Mechanism of cGMP-gated channel block by intracellular polyamines

Journal of General Physiology

Volumn 115, Issue 6, 2000, Pages 783-797

  Gou, Donglin ^a   Lu, Zhe ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Diamine; Ion permeation; Polyamine; Protonation; Retinal cyclic guanine monophosphate gated channel

Indexed keywords

CYCLIC GMP; CYCLIC NUCLEOTIDE; ION CHANNEL; POLYAMINE; PUTRESCINE; SPERMINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MOLECULAR BIOLOGY; MUTATION; NONHUMAN; OOCYTE; PROTEIN STRUCTURE; PROTON TRANSPORT;

ANIMALS; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; HYDROGEN-ION CONCENTRATION; ION CHANNEL GATING; ION CHANNELS; KINETICS; MEMBRANE POTENTIALS; MODELS, MOLECULAR; MUTAGENESIS; OOCYTES; PROTEIN CONFORMATION; PROTONS; PUTRESCINE; SPERMINE; XENOPUS LAEVIS;

EID: 0342493313     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.115.6.783     Document Type: Article

References (63)

1. Albert, A., and E.P. Serjeant. 1971. The determination of ionization constants (a laboratory manual). Chapman and Hall Ltd. London, UK.
2. Araneda, R.C., R.S. Zukin, and M.V.L. Bennett. 1993. Effects of polyamines on NMDA-induced currents in rat hippocampal neurons: a whole-cell and single channel study. Neurosci. Lett. 152: 107-112.
3. Ault, B., R.H. Evans, A.A. Francis, D.J. Oakes, and J.C. Witkins. 1980. Selective depression of excitatory amino acid induced depolarization by magnesium ions in isolated spinal cord preparations. J. Physiol. 307:413-428.
4. Bader, C.R., P.R. Macleish, and E.A. Schwartz. 1979. A voltage-clamp study of the light response in solitary rods of the tiger salamander. J. Physiol. 296:1-26.
5. Bähring, R., D. Bowie, M. Benveniste, and M.L. Mayer. 1997. Permeation and block of the rat GluR6 glutamate receptor channels by internal and external polyamines. J. Physiol. 502:575-589.
6. Bastian, B.L., and G.L. Fein. 1982. The effects of sodium replacement on the responses of toad rods. J. Physiol. 330:331-347.
7. Baylor, D.A., and B.J. Nunn. 1986. Electrical properties of the light-sensitive conductance of salamander rods. J. Physiol. 371:115-145.
8. Benveniste, M., and M.L. Mayer. 1993. Multiple effects of spermine on N-methyl-D-aspartic acid receptor responses of rat cultured hippocampal neurons. J. Physiol. 464:131-163.
9. Bododia, R.D., and P.B. Detwiler. 1985. Patch-clamp recordings of the light-sensitive dark noise in retinal rods from the lizard and frog. J. Physiol. 367:183-216.
10. Bowie, D., and M.L. Mayer. 1995. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron. 15:453-462.
11. Bowie, D., G.D. Lange, and M.L. Mayer. 1998. Activity-dependent modulation of glutamate receptors by polyamines. J. Neurosci. 18: 8175-8185.
12. Capovilla, M., A. Caretta, L. Cervetto, and V. Torre. 1983. Ionic movements through light-sensitive channels of toad rods. J. Physiol. 343:295-310.
13. 1-(n-octane-sulfonyl)-spermine, novel glutamate receptor antagonists: block and permeation of N-methyl-D-aspartate receptors. Mol. Pharmacol. 51:861-871.
14. Colamartino, G., A. Menini, and V. Torre. 1991. Blockade and permeation of divalent cations through the cyclic GMP-activated channel from tiger salamander retinal rods. J. Physiol. 440:189-206.
15. Cu, C., R. Bähring, and M.L. Mayer. 1998. The role of hydrophobic interactions in binding of polyamines to non NMDA receptor ion channels. Neuropharmacology. 37:1381-1391.
16. 2+-permeable α-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors. Proc. Natl. Acad. Sci. USA. 92:9298-9302.
17. 2+ blockage, and ion selectivity. Proc. Natl. Acad. Sci. USA. 91: 1109-1113.
18. + channels is caused by intracellular spermine. Cell 80:149-154.
19. + channels. Science. 266:1068-1072.
20. Fodor, A.A., S.E. Gordon, and W.N. Zagotta. 1997. Mechanism of tetracaine block of cyclic nucleotide-gated channels. J. Gen. Physiol. 109:3-14.
21. Goulding, E.H., J. Ngai, R.H. Kramer, S. Colicos, R. Axel, S.A. Siegelbaum, and A. Chess. 1992. Molecular cloning and single channel properties of the cyclic nucleotide-gated channel from catfish olfactory neurons. Neuron. 8:45-58.
22. Goulding, E.H., G.R. Tibbs, D. Liu, and S.A. Siegelbaum. 1993. Role of H5 domain in determining pore diameter and ion permeation through cyclic nucleotide-gated channels. Nature. 364: 61-64.
23. Goulding, E.H, G.R. Tibbs, and S.A. Siegelbaum. 1994. Molecular mechanisms of cyclic-nucleotide-gated channel activation. Nature. 327:369-374.
24. Guo, D., and Z. Lu. 2000. Mechanism of IRK1 channel block by intracellular polyamines. J. Gen. Physiol. 115:799-813.
25. Haghighi, A.P., and E. Cooper. 1998. Neuronal nicotinic acetylcholine receptors are blocked by intracellular spermine in a voltage-dependent manner. J. Neurosci. 18:4050-4062.
26. Haynes, L.W., A.R. Kay, and K.-W. Yau. 1986. Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature. 321:66-70.
27. Hodgkin, A.L., P.A. McNaughton, B.J. Nunn, and K.-W. Yau. 1984. Effects of ions on retinal rods from Bufo marinus. J. Physiol. 350: 649-680.
28. Hodgkin, A.L., P.A. McNaughton, and B.J. Nunn. 1985. The ion selectivity and calcium dependence of the light-sensitive pathway in toad rods. J. Physiol. 358:447-468.
29. Horie, M., H. Irisawa, and A. Noma. 1987. Voltage-dependent magnesium block of adenosine-triphosphate-sensitive potassium channel in guinea-pig ventricular cells. J. Physiol. 387:251-272.
30. Ifune, C.K., and J.H. Steinback. 1991. Voltage-dependent block by magnesium of neuronal nicotinic acetylcholine receptor channel in rat phaeochromocytoma cells. J. Physiol. 443:683-701.
31. Igarashi, K., and K. Williams. 1995. Antagonist properties of polyamines and bis(ethyl)polyamines at N-methyl-D-aspartate receptors. J. Pharmacol. Exp. Ther. 272:1101-1109.
32. 2+ permeable AMPA receptor channels. Neuroreport. 6:2045-2048.
33. Kamboj, S.K., G.T. Swanson, and S.G Cull-Candy. 1995. Intracellular spermine confers rectification on rat calcium permeable AMPA and kainate receptors. J. Physiol. 486:297-303.
34. Kaupp, U.B., T. Niidome, T. Tanabe, S. Terada, W. Baningk, W. Stühmer, N. Cook, K. Kangawa, H. Matsuo, T. Hirose, and S. Numa. 1989. Primary structure and functional expression from complementary DNA of rod photoreceptor cyclic GMP-gated channel. Nature. 342:283-292.
35. 2+-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J. Physiol. 486:305-312.
36. + channel determined by construction of multimeric cDNAs. Neuron. 9:861-871.
37. Lopatin, A.N., E.N. Makhaaina, and C.G. Nichols. 1994. Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature. 372:366-369.
38. Lu, Z., and L. Ding. 1999. Blockade of a retinal cGMP-gated channel by polyamines. J. Gen. Physiol. 113:35-43.
39. Mathie, A., D. Colquhoun, and S.G. Cull-Candy. 1990. Rectification of currents activated by nicotinic receptors in rat sympathetic ganglion neurons. J. Physiol. 427:625-655.
40. 2+. Nature. 325:156-159.
41. 2+ of NMDA responses in spinal cord neurons. Nature. 309:261-263.
42. + channel. J. Gen. Physiol. 79:869-891.
43. Nakatani, K., and K.-W. Yau. 1988. Calcium and magnesium fluxes across the plasma membrane of the toad rod outer segment. J. Physiol. 395:695-729.
44. Nowak, L., P. Bregestovski, P. Ascher, A. Herbet, and A. Prochiantz. 1984. Magnesium gates glutamate-activated channels in mouse central neurons. Nature. 307:462-465.
45. Palmer, B.B., and H.K.J. Powell. 1974. Complex formation between 4,9-diazododecane-1, 12-diamine (spermine) and copper(II) ions and protons in aqueous solution. J. Chem. Soc. Dalton Trans. 19:2086-2089.
46. Park, C.-S., and R. MacKinnon. 1995. Divalent cation selectivity in a cyclic nucleotide-gated ion channel. Biochemistry. 34:13326-13333.
47. Rock, D.M., and R.L. Macdonald. 1992a. The polyamine spermine has multiple actions on N-methyl-D-aspartate receptor single-channel currents in cultured cortical neurons. Mol. Pharmacol. 41:83-88.
48. Rock, D.M., and R.L. Macdonald. 1992b. Spermine and related polyamines produce a voltage-dependent reduction of N-methyl-D-aspartate receptor single-channel conductance. Mol. Pharmacol. 42:157-164.
49. Root, M.J., and R. MacKinnon. 1993. Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel. Neuron. 11:459-466.
50. Root, M.J., and R. MacKinnon. 1994. Two identical noninteracting sites in an ion channel revealed by proton transfer. Science. 256: 1852-1856.
51. Sands, S.B., and M.E. Barish. 1992. Neuronal nicotinic acetylcholine receptor currents in phaeochromocytoma (PC12) cells: dual mechanisms of rectification. J. Physiol. 447:467-487.
52. Stern, J.H., H. Knutsson, and P.R. Macleish. 1987. Divalent cations directly affect the conductance ot excised patches of rod photoreceptor membrane. Science. 236:1674-1678.
53. Sunderman, E.R., and W.N. Zagotta. 1999. Sequence of events underlying the allosteric transition of rod cyclic nucleotide-gated channels. J. Gen. Physiol. 113:621-640.
54. Torre, V., H.R. Matthews, and T.D. Lamb. 1987. Ion selectivity blockage and control of light-sensitive conductance. Neurosci. Res. Suppl. 6:S25-S44.
55. Vandenberg, C.A. 1987. Inward rectification of a potassium channel in cardiac ventricular cells depends on internal magnesium ions. Proc. Natl. Acad. Sci. USA. 84:2560-2564.
56. Varnum, M.D., K.D. Black, and W.N. Zagotta. 1995. Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channel. Neuron. 15:619-625.
57. Werblin, E.S. 1975. Regeneration of hyperpolarization in rods. J. Physiol. 244:53-81.
58. Williams, K. 1997. Modulation and block of ion channels: a new biology of polyamines. Cell. Signal. 9:1-13.
59. Woodruff, M.L., G.L. Fain, and B.L. Bastian. 1982. Light-dependent ion flux into toad photoreceptors. J. Gen. Physiol. 80:517-536.
60. Yau, K.-W., and D.A. Baylor. 1989. Cyclic GMP-activated conductance of retinal photoreceptor. Annu. Rev. Neurosci. 12:289-327.
61. Yau, K.-W., P.A. McNaughton, and A.L. Hodgkin. 1981. Effects of ions on the light-sensitive current in retinal rods. Nature. 292: 502-505.
62. Yau, K.-W., and K. Nakatini. 1984. Cation selectivity of light-sensitive conductance in retinal rods. Nature. 309:352-354.
63. Zimmerman, A.L., and D.A. Baylor. 1992. Cation interactions within the cyclic GMP-activated channel of retinal rods from the tiger salamander. J. Physiol. 449:759-783.