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. 1997 Jul 15;325(Pt 2):289–297. doi: 10.1042/bj3250289

Interactions of polyamines with ion channels.

K Williams 1
PMCID: PMC1218558  PMID: 9230104

Abstract

Endogenous polyamines, in particular spermine, have been found to cause block and modulation of a number of types of ion channel. Intracellular spermine is responsible for intrinsic gating and rectification of strong inward rectifier K+ channels by directly plugging the ion channel pore. These K+ channels control the resting membrane potential in both excitable and non-excitable cells, and control the excitability threshold in neurons and muscle cells. Intracellular spermine causes inward rectification at some subtypes of Ca2+-permeable glutamate receptors in the central nervous system, again by plugging the receptor channel pore, and spermine can even permeate the ion channel of these receptors. Extracellular spermine has multiple effects at the N-methyl-d-aspartate (NMDA) subtype of glutamate receptor, including stimulation that increases the size of NMDA receptor currents, and voltage-dependent block. A number of polyamine-conjugated arthropod toxins and synthetic polyamine analogues are potent antagonists of glutamate receptors, and represent new tools with which to study these receptors. Interactions of polyamines with other types of cation channels have been reported. This area of research represents a new biology and a new pharmacology of polyamines.

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Selected References

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  1. Aleksandrov A., Velimirovic B., Clapham D. E. Inward rectification of the IRK1 K+ channel reconstituted in lipid bilayers. Biophys J. 1996 Jun;70(6):2680–2687. doi: 10.1016/S0006-3495(96)79837-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anis N., Sherby S., Goodnow R., Jr, Niwa M., Konno K., Kallimopoulos T., Bukownik R., Nakanishi K., Usherwood P., Eldefrawi A. Structure-activity relationships of philanthotoxin analogs and polyamines on N-methyl-D-aspartate and nicotinic acetylcholine receptors. J Pharmacol Exp Ther. 1990 Sep;254(3):764–773. [PubMed] [Google Scholar]
  3. Araneda R. C., Zukin R. S., Bennett M. V. Effects of polyamines on NMDA-induced currents in rat hippocampal neurons: a whole-cell and single-channel study. Neurosci Lett. 1993 Apr 2;152(1-2):107–112. doi: 10.1016/0304-3940(93)90495-7. [DOI] [PubMed] [Google Scholar]
  4. Bennett J. A., Dingledine R. Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining reentrant membrane loop. Neuron. 1995 Feb;14(2):373–384. doi: 10.1016/0896-6273(95)90293-7. [DOI] [PubMed] [Google Scholar]
  5. Benveniste M., Mayer M. L. Multiple effects of spermine on N-methyl-D-aspartic acid receptor responses of rat cultured hippocampal neurones. J Physiol. 1993 May;464:131–163. doi: 10.1113/jphysiol.1993.sp019627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bianchi L., Roy M. L., Taglialatela M., Lundgren D. W., Brown A. M., Ficker E. Regulation by spermine of native inward rectifier K+ channels in RBL-1 cells. J Biol Chem. 1996 Mar 15;271(11):6114–6121. doi: 10.1074/jbc.271.11.6114. [DOI] [PubMed] [Google Scholar]
  7. Bowie D., Mayer M. L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron. 1995 Aug;15(2):453–462. doi: 10.1016/0896-6273(95)90049-7. [DOI] [PubMed] [Google Scholar]
  8. Brackley P., Goodnow R., Jr, Nakanishi K., Sudan H. L., Usherwood P. N. Spermine and philanthotoxin potentiate excitatory amino acid responses of Xenopus oocytes injected with rat and chick brain RNA. Neurosci Lett. 1990 Jun 22;114(1):51–56. doi: 10.1016/0304-3940(90)90427-b. [DOI] [PubMed] [Google Scholar]
  9. Burnashev N., Monyer H., Seeburg P. H., Sakmann B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron. 1992 Jan;8(1):189–198. doi: 10.1016/0896-6273(92)90120-3. [DOI] [PubMed] [Google Scholar]
  10. Béhé P., Stern P., Wyllie D. J., Nassar M., Schoepfer R., Colquhoun D. Determination of NMDA NR1 subunit copy number in recombinant NMDA receptors. Proc Biol Sci. 1995 Nov 22;262(1364):205–213. doi: 10.1098/rspb.1995.0197. [DOI] [PubMed] [Google Scholar]
  11. Casero R. A., Jr, Pegg A. E. Spermidine/spermine N1-acetyltransferase--the turning point in polyamine metabolism. FASEB J. 1993 May;7(8):653–661. [PubMed] [Google Scholar]
  12. Chao J., Seiler N., Renault J., Kashiwagi K., Masuko T., Igarashi K., Williams K. N1-dansyl-spermine and N1-(n-octanesulfonyl)-spermine, novel glutamate receptor antagonists: block and permeation of N-methyl-D-aspartate receptors. Mol Pharmacol. 1997 May;51(5):861–871. doi: 10.1124/mol.51.5.861. [DOI] [PubMed] [Google Scholar]
  13. Choi D. W. Glutamate neurotoxicity and diseases of the nervous system. Neuron. 1988 Oct;1(8):623–634. doi: 10.1016/0896-6273(88)90162-6. [DOI] [PubMed] [Google Scholar]
  14. Collingridge G. L., Lester R. A. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol Rev. 1989 Jun;41(2):143–210. [PubMed] [Google Scholar]
  15. Colombo R., Cerana R., Bagni N. Evidence for polyamine channels in protoplasts and vacuoles of Arabidopsis thaliana cells. Biochem Biophys Res Commun. 1992 Feb 14;182(3):1187–1192. doi: 10.1016/0006-291x(92)91857-m. [DOI] [PubMed] [Google Scholar]
  16. Donevan S. D., Rogawski M. A. Intracellular polyamines mediate inward rectification of Ca(2+)-permeable alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9298–9302. doi: 10.1073/pnas.92.20.9298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Donevan S. D., Rogawski M. A. Multiple actions of arylalkylamine arthropod toxins on the N-methyl-D-aspartate receptor. Neuroscience. 1996 Jan;70(2):361–375. doi: 10.1016/0306-4522(95)00342-8. [DOI] [PubMed] [Google Scholar]
  18. Doupnik C. A., Davidson N., Lester H. A. The inward rectifier potassium channel family. Curr Opin Neurobiol. 1995 Jun;5(3):268–277. doi: 10.1016/0959-4388(95)80038-7. [DOI] [PubMed] [Google Scholar]
  19. Drouin H., Hermann A. Intracellular action of spermine on neuronal Ca2+ and K+ currents. Eur J Neurosci. 1994 Mar 1;6(3):412–419. doi: 10.1111/j.1460-9568.1994.tb00284.x. [DOI] [PubMed] [Google Scholar]
  20. Durand G. M., Bennett M. V., Zukin R. S. Splice variants of the N-methyl-D-aspartate receptor NR1 identify domains involved in regulation by polyamines and protein kinase C. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6731–6735. doi: 10.1073/pnas.90.14.6731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Durand G. M., Gregor P., Zheng X., Bennett M. V., Uhl G. R., Zukin R. S. Cloning of an apparent splice variant of the rat N-methyl-D-aspartate receptor NMDAR1 with altered sensitivity to polyamines and activators of protein kinase C. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9359–9363. doi: 10.1073/pnas.89.19.9359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Egebjerg J., Heinemann S. F. Ca2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):755–759. doi: 10.1073/pnas.90.2.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Fage D., Voltz C., Scatton B., Carter C. Selective release of spermine and spermidine from the rat striatum by N-methyl-D-aspartate receptor activation in vivo. J Neurochem. 1992 Jun;58(6):2170–2175. doi: 10.1111/j.1471-4159.1992.tb10960.x. [DOI] [PubMed] [Google Scholar]
  24. Fakler B., Brändle U., Bond C., Glowatzki E., König C., Adelman J. P., Zenner H. P., Ruppersberg J. P. A structural determinant of differential sensitivity of cloned inward rectifier K+ channels to intracellular spermine. FEBS Lett. 1994 Dec 19;356(2-3):199–203. doi: 10.1016/0014-5793(94)01258-x. [DOI] [PubMed] [Google Scholar]
  25. Fakler B., Brändle U., Glowatzki E., Weidemann S., Zenner H. P., Ruppersberg J. P. Strong voltage-dependent inward rectification of inward rectifier K+ channels is caused by intracellular spermine. Cell. 1995 Jan 13;80(1):149–154. doi: 10.1016/0092-8674(95)90459-x. [DOI] [PubMed] [Google Scholar]
  26. Ferrer-Montiel A. V., Montal M. Pentameric subunit stoichiometry of a neuronal glutamate receptor. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2741–2744. doi: 10.1073/pnas.93.7.2741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ficker E., Taglialatela M., Wible B. A., Henley C. M., Brown A. M. Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science. 1994 Nov 11;266(5187):1068–1072. doi: 10.1126/science.7973666. [DOI] [PubMed] [Google Scholar]
  28. Gu J. G., Albuquerque C., Lee C. J., MacDermott A. B. Synaptic strengthening through activation of Ca2+-permeable AMPA receptors. Nature. 1996 Jun 27;381(6585):793–796. doi: 10.1038/381793a0. [DOI] [PubMed] [Google Scholar]
  29. Harman R. J., Shaw G. G. High-affinity uptake of spermine by slices of rat cerebral cortex. J Neurochem. 1981 May;36(5):1609–1615. doi: 10.1111/j.1471-4159.1981.tb00409.x. [DOI] [PubMed] [Google Scholar]
  30. Harman R. J., Shaw G. G. The spontaneous and evoked release of spermine from rat brain in vitro. Br J Pharmacol. 1981 May;73(1):165–174. doi: 10.1111/j.1476-5381.1981.tb16786.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hayashi S., Murakami Y. Rapid and regulated degradation of ornithine decarboxylase. Biochem J. 1995 Feb 15;306(Pt 1):1–10. doi: 10.1042/bj3060001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hollmann M., Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci. 1994;17:31–108. doi: 10.1146/annurev.ne.17.030194.000335. [DOI] [PubMed] [Google Scholar]
  33. Hollmann M., Maron C., Heinemann S. N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron. 1994 Dec;13(6):1331–1343. doi: 10.1016/0896-6273(94)90419-7. [DOI] [PubMed] [Google Scholar]
  34. Hsu K. S. Modulation of the nicotinic acetylcholine receptor channels by spermine in Xenopus muscle cell culture. Neurosci Lett. 1994 Nov 21;182(1):99–103. doi: 10.1016/0304-3940(94)90216-x. [DOI] [PubMed] [Google Scholar]
  35. Hume R. I., Dingledine R., Heinemann S. F. Identification of a site in glutamate receptor subunits that controls calcium permeability. Science. 1991 Aug 30;253(5023):1028–1031. doi: 10.1126/science.1653450. [DOI] [PubMed] [Google Scholar]
  36. Igarashi K., Williams K. Antagonist properties of polyamines and bis(ethyl)polyamines at N-methyl-D-aspartate receptors. J Pharmacol Exp Ther. 1995 Mar;272(3):1101–1109. [PubMed] [Google Scholar]
  37. Iino M., Ozawa S., Tsuzuki K. Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J Physiol. 1990 May;424:151–165. doi: 10.1113/jphysiol.1990.sp018060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Isa T., Iino M., Itazawa S., Ozawa S. Spermine mediates inward rectification of Ca(2+)-permeable AMPA receptor channels. Neuroreport. 1995 Oct 23;6(15):2045–2048. doi: 10.1097/00001756-199510010-00022. [DOI] [PubMed] [Google Scholar]
  39. Ishihara K., Hiraoka M., Ochi R. The tetravalent organic cation spermine causes the gating of the IRK1 channel expressed in murine fibroblast cells. J Physiol. 1996 Mar 1;491(Pt 2):367–381. doi: 10.1113/jphysiol.1996.sp021222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Jackson H., Parks T. N. Spider toxins: recent applications in neurobiology. Annu Rev Neurosci. 1989;12:405–414. doi: 10.1146/annurev.ne.12.030189.002201. [DOI] [PubMed] [Google Scholar]
  41. Jackson H., Usherwood P. N. Spider toxins as tools for dissecting elements of excitatory amino acid transmission. Trends Neurosci. 1988 Jun;11(6):278–283. doi: 10.1016/0166-2236(88)90112-9. [DOI] [PubMed] [Google Scholar]
  42. Jonas P., Racca C., Sakmann B., Seeburg P. H., Monyer H. Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron. 1994 Jun;12(6):1281–1289. doi: 10.1016/0896-6273(94)90444-8. [DOI] [PubMed] [Google Scholar]
  43. Kamboj S. K., Swanson G. T., Cull-Candy S. G. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol. 1995 Jul 15;486(Pt 2):297–303. doi: 10.1113/jphysiol.1995.sp020812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Karst H., Joëls M., Wadman W. J., Piek T. Philanthotoxin inhibits Ca2+ currents in rat hippocampal CA1 neurons. Eur J Pharmacol. 1994 Aug 3;270(4):357–360. doi: 10.1016/0926-6917(94)90012-4. [DOI] [PubMed] [Google Scholar]
  45. Kashiwagi K., Fukuchi J., Chao J., Igarashi K., Williams K. An aspartate residue in the extracellular loop of the N-methyl-D-aspartate receptor controls sensitivity to spermine and protons. Mol Pharmacol. 1996 Jun;49(6):1131–1141. [PubMed] [Google Scholar]
  46. Koh D. S., Burnashev N., Jonas P. Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol. 1995 Jul 15;486(Pt 2):305–312. doi: 10.1113/jphysiol.1995.sp020813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Lerma J. Spermine regulates N-methyl-D-aspartate receptor desensitization. Neuron. 1992 Feb;8(2):343–352. doi: 10.1016/0896-6273(92)90300-3. [DOI] [PubMed] [Google Scholar]
  48. Lopatin A. N., Makhina E. N., Nichols C. G. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature. 1994 Nov 24;372(6504):366–369. doi: 10.1038/372366a0. [DOI] [PubMed] [Google Scholar]
  49. Lopatin A. N., Makhina E. N., Nichols C. G. The mechanism of inward rectification of potassium channels: "long-pore plugging" by cytoplasmic polyamines. J Gen Physiol. 1995 Nov;106(5):923–955. doi: 10.1085/jgp.106.5.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Luo J., Wang Y., Yasuda R. P., Dunah A. W., Wolfe B. B. The majority of N-methyl-D-aspartate receptor complexes in adult rat cerebral cortex contain at least three different subunits (NR1/NR2A/NR2B). Mol Pharmacol. 1997 Jan;51(1):79–86. doi: 10.1124/mol.51.1.79. [DOI] [PubMed] [Google Scholar]
  51. Marton L. J., Pegg A. E. Polyamines as targets for therapeutic intervention. Annu Rev Pharmacol Toxicol. 1995;35:55–91. doi: 10.1146/annurev.pa.35.040195.000415. [DOI] [PubMed] [Google Scholar]
  52. Matsuda H. Magnesium gating of the inwardly rectifying K+ channel. Annu Rev Physiol. 1991;53:289–298. doi: 10.1146/annurev.ph.53.030191.001445. [DOI] [PubMed] [Google Scholar]
  53. McBain C. J., Dingledine R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J Physiol. 1993 Mar;462:373–392. doi: 10.1113/jphysiol.1993.sp019560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. McBain C. J., Mayer M. L. N-methyl-D-aspartic acid receptor structure and function. Physiol Rev. 1994 Jul;74(3):723–760. doi: 10.1152/physrev.1994.74.3.723. [DOI] [PubMed] [Google Scholar]
  55. McGurk J. F., Bennett M. V., Zukin R. S. Polyamines potentiate responses of N-methyl-D-aspartate receptors expressed in xenopus oocytes. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9971–9974. doi: 10.1073/pnas.87.24.9971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature. 1991 Nov 7;354(6348):31–37. doi: 10.1038/354031a0. [DOI] [PubMed] [Google Scholar]
  57. Nichols C. G., Makhina E. N., Pearson W. L., Sha Q., Lopatin A. N. Inward rectification and implications for cardiac excitability. Circ Res. 1996 Jan;78(1):1–7. doi: 10.1161/01.res.78.1.1. [DOI] [PubMed] [Google Scholar]
  58. Olney J. W. Excitotoxic amino acids and neuropsychiatric disorders. Annu Rev Pharmacol Toxicol. 1990;30:47–71. doi: 10.1146/annurev.pa.30.040190.000403. [DOI] [PubMed] [Google Scholar]
  59. Paoletti P., Neyton J., Ascher P. Glycine-independent and subunit-specific potentiation of NMDA responses by extracellular Mg2+. Neuron. 1995 Nov;15(5):1109–1120. doi: 10.1016/0896-6273(95)90099-3. [DOI] [PubMed] [Google Scholar]
  60. Parks T. N., Mueller A. L., Artman L. D., Albensi B. C., Nemeth E. F., Jackson H., Jasys V. J., Saccomano N. A., Volkmann R. A. Arylamine toxins from funnel-web spider (Agelenopsis aperta) venom antagonize N-methyl-D-aspartate receptor function in mammalian brain. J Biol Chem. 1991 Nov 15;266(32):21523–21529. [PubMed] [Google Scholar]
  61. Pegg A. E. Recent advances in the biochemistry of polyamines in eukaryotes. Biochem J. 1986 Mar 1;234(2):249–262. doi: 10.1042/bj2340249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Priestley T., Woodruff G. N., Kemp J. A. Antagonism of responses to excitatory amino acids on rat cortical neurones by the spider toxin, argiotoxin636. Br J Pharmacol. 1989 Aug;97(4):1315–1323. doi: 10.1111/j.1476-5381.1989.tb12594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Raditsch M., Ruppersberg J. P., Kuner T., Günther W., Schoepfer R., Seeburg P. H., Jahn W., Witzemann V. Subunit-specific block of cloned NMDA receptors by argiotoxin636. FEBS Lett. 1993 Jun 7;324(1):63–66. doi: 10.1016/0014-5793(93)81533-6. [DOI] [PubMed] [Google Scholar]
  64. Ragsdale D., Gant D. B., Anis N. A., Eldefrawi A. T., Eldefrawi M. E., Konno K., Miledi R. Inhibition of rat brain glutamate receptors by philanthotoxin. J Pharmacol Exp Ther. 1989 Oct;251(1):156–163. [PubMed] [Google Scholar]
  65. Ransom R. W., Stec N. L. Cooperative modulation of [3H]MK-801 binding to the N-methyl-D-aspartate receptor-ion channel complex by L-glutamate, glycine, and polyamines. J Neurochem. 1988 Sep;51(3):830–836. doi: 10.1111/j.1471-4159.1988.tb01818.x. [DOI] [PubMed] [Google Scholar]
  66. Rock D. M., MacDonald R. L. Spermine and related polyamines produce a voltage-dependent reduction of N-methyl-D-aspartate receptor single-channel conductance. Mol Pharmacol. 1992 Jul;42(1):157–164. [PubMed] [Google Scholar]
  67. Rock D. M., Macdonald R. L. The polyamine spermine has multiple actions on N-methyl-D-aspartate receptor single-channel currents in cultured cortical neurons. Mol Pharmacol. 1992 Jan;41(1):83–88. [PubMed] [Google Scholar]
  68. Scott R. H., Sutton K. G., Dolphin A. C. Interactions of polyamines with neuronal ion channels. Trends Neurosci. 1993 Apr;16(4):153–160. doi: 10.1016/0166-2236(93)90124-5. [DOI] [PubMed] [Google Scholar]
  69. Scott R. H., Sweeney M. I., Kobrinsky E. M., Pearson H. A., Timms G. H., Pullar I. A., Wedley S., Dolphin A. C. Actions of arginine polyamine on voltage and ligand-activated whole cell currents recorded from cultured neurones. Br J Pharmacol. 1992 May;106(1):199–207. doi: 10.1111/j.1476-5381.1992.tb14315.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Seeburg P. H. The role of RNA editing in controlling glutamate receptor channel properties. J Neurochem. 1996 Jan;66(1):1–5. doi: 10.1046/j.1471-4159.1996.66010001.x. [DOI] [PubMed] [Google Scholar]
  71. Sha Q., Romano C., Lopatin A. N., Nichols C. G. Spermidine release from xenopus oocytes. Electrodiffusion through a membrane channel. J Biol Chem. 1996 Feb 16;271(7):3392–3397. doi: 10.1074/jbc.271.7.3392. [DOI] [PubMed] [Google Scholar]
  72. Sheng M., Cummings J., Roldan L. A., Jan Y. N., Jan L. Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature. 1994 Mar 10;368(6467):144–147. doi: 10.1038/368144a0. [DOI] [PubMed] [Google Scholar]
  73. Shieh R. C., John S. A., Lee J. K., Weiss J. N. Inward rectification of the IRK1 channel expressed in Xenopus oocytes: effects of intracellular pH reveal an intrinsic gating mechanism. J Physiol. 1996 Jul 15;494(Pt 2):363–376. doi: 10.1113/jphysiol.1996.sp021498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Shyng S. L., Sha Q., Ferrigni T., Lopatin A. N., Nichols C. G. Depletion of intracellular polyamines relieves inward rectification of potassium channels. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):12014–12019. doi: 10.1073/pnas.93.21.12014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Silver M. R., DeCoursey T. E. Intrinsic gating of inward rectifier in bovine pulmonary artery endothelial cells in the presence or absence of internal Mg2+. J Gen Physiol. 1990 Jul;96(1):109–133. doi: 10.1085/jgp.96.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tabor C. W., Tabor H. Polyamines. Annu Rev Biochem. 1984;53:749–790. doi: 10.1146/annurev.bi.53.070184.003533. [DOI] [PubMed] [Google Scholar]
  77. Taglialatela M., Ficker E., Wible B. A., Brown A. M. C-terminus determinants for Mg2+ and polyamine block of the inward rectifier K+ channel IRK1. EMBO J. 1995 Nov 15;14(22):5532–5541. doi: 10.1002/j.1460-2075.1995.tb00240.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Tang C. M., Dichter M., Morad M. Modulation of the N-methyl-D-aspartate channel by extracellular H+. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6445–6449. doi: 10.1073/pnas.87.16.6445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Traynelis S. F., Cull-Candy S. G. Proton inhibition of N-methyl-D-aspartate receptors in cerebellar neurons. Nature. 1990 May 24;345(6273):347–350. doi: 10.1038/345347a0. [DOI] [PubMed] [Google Scholar]
  80. Traynelis S. F., Hartley M., Heinemann S. F. Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science. 1995 May 12;268(5212):873–876. doi: 10.1126/science.7754371. [DOI] [PubMed] [Google Scholar]
  81. Uehara A., Fill M., Vélez P., Yasukochi M., Imanaga I. Rectification of rabbit cardiac ryanodine receptor current by endogenous polyamines. Biophys J. 1996 Aug;71(2):769–777. doi: 10.1016/S0006-3495(96)79276-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Usherwood P. N., Blagbrough I. S. Spider toxins affecting glutamate receptors: polyamines in therapeutic neurochemistry. Pharmacol Ther. 1991 Nov;52(2):245–268. doi: 10.1016/0163-7258(91)90012-b. [DOI] [PubMed] [Google Scholar]
  83. Verdoorn T. A., Burnashev N., Monyer H., Seeburg P. H., Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science. 1991 Jun 21;252(5013):1715–1718. doi: 10.1126/science.1710829. [DOI] [PubMed] [Google Scholar]
  84. Wafford K. A., Bain C. J., Le Bourdelles B., Whiting P. J., Kemp J. A. Preferential co-assembly of recombinant NMDA receptors composed of three different subunits. Neuroreport. 1993 Sep 30;4(12):1347–1349. doi: 10.1097/00001756-199309150-00015. [DOI] [PubMed] [Google Scholar]
  85. Washburn M. S., Dingledine R. Block of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther. 1996 Aug;278(2):669–678. [PubMed] [Google Scholar]
  86. Weiger T., Hermann A. Polyamines block Ca(2+)-activated K+ channels in pituitary tumor cells (GH3). J Membr Biol. 1994 Jun;140(2):133–142. doi: 10.1007/BF00232901. [DOI] [PubMed] [Google Scholar]
  87. Wible B. A., Taglialatela M., Ficker E., Brown A. M. Gating of inwardly rectifying K+ channels localized to a single negatively charged residue. Nature. 1994 Sep 15;371(6494):246–249. doi: 10.1038/371246a0. [DOI] [PubMed] [Google Scholar]
  88. Williams G., Sallis J. D. Structure--activity relationship of inhibitors of hydroxyapatite formation. Biochem J. 1979 Oct 15;184(1):181–184. doi: 10.1042/bj1840181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Williams K., Dawson V. L., Romano C., Dichter M. A., Molinoff P. B. Characterization of polyamines having agonist, antagonist, and inverse agonist effects at the polyamine recognition site of the NMDA receptor. Neuron. 1990 Aug;5(2):199–208. doi: 10.1016/0896-6273(90)90309-4. [DOI] [PubMed] [Google Scholar]
  90. Williams K. Effects of Agelenopsis aperta toxins on the N-methyl-D-aspartate receptor: polyamine-like and high-affinity antagonist actions. J Pharmacol Exp Ther. 1993 Jul;266(1):231–236. [PubMed] [Google Scholar]
  91. Williams K., Kashiwagi K., Fukuchi J., Igarashi K. An acidic amino acid in the N-methyl-D-aspartate receptor that is important for spermine stimulation. Mol Pharmacol. 1995 Dec;48(6):1087–1098. [PubMed] [Google Scholar]
  92. Williams K. Mechanisms influencing stimulatory effects of spermine at recombinant N-methyl-D-aspartate receptors. Mol Pharmacol. 1994 Jul;46(1):161–168. [PubMed] [Google Scholar]
  93. Williams K. Modulation and block of ion channels: a new biology of polyamines. Cell Signal. 1997 Jan;9(1):1–13. doi: 10.1016/s0898-6568(96)00089-7. [DOI] [PubMed] [Google Scholar]
  94. Williams K., Romano C., Dichter M. A., Molinoff P. B. Modulation of the NMDA receptor by polyamines. Life Sci. 1991;48(6):469–498. doi: 10.1016/0024-3205(91)90463-l. [DOI] [PubMed] [Google Scholar]
  95. Williams K., Zappia A. M., Pritchett D. B., Shen Y. M., Molinoff P. B. Sensitivity of the N-methyl-D-aspartate receptor to polyamines is controlled by NR2 subunits. Mol Pharmacol. 1994 May;45(5):803–809. [PubMed] [Google Scholar]
  96. Wo Z. G., Oswald R. E. Transmembrane topology of two kainate receptor subunits revealed by N-glycosylation. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7154–7158. doi: 10.1073/pnas.91.15.7154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Wo Z. G., Oswald R. E. Unraveling the modular design of glutamate-gated ion channels. Trends Neurosci. 1995 Apr;18(4):161–168. doi: 10.1016/0166-2236(95)93895-5. [DOI] [PubMed] [Google Scholar]
  98. Yamada M., Kurachi Y. Spermine gates inward-rectifying muscarinic but not ATP-sensitive K+ channels in rabbit atrial myocytes. Intracellular substance-mediated mechanism of inward rectification. J Biol Chem. 1995 Apr 21;270(16):9289–9294. doi: 10.1074/jbc.270.16.9289. [DOI] [PubMed] [Google Scholar]
  99. Yamashita T., Horio Y., Yamada M., Takahashi N., Kondo C., Kurachi Y. Competition between Mg2+ and spermine for a cloned IRK2 channel expressed in a human cell line. J Physiol. 1996 May 15;493(Pt 1):143–156. doi: 10.1113/jphysiol.1996.sp021370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Yang J., Jan Y. N., Jan L. Y. Control of rectification and permeation by residues in two distinct domains in an inward rectifier K+ channel. Neuron. 1995 May;14(5):1047–1054. doi: 10.1016/0896-6273(95)90343-7. [DOI] [PubMed] [Google Scholar]
  101. Zhang L., Zheng X., Paupard M. C., Wang A. P., Santchi L., Friedman L. K., Zukin R. S., Bennett M. V. Spermine potentiation of recombinant N-methyl-D-aspartate receptors is affected by subunit composition. Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10883–10887. doi: 10.1073/pnas.91.23.10883. [DOI] [PMC free article] [PubMed] [Google Scholar]

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