Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells

Journal of Neurophysiology

Volumn 95, Issue 5, 2006, Pages 2866-2877

  Hoffpauir, Brian ^b   McMains, Emily ^a   Gleason, Evanna ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHLORIDE ION; GLYCINE; NITRIC OXIDE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CELL CULTURE; CELL LEVEL; CELL TYPE; CHANNEL GATING; CHLORIDE CURRENT; CHLORIDE TRANSPORT; CONTROLLED STUDY; CYTOSOL; EMBRYO; EMBRYO CULTURE; EXCITATORY JUNCTION POTENTIAL; GABAERGIC SYSTEM; HIPPOCAMPUS; MEMBRANE CURRENT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR INTRINSIC ACTIVITY; RETINA AMACRINE CELL; SIGNAL TRANSDUCTION; SYNAPTIC INHIBITION; SYNAPTIC MEMBRANE; VOLTAGE CLAMP;

AMACRINE CELLS; ANIMALS; ANIMALS, NEWBORN; BUMETANIDE; CELLS, CULTURED; CHICK EMBRYO; CYCLIC N-OXIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; FREE RADICAL SCAVENGERS; FUROSEMIDE; GAMMA-AMINOBUTYRIC ACID; GLYCINE; HIPPOCAMPUS; IMIDAZOLES; MEMBRANE POTENTIALS; MESYLATES; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NITRIC OXIDE; NITRIC OXIDE DONORS; PATCH-CLAMP TECHNIQUES; PENICILLAMINE; POTASSIUM; RATS; RATS, INBRED F344; RETINA; SODIUM; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SYNAPSES;

EID: 33646183694     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.01317.2005     Document Type: Article

References (49)

1. Ahern GP, Klyachko VA, and Jackson MB. cGMP and s-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517, 2002.
2. Biscoe TJ and Duchen MR. The anion selectivity of GABA-mediated post-synaptic potentials in mouse hippocampal cells. Q J Exp Physiol 70: 305-312, 1985.
3. Bormann J, Hamill OP, and Sakmann B. Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol 385: 243-86, 1987.
4. Blute TA, Lee MR, and Eldred WD. Direct imaging of NMDA-stimulated nitric oxide production in the retina. Vis Neurosci 17: 557-566, 2000.
5. Blute TA, Mayer B, and Eldred WD. Immunological and histochemical localization of nitric oxide synthase in the turtle retina. Vis Neurosci 14: 717-729, 1997.
6. Blute TA, Strang C, Keyser KT, and Eldred WD. Activation of the cGMP/nitric oxide signal transduction system by nicotine in the retina. Vis Neurosci 20: 165-176, 2003.
7. Cudeiro S and Rivadulla C. Sight and insight: on the physiological role of nitric oxide in the visual system. Trends Neurosci 22: 109-116, 1999.
8. Chun M, Oh S, Kim I, and Kim K. Light and electron microscopical analysis of nitric oxide synthase-like immunoreactive neurons in the rat retina. Vis Neurosci 16: 379-389, 1999.
9. Crousillac S, LeRouge M, Rankin M, and Gleason E. Immunolocalization of TRPC channel subunits 1 and 4 in the chicken retina. Vis Neurosci 20: 453-463, 2003.
10. Davis KL, Martin E, Turko IV, and Murad F. Novel effects of nitric oxide. Annu Rev Pharmacol Toxicol 41: 203-236, 2001.
11. Donati G, Pournaras CJ, Munoz JL, Poitry S, Poitry-Yamate CL, and Tsacopoulos M. Nitric oxide controls arteriolar tone in the retina of the miniature pig. Invest Ophthalmol Vis Sci 36: 2228-2237, 1995.
12. Dowling JE and Boycott BB. Neural connections of the retina: Fine structure of the inner plexiform layer. Cold Spring Harb Symp Quant Biol 30: 393-402, 1965.
13. Eldred WD and Blute TA. Imaging of nitric oxide in the retina. Vis Res 45: 3469-3486, 2005.
14. Faundez V and Hartzell HC. Intracellular chloride channels: determinants of function in the endosomal pathway. Science STKE 233: 1-8, 2004.
15. Fischer AJ and Stell WK. Nitric oxide synthase-containing cells in the retina, pigmented epithelium, choroid, and sclera of the chick eye. J Comp Neurol 405: 1-14, 1999.
16. +-ATPase of clathrin-coated vesicles is reversibly inhibited by S-Nitrosoglutathione. J Biol Chem 274: 1301-1305, 1999.
17. Gavrikov KE, Dmitriev AV, Keyser KT, and Mangel SC. Cation-chloride cotransporters mediate neural computation in the retina. Proc Natl Acad Sci USA 100: 16047-16052, 2003.
18. Gleason E, Borges S, and Wilson M. Synaptic transmission between pairs of retinal amacrine cells in culture. J Neurosci 13: 2359-2370, 1993.
19. Groppe M, Thanos S, Schuhmann W, and Heiduschka P. Measurement of nitric oxide production by the lesioned rat retina with a sensitive nitric oxide electrode. Anal Bioanal Chem 376: 797-807, 2003.
20. Hartveit E. Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 81: 2923-2936, 1999.
21. Heiduschka P and Thanos S. NO production during neuronal cell death can be directly assessed by a chemical reaction in vivo. Neuroreport 9: 4051-4057, 1998.
22. A receptor function in retinal amacrine cells. J Neurophysiol 88: 1766-1776, 2002.
23. Hölscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci 20: 298-303, 1997.
24. Huang RQ and Dillon GH. Effect of extracellular pH on GABA-activated current in rat recombinant receptors and thin hypothalamic slices. J Neurophysiol 82: 1233-1243, 1999.
25. Huba R and Hofmann HD. Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures. Visual Neurosci 6: 303-314, 1991.
26. Huba R, Schneider H, and Hofmann HD. Voltage gated currents of putative GABAergic amacrine cells in primary cultures and in the retinal slice preparation. Brain Res 577: 10-18, 1992.
27. - accumulation responsible for depolarizing GABAergic responses in mature hippocampal neurons. J Neurophysiol 90: 2752-2756, 2003.
28. Jentsch TJ, Stein V, Weinreich F, and Zdebik AA. Molecular structure and physiological function of chloride channels. Physiol Rev 82: 503-568, 2002.
29. - cotransport in rat central neurons. J Neurophysiol 84: 281-288, 2000.
30. Kim I, Lee E, Kim K, Ju W, Oh S, Joo C, and Chun M. Immunocytochemical localization of nitric oxide synthase in the mammalian retina. Neurosci Lett 267: 193-196, 1999.
31. Kolb H. Amacrine cells of the mammalian retina: neurocircuitry and functional roles. Eye 11: 904-923, 1997.
32. Langado L. Retinal processing: amacrine cells keep it short and sweet. Curr Biol 8: R593-R600, 1998.
33. Marc RE and Liu W. Fundamental GABAergic amacrine cell circuitries in the retina: nested feedback, concatenated inhibition, and axosomatic synapses. J Comp Neurol 425: 560-582, 2000.
34. Mills SL and Massey SC. Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377: 734-737, 1995.
35. Neal M, Cunningham J, and Matthews K. Selective release of nitric oxide from retinal amacrine and bipolar cells. Invest Ophthalmol Vis Sci 39: 850-853, 1998.
36. Payne JA, Rivera C, Voipio J, and Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199-206, 2003.
37. Ríos H, López-Costa JJ, Fosser NS, Brusco A, and Saavedra JP. Development of nitric oxide neurons in the chick embryo retina. Brain Res Dev Brain Res 120: 17-25, 2000.
38. Rogers PA, Eide L, Klungland A, and Ding H. Reversible inactivation of E. coli endonuclease III by nitric oxide via modification of its [4Fe-4S] cluster. DNA Repair 2: 809-817, 2003.
39. Russell JM. Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276, 2000.
40. Shin D, Lee H, Kim H, Lee E, Lu K, Lu W, Cho S, and Burk S. In situ localization of neuronal nitric oxide synthase (nNOS) mRNA in the rat retina. Neuroscience Lett 270: 53-55, 1999.
41. -] in recycling and late endosomes and Golgi complex measured using fluorescent ligands. J Cell Biol 160: 1129-1138, 2003.
42. Staley K, Smith R, Schaack J, Wilcox C, and Jentsch T. Alteration of GABAA receptor function following gene transfer of the CLC-2 chloride channel. Neuron 17: 543-551, 1996.
43. Stamler JS, Toone EJ, Lipton SA, and Sucher NJ. (S) NO signals: translocution, regulation and a consensus motif. Neuron 18: 691-696, 1997.
44. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl MR, Ruether K, Jahn H, Draguhn A, Jahn R, and Jentsch T. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29: 185-196, 2001.
45. Taylor R and Vaney D. New directions in retinal research. Trends Neurosci 26: 379-385, 2003.
46. Vardi N, Zhang LL, Payne JA, and Sterling P. Evidence that different cation choride cotransporters in retinal neruons allow opposite responses to GABA. J Neurosci 20: 7657-7663, 2000.
47. Wang G-Y, Liets LC, and Chalupa LM. Nitric oxide differentially modulates ON and OFF responses of retinal ganglion cells. J Neurophysiol 90: 1304-1313, 2003.
48. A receptor function via coactivation of cgmp-dependent kinase and phosphodiesterase. J Neurosci 18: 2342-2349, 1998.
49. Zheng J, Lee S, and Zhou ZJ. A developmental switch in the excitability and function of the starburst network in the mammalian retina. Neuron 44: 851-864, 2004.