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. 1993 Jan;460:741–758. doi: 10.1113/jphysiol.1993.sp019497

The permeability of the cGMP-activated channel to organic cations in retinal rods of the tiger salamander.

C Picco 1, A Menini 1
PMCID: PMC1175239  PMID: 7683718

Abstract

1. The permeability of the channel activated by guanosine 3',5'-cyclic monophosphate (cGMP) to many organic monovalent cations was determined by recording macroscopic currents in excised inside-out patches of plasma membrane from isolated retinal rod outer segments of the tiger salamander. 2. Current-voltage relations were measured when the NaCl of the bathing medium was replaced by salts of organic cations. Permeability ratios relative to Na+ ions were calculated with the Goldman-Hodgkin-Katz potential equation from the measured changes of reversal potentials. 3. Hydroxylammonium+, hydrazinium+ and methylammonium+, which are molecules of very similar shape and size, permeate the channel with very different permeability ratios: 5.92, 1.99 and 0.60 respectively. 4. Methylated and ethylated ammonium+ compounds were investigated. It was found that, not only methylammonium+, but also dimethylammonium+ and ethylammonium+ were permeant with permeability ratios of 0.6, 0.14 and 0.16 respectively. Trimethylammonium+, tetramethylammonium+, diethylammonium+, triethylammonium+, and tetraethylammonium+ were not permeant. 5. Guanidinium+ and its derivatives formamidinium+, aminoguanidinium+, acetamidinium+ and methylguanidinium+ were all permeant with permeability ratios 1.12, 1.00, 0.63, 0.36 and 0.33 respectively. 6. The cGMP-activated channel was found to be permeable to at least thirteen organic cations. Molecular models of the permeant cations indicate that the cross-section of the narrowest part of the pore must be at least as large as a rectangle of 0.38 x 0.5 nm dimensions.

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Selected References

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  1. Adams D. J., Dwyer T. M., Hille B. The permeability of endplate channels to monovalent and divalent metal cations. J Gen Physiol. 1980 May;75(5):493–510. doi: 10.1085/jgp.75.5.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Capovilla M., Caretta A., Cervetto L., Torre V. Ionic movements through light-sensitive channels of toad rods. J Physiol. 1983 Oct;343:295–310. doi: 10.1113/jphysiol.1983.sp014893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Dwyer T. M., Adams D. J., Hille B. The permeability of the endplate channel to organic cations in frog muscle. J Gen Physiol. 1980 May;75(5):469–492. doi: 10.1085/jgp.75.5.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eisenman G., Horn R. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J Membr Biol. 1983;76(3):197–225. doi: 10.1007/BF01870364. [DOI] [PubMed] [Google Scholar]
  7. Fesenko E. E., Kolesnikov S. S., Lyubarsky A. L. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature. 1985 Jan 24;313(6000):310–313. doi: 10.1038/313310a0. [DOI] [PubMed] [Google Scholar]
  8. Fukushima Y., Hagiwara S. Currents carried by monovalent cations through calcium channels in mouse neoplastic B lymphocytes. J Physiol. 1985 Jan;358:255–284. doi: 10.1113/jphysiol.1985.sp015550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Furman R. E., Tanaka J. C. Monovalent selectivity of the cyclic guanosine monophosphate-activated ion channel. J Gen Physiol. 1990 Jul;96(1):57–82. doi: 10.1085/jgp.96.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Guy H. R., Durell S. R., Warmke J., Drysdale R., Ganetzky B. Similarities in amino acid sequences of Drosophila eag and cyclic nucleotide-gated channels. Science. 1991 Nov 1;254(5032):730–730. doi: 10.1126/science.1658932. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Haynes L., Yau K. W. Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature. 1985 Sep 5;317(6032):61–64. doi: 10.1038/317061a0. [DOI] [PubMed] [Google Scholar]
  13. Hille B. Potassium channels in myelinated nerve. Selective permeability to small cations. J Gen Physiol. 1973 Jun;61(6):669–686. doi: 10.1085/jgp.61.6.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hille B. The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol. 1972 Jun;59(6):637–658. doi: 10.1085/jgp.59.6.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hille B. The permeability of the sodium channel to organic cations in myelinated nerve. J Gen Physiol. 1971 Dec;58(6):599–619. doi: 10.1085/jgp.58.6.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hodgkin A. L., McNaughton P. A., Nunn B. J. The ionic selectivity and calcium dependence of the light-sensitive pathway in toad rods. J Physiol. 1985 Jan;358:447–468. doi: 10.1113/jphysiol.1985.sp015561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jan L. Y., Jan Y. N. A superfamily of ion channels. Nature. 1990 Jun 21;345(6277):672–672. doi: 10.1038/345672a0. [DOI] [PubMed] [Google Scholar]
  18. Kaupp U. B. The cyclic nucleotide-gated channels of vertebrate photoreceptors and olfactory epithelium. Trends Neurosci. 1991 Apr;14(4):150–157. doi: 10.1016/0166-2236(91)90087-b. [DOI] [PubMed] [Google Scholar]
  19. McCleskey E. W., Almers W. The Ca channel in skeletal muscle is a large pore. Proc Natl Acad Sci U S A. 1985 Oct;82(20):7149–7153. doi: 10.1073/pnas.82.20.7149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McNaughton P. A. Light response of vertebrate photoreceptors. Physiol Rev. 1990 Jul;70(3):847–883. doi: 10.1152/physrev.1990.70.3.847. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Menini A., Rispoli G., Torre V. The ionic selectivity of the light-sensitive current in isolated rods of the tiger salamander. J Physiol. 1988 Aug;402:279–300. doi: 10.1113/jphysiol.1988.sp017204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nakamura T., Gold G. H. A cyclic nucleotide-gated conductance in olfactory receptor cilia. 1987 Jan 29-Feb 4Nature. 325(6103):442–444. doi: 10.1038/325442a0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Pugh E. N., Jr, Lamb T. D. Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res. 1990;30(12):1923–1948. doi: 10.1016/0042-6989(90)90013-b. [DOI] [PubMed] [Google Scholar]
  26. Yau K. W., Baylor D. A. Cyclic GMP-activated conductance of retinal photoreceptor cells. Annu Rev Neurosci. 1989;12:289–327. doi: 10.1146/annurev.ne.12.030189.001445. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. 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]

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