., Hofmann F. Molecular cloning of cyclic nucleotide-gated cation channel subunits from rat pineal gland. Brain Res Mol Brain Res. 1997 Aug;48(1):171–175. doi: 10.1016/s0169-328x(97)00155-1. [DOI] [PubMed] [Google Scholar]
  69. Sautter A., Zong X., Hofmann F., Biel M. An isoform of the rod photoreceptor cyclic nucleotide-gated channel beta subunit expressed in olfactory neurons. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4696–4701. doi: 10.1073/pnas.95.8.4696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Savchenko A., Barnes S., Kramer R. H. Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide. Nature. 1997 Dec 18;390(6661):694–698. doi: 10.1038/37803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Schneggenburger R. Simultaneous measurement of Ca2+ influx and reversal potentials in recombinant N-methyl-D-aspartate receptor channels. Biophys J. 1996 May;70(5):2165–2174. doi: 10.1016/S0006-3495(96)79782-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Schneggenburger R., Zhou Z., Konnerth A., Neher E. Fractional contribution of calcium to the cation current through glutamate receptor channels. Neuron. 1993 Jul;11(1):133–143. doi: 10.1016/0896-6273(93)90277-x. [DOI] [PubMed] [Google Scholar]
  73. Seifert R., Eismann E., Ludwig J., Baumann A., Kaupp U. B. Molecular determinants of a Ca2+-binding site in the pore of cyclic nucleotide-gated channels: S5/S6 segments control affinity of intrapore glutamates. EMBO J. 1999 Jan 4;18(1):119–130. doi: 10.1093/emboj/18.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Sesti F., Eismann E., Kaupp U. B., Nizzari M., Torre V. The multi-ion nature of the cGMP-gated channel from vertebrate rods. J Physiol. 1995 Aug 15;487(1):17–36. doi: 10.1113/jphysiol.1995.sp020858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Tang S., Mikala G., Bahinski A., Yatani A., Varadi G., Schwartz A. Molecular localization of ion selectivity sites within the pore of a human L-type cardiac calcium channel. J Biol Chem. 1993 Jun 25;268(18):13026–13029. [PubMed] [Google Scholar]
  76. Tempia F., Kano M., Schneggenburger R., Schirra C., Garaschuk O., Plant T., Konnerth A. Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J Neurosci. 1996 Jan 15;16(2):456–466. doi: 10.1523/JNEUROSCI.16-02-00456.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Thompson S. H. Cyclic GMP-gated channels in a sympathetic neuron cell line. J Gen Physiol. 1997 Aug;110(2):155–164. doi: 10.1085/jgp.110.2.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Trouslard J., Marsh S. J., Brown D. A. Calcium entry through nicotinic receptor channels and calcium channels in cultured rat superior cervical ganglion cells. J Physiol. 1993 Aug;468:53–71. doi: 10.1113/jphysiol.1993.sp019759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Tsien R. W., Hess P., McCleskey E. W., Rosenberg R. L. Calcium channels: mechanisms of selectivity, permeation, and block. Annu Rev Biophys Biophys Chem. 1987;16:265–290. doi: 10.1146/annurev.bb.16.060187.001405. [DOI] [PubMed] [Google Scholar]
  80. Vernino S., Rogers M., Radcliffe K. A., Dani J. A. Quantitative measurement of calcium flux through muscle and neuronal nicotinic acetylcholine receptors. J Neurosci. 1994 Sep;14(9):5514–5524. doi: 10.1523/JNEUROSCI.14-09-05514.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Weyand I., Godde M., Frings S., Weiner J., Müller F., Altenhofen W., Hatt H., Kaupp U. B. Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature. 1994 Apr 28;368(6474):859–863. doi: 10.1038/368859a0. [DOI] [PubMed] [Google Scholar]
  82. Wiesner B., Weiner J., Middendorff R., Hagen V., Kaupp U. B., Weyand I. Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J Cell Biol. 1998 Jul 27;142(2):473–484. doi: 10.1083/jcb.142.2.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Yang J., Ellinor P. T., Sather W. A., Zhang J. F., Tsien R. W. Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature. 1993 Nov 11;366(6451):158–161. doi: 10.1038/366158a0. [DOI] [PubMed] [Google Scholar]
  84. Yau K. W., Nakatani K. Cation selectivity of light-sensitive conductance in retinal rods. Nature. 1984 May 24;309(5966):352–354. doi: 10.1038/309352a0. [DOI] [PubMed] [Google Scholar]
  85. Zagotta W. N., Siegelbaum S. A. Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci. 1996;19:235–263. doi: 10.1146/annurev.ne.19.030196.001315. [DOI] [PubMed] [Google Scholar]
  86. Zeilhofer H. U., Kress M., Swandulla D. Fractional Ca2+ currents through capsaicin- and proton-activated ion channels in rat dorsal root ganglion neurones. J Physiol. 1997 Aug 15;503(Pt 1):67–78. doi: 10.1111/j.1469-7793.1997.067bi.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Zhou Z., Neher E. Calcium permeability of nicotinic acetylcholine receptor channels in bovine adrenal chromaffin cells. Pflugers Arch. 1993 Dec;425(5-6):511–517. doi: 10.1007/BF00374879. [DOI] [PubMed] [Google Scholar]
  88. Zimmerman A. L., Baylor D. A. Cation interactions within the cyclic GMP-activated channel of retinal rods from the tiger salamander. J Physiol. 1992 Apr;449:759–783. doi: 10.1113/jphysiol.1992.sp019112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Zimmerman A. L., Baylor D. A. Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature. 1986 May 1;321(6065):70–72. doi: 10.1038/321070a0. [DOI] [PubMed] [Google Scholar]
  90. Zimmerman A. L., Karpen J. W., Baylor D. A. Hindered diffusion in excised membrane patches from retinal rod outer segments. Biophys J. 1988 Aug;54(2):351–355. doi: 10.1016/S0006-3495(88)82966-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Zufall F., Firestein S. Divalent cations block the cyclic nucleotide-gated channel of olfactory receptor neurons. J Neurophysiol. 1993 May;69(5):1758–1768. doi: 10.1152/jn.1993.69.5.1758. [DOI] [PubMed] [Google Scholar]
  92. Zufall F., Shepherd G. M., Barnstable C. J. Cyclic nucleotide gated channels as regulators of CNS development and plasticity. Curr Opin Neurobiol. 1997 Jun;7(3):404–412. doi: 10.1016/s0959-4388(97)80070-0. [DOI] [PubMed] [Google Scholar]
  93. el-Husseini A el-D, Bladen C., Vincent S. R. Expression of the olfactory cyclic nucleotide gated channel (CNG1) in the rat brain. Neuroreport. 1995 Jul 10;6(10):1459–1463. doi: 10.1097/00001756-199507100-00024. [DOI] [PubMed] [Google Scholar]

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