Nitric oxide activates leak K+ currents in the presumed cholinergic neuron of basal forebrain

Journal of Neurophysiology

Volumn 98, Issue 6, 2007, Pages 3397-3410

  Kang, Youngnam ^a,b   Dempo, Yoshie ^b   Ohashi, Atsuko ^b   Saito, Mitsuru ^a   Toyoda, Hiroki ^a   Sato, Hajime ^a   Koshino, Hisashi ^b   Maeda, Yoshinobu ^a   Hirai, Toshihiro ^b  

^a OSAKA UNIVERSITY   (Japan)

^b HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC GMP; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANOSINE TRIPHOSPHATE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; POTASSIUM; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FEMALE; FOREBRAIN; HYPERPOLARIZATION; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; VOLTAGE CLAMP;

ADENOSINE TRIPHOSPHATE; ANIMALS; BARIUM; CESIUM; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; FEMALE; FLUORESCENT DYES; GUANYLATE CYCLASE; MALE; NEURONS; NITRIC OXIDE; NITRIC OXIDE DONORS; PARASYMPATHETIC NERVOUS SYSTEM; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PROSENCEPHALON; RATS; RATS, WISTAR; S-NITROSO-N-ACETYLPENICILLAMINE; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 37549042323     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00536.2007     Document Type: Article

References (63)

1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Part IV. Internal organization of the cell, 14. Energy conversion: mitochondria and chloroplasts. In: Molecular Biology of the Cell. New York: Garland Science, 2002, p. 767-829.
2. ATP channels. J Physiol 554: 353-370, 2004.
3. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87: 1025-1035, 1996.
4. Ashcroft SJ, Ashcroft FM. Properties and functions of ATP-sensitive K channels. Cell Signal 2: 197-214, 1990.
5. ATP channel in normoxic and chronically hypoxic hearts by a cyclic GMP-dependent mechanism. J Mol Cell Cardiol 33: 331-341, 2001.
6. Bartus RT, Dean RL 3rd, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-414, 1982.
7. Beckman JS. The double-edged role of nitric oxide in brain function and superoxide-mediated injury. J Dev Physiol 15: 53-59, 1991.
8. Bereiter-Hahn J. Behavior of mitochondria in the living cell. Int Rev Cytol 122: 1-63, 1990.
9. Brorson JR, Schumacker PT, Zhang H. Nitric oxide acutely inhibits neuronal energy production. The Committees on Neurobiology and Cell Physiology. J Neurosci 19: 147-158, 1999.
10. Buerk DG, Ances BM, Greenberg JH, Detre JA. Temporal dynamics of brain tissue nitric oxide during functional forepaw stimulation in rats. Neuroimage 18: 1-9, 2003.
11. Chapman JB, Johnson EA, Kootsey JM. Electrical and biochemical properties of an enzyme model of the sodium pump. J Membr Biol 74: 139-153, 1983.
12. Chien WL, Liang KC, Teng CM, Kuo SC, Lee FY, Fu WM. Enhancement of learning behaviour by a potent nitric oxide-guanylate cyclase activator YC-1. Eur J Neurosci 21: 1679-1688, 2005.
13. Coyle JT, Price DL, DeLong MR. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219: 1184-1190, 1983.
14. + channels in urinary bladder myocytes through a c-GMP-dependent mechanism. Eur J Pharmacol 492: 13-19, 2004.
15. Dunnett SB, Fibiger HC. Role of forebrain cholinergic systems in learning and memory: relevance to the cognitive deficits of aging and Alzheimer's dementia. Prog Brain Res 98: 413-420, 1993.
16. Fass U, Panickar K, Personett D, Bryan D, Williams K, Gonzales J, Sugaya K, McKinney M. Differential vulnerability of primary cultured cholinergic neurons to nitric oxide excess. Neuroreport 11: 931-936, 2000.
17. Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N. Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2: 175-184, 2001.
18. Griffith WH, Matthews RT. Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci Lett 71: 169-174, 1986.
19. Gu Q. Contribution of acetylcholine to visual cortex plasticity. Neurobiol Learn Mem 80: 291-301, 2003.
20. Gui J, Song Y, Han NL, Sheu FS. Characterization of transcriptional regulation of neurogranin by nitric oxide and the role of neurogranin in SNP-induced cell death: implication of neurogranin in an increased neuronal susceptibility to oxidative stress. Int J Biol Sci 3: 212-224, 2007.
21. +-ATPase activity by endothelin in rabbit aorta. Am J Physiol Heart Circ Physiol 266: H577-582, 1994.
22. +-ATPase in the regulation of human corpus cavernosum smooth muscle contractility by nitric oxide. Br J Pharmacol 116: 2201-2206, 1995.
23. Hagiwara S. Membrane Potential-Dependent Ion Channels in Cell Membrane. Phylogenetic and Developmental Approaches. New York: Raven, 1983.
24. + channel in mouse neocortical neurons by nitric oxide. J Neurophysiol 95: 2167-2178, 2006.
25. Hanafy KA, Krumenacker JS, Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med Sci Monit 7: 801-819, 2001.
26. Hawkins RD, Son H, Arancio O. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118: 155-172, 1998.
27. Hewett SJ, Csernansky CA, Choi DW. Selective potentiation of NMDA-induced neuronal injury following induction of astrocytic iNOS. Neuron 13: 487-494, 1994.
28. Hille B. Ion Channels of Excitable Membranes (3rd ed.). Sunderland, MA: Sinauer, 2001.
29. Isaacs AM, Senn DB, Yuan M, Shine JP, Yankner BA. Acceleration of amyloid β-peptide aggregation by physiological concentrations of calcium. J Biol Chem 281: 27916-27923, 2006.
30. + pumps in mesencephalic trigeminal neurons. J Neurosci 24: 3694-3702, 2004.
31. + current in spike-initiation in primary sensory neurons of the rat mesencephalic trigeminal nucleus. J Neurophysiol 97: 2385-2393, 2007.
32. Kent C, Sugaya K, Bryan D, Personett D, McKinney M. Expression of superoxide dismutase messenger RNA in adult rat brain cholinergic neurons. J Mol Neurosci 12: 1-10, 1999.
33. Kopf SR, Benton RS, Kalfin R, Giovannini MG, Pepeu G. NO synthesis inhibition decreases cortical ACh release and impairs retention of a conditioned response. Brain Res 894: 141-144, 2001.
34. Kovacs R, Kardos J, Heinemann U, Kann O. Mitochondrial calcium ion and membrane potential transients follow the pattern of epileptiform discharges in hippocampal slice cultures. J Neurosci 25: 4260-4269, 2005.
35. Law A, Gauthier S, Quirion R. Say NO to Alzheimer's disease: the putative links between nitric oxide and dementia of the Alzheimer's type. Brain Res Brain Res Rev 35: 73-96, 2001.
36. Lizasoain I, Moro MA, Knowles RG, Darley-Usmar V, Moncada S. Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose. Biochem J 314: 877-880, 1996.
37. Markram H, Segal M. Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res 513: 171-174, 1990.
38. + pump as a site of action for carbon monoxide and glutamate: a mechanism for long-term modulation of cellular activity. Neuron 14: 781-794, 1995.
39. Nichols CG, Lopatin AN. Inward rectifier potassium channels. Annu Rev Physiol 59: 171-191, 1997.
40. Nixon RA. A "protease activation cascade" in the pathogenesis of Alzheimer's disease. Ann NY Acad Sci 924: 117-131, 2000.
41. O'Dell TJ, Hawkins RD, Kandel ER, Arancio O. Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc Natl Acad Sci USA 88: 11285-11289, 1991.
42. Pasqualotto BA, Vincent SR. Galanin and NADPH-diaphorase coexistence in cholinergic neurons of the rat basal forebrain. Brain Res 551: 78-86, 1991.
43. + channels. Trends Neurosci 24: 339-346, 2001.
44. Pierrot N, Santos SF, Feyt C, Morel M, Brion JP, Octave JN. Calcium-mediated transient phosphorylation of tau and amyloid precursor protein followed by intraneuronal amyloid-β accumulation. J Biol Chem 281: 39907-39914, 2006.
45. Pitsikas N, Rigamonti AE, Cella SG, Sakellaridis N, Muller EE. The nitric oxide donor molsidomine antagonizes age-related memory deficits in the rat. Neurobiol Aging 26: 259-264, 2005.
46. Radi R, Rodriguez M, Castro L, Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys 308: 89-95, 1994.
47. Ruiz-Stewart I, Tiyyagura SR, Lin JE, Kazerounian S, Pitari GM, Schulz S, Martin E, Murad F, Waldman SA. Guanylyl cyclase is an ATP sensor coupling nitric oxide signaling to cell metabolism. Proc Natl Acad Sci USA 101: 37-42, 2004.
48. Saito K, Elce JS, Hamos JE, Nixon RA. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc Natl Acad Sci USA 90: 2628-2632, 1993.
49. + current in initiation and invasion of spikes in rat mesencephalic trigeminal neurons. J Neurophysiol 96: 1887-1901, 2006.
50. Schuman EM, Madison DV. A requirement for the intercellular messenger nitric oxide in long-term potentiation. Science 254: 1503-1506, 1991.
51. + channel is a molecular substrate for neuronal effects of inhalation anesthetics. J Neurosci 20: 6347-6354, 2000.
52. Stanfield PR, Nakajima Y, Yamaguchi K. Substance P raises neuronal membrane excitability by reducing inward rectification. Nature 315: 498-501, 1985.
53. Sugaya K, McKinney M. Nitric oxide synthase gene expression in cholinergic neurons in the rat brain examined by combined immunocytochemistry and in situ hybridization histochemistry. Brain Res Mol Brain Res 23: 111-125, 1994.
54. Susswein AJ, Katzoff A, Miller N, Hurwitz I. Nitric oxide and memory. Neuroscientist 10: 153-162, 2004.
55. Tavalin SJ, Ellis EF, Satin LS. Inhibition of the electrogenic Na pump underlies delayed depolarization of cortical neurons after mechanical injury or glutamate. J Neurophysiol 77: 632-638, 1997.
56. + channels in the presumed cholinergic neuron of basal forebrain. Program No. 138.1/G28. 2007 Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience, 2007. Online.
57. Traut TW. Physiological concentrations of purines and pyrimidines. Mol Cell Biochem 140: 1-22, 1994.
58. Weitzdoerfer R, Hoeger H, Engidawork E, Engelmann M, Singewald N, Lubec G, Lubec B. Neuronal nitric oxide synthase knock-out mice show impaired cognitive performance. Nitric Oxide 10: 130-140, 2004.
59. + pump in isolated rabbit cardiac myocytes. J Physiol 565: 815-825, 2005.
60. Xu ZQ, de Vente J, Steinbusch H, Grillner S, Hokfelt T. The NO-cGMP pathway in the rat locus coeruleus: electrophysiological, immunohistochemical and in situ hybridization studies. Eur J Neurosci 10: 3508-3516, 1998.
61. Yamaguchi K, Nakajima Y, Nakajima S, Stanfield PR. Modulation of inwardly rectifying channels by substance P in cholinergic neurones from rat brain in culture. J Physiol 426: 499-520, 1990.
62. Zhang J, Dawson VL, Dawson TM, Snyder SH. Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science 263: 687-689, 1994.
63. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD. Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368: 635-639, 1994.