Nitric oxide potentiation of the homomeric ρ1 GABAC receptor function

British Journal of Pharmacology

Volumn 167, Issue 6, 2012, Pages 1369-1377

  Gasulla, J ^a   Beltran Gonzalez A N ^a   Calvo, D J ^a  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

Author keywords

GABA receptor; GABAC receptor; nitric oxide; retina; S nytrosylation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALANINE; COMPLEMENTARY RNA; CYSTEINE; ION CHANNEL; N ETHYLMALEIMIDE; NEUROTRANSMITTER RECEPTOR; NITRIC OXIDE; SCAVENGER; THIOL DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; GENE MUTATION; IN VITRO STUDY; NEUROTRANSMISSION; NITROSYLATION; NONHUMAN; OOCYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; SITE DIRECTED MUTAGENESIS; VOLTAGE CLAMP; WILD TYPE; XENOPUS LAEVIS;

ANIMALS; BENZOATES; ETHYL METHANESULFONATE; ETHYLMALEIMIDE; GAMMA-AMINOBUTYRIC ACID; HYDRAZINES; IMIDAZOLES; NITRIC OXIDE; NITRIC OXIDE DONORS; OOCYTES; RECEPTORS, GABA; S-NITROSOGLUTATHIONE; XENOPUS LAEVIS;

EID: 84867838715     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.02087.x     Document Type: Article

References (61)

1. + channels. J Physiol 520 (Pt 1): 165-176.
2. Ahern GP, Klyachko VA, Jackson MB, (2002). cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci 25: 510-517.
3. Amato A, Connolly CN, Moss SJ, Smart TG, (1999). Modulation of neuronal and recombinant GABAA receptors by redox reagents. J Physiol 517 (Pt 1): 35-50.
4. Amin J, Dickerson IM, Weiss DS, (1994). The agonist binding site of the gamma-aminobutyric acid type A channel is not formed by the extracellular cysteine loop. Mol Pharmacol 45: 317-323.
5. Bolotina VM, Najibi S, Palacino JJ, Pagano PJ, Cohen RA, (1994). Nitric oxide directly activates calcium-dependent potassium channels in vascular smooth muscle. Nature 368: 850-853.
6. Boue-Grabot E, Roudbaraki M, Bascles L, Tramu G, Bloch B, Garret M, (1998). Expression of GABA receptor rho subunits in rat brain. J Neurochem 70: 899-907.
7. Broillet MC, Firestein S, (1996). Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16: 377-385.
8. Calero CI, Calvo DJ, (2008). Redox modulation of homomeric rho1 GABA receptors. J Neurochem 105: 2367-2374.
9. Calero CI, Vickers E, Cid GM, Aguayo LG, von Gersdorff H, Calvo DJ, (2011). Allosteric modulation of retinal GABA receptors by ascorbic acid. J Neurosci 31: 9672-9682.
10. Castel H, Vaudry H, (2001). Nitric oxide directly activates GABA(A) receptor function through a cGMP/protein kinase-independent pathway in frog pituitary melanotrophs. J Neuroendocrinol 13: 695-705.
11. Castel H, Jegou S, Tonon MC, Vaudry H, (2000). Regulation of the GABA(A) receptor by nitric oxide in frog pituitary melanotrophs. Endocrinology 141: 3451-3460.
12. Chang Y, Weiss DS, (2002). Site-specific fluorescence reveals distinct structural changes with GABA receptor activation and antagonism. Nat Neurosci 5: 1163-1168.
13. Choi Y, Chen HV, Lipton SA, (2001). Three pairs of cysteine residues mediate both redox and zn2+ modulation of the nmda receptor. J Neurosci 21: 392-400.
14. Choi YB, Tenneti L, Le DA, Ortiz J, Bai G, Chen HS, et al,. (2000). Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat Neurosci 3: 15-21.
15. Cserep C, Szonyi A, Veres JM, Nemeth B, Szabadits E, de Vente J, et al,. (2011). Nitric oxide signaling modulates synaptic transmission during early postnatal development. Cereb Cortex 21: 2065-2074.
16. Dong CJ, Werblin FS, (1998). Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. J Neurophysiol 79: 2171-2180.
17. Eldred WD, Blute TA, (2005). Imaging of nitric oxide in the retina. Vision Res 45: 3469-3486.
18. Enz R, Brandstatter JH, Hartveit E, Wassle H, Bormann J, (1995). Expression of GABA receptor rho 1 and rho 2 subunits in the retina and brain of the rat. Eur J Neurosci 7: 1495-1501.
19. Eu JP, Sun J, Xu L, Stamler JS, Meissner G, (2000). The skeletal muscle calcium release channel: coupled O2 sensor and NO signaling functions. Cell 102: 499-509.
20. Farrant M, Nusser Z, (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229.
21. Fernhoff NB, Derbyshire ER, Marletta MA, (2009). A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc Natl Acad Sci U S A 106: 21602-21607.
22. Fukami S, Uchida I, Mashimo T, Takenoshita M, Yoshiya I, (1998). Gamma subunit dependent modulation by nitric oxide (NO) in recombinant GABAA receptor. Neuroreport 9: 1089-1092.
23. Garthwaite J, (2008). Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 27: 2783-2802.
24. Goutman JD, Escobar AL, Calvo DJ, (2005). Analysis of macroscopic ionic currents mediated by GABArho1 receptors during lanthanide modulation predicts novel states controlling channel gating. Br J Pharmacol 146: 1000-1009.
25. Groppe M, Thanos S, Schuhmann W, Heiduschka P, (2003). Measurement of nitric oxide production by the lesioned rat retina with a sensitive nitric oxide electrode. Anal Bioanal Chem 376: 797-807.
26. Hall CN, Garthwaite J, (2009). What is the real physiological NO concentration in vivo? Nitric Oxide 21: 92-103.
27. Hartveit E, (1999). Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 81: 2923-2936.
28. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS, (2005). Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6: 150-166.
29. Hoffpauir B, McMains E, Gleason E, (2006). Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells. J Neurophysiol 95: 2866-2877.
30. Hull C, Li GL, von Gersdorff H, (2006). GABA transporters regulate a standing GABAC receptor-mediated current at a retinal presynaptic terminal. J Neurosci 26: 6979-6984.
31. Jones SM, Palmer MJ, (2009). Activation of the tonic GABAC receptor current in retinal bipolar cell terminals by nonvesicular GABA release. J Neurophysiol 102: 691-699.
32. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
33. Kim WK, Choi YB, Rayudu PV, Das P, Asaad W, Arnelle DR, et al,. (1999). Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO. Neuron 24: 461-469.
34. Koulen P, Brandstatter JH, Enz R, Bormann J, Wassle H, (1998). Synaptic clustering of GABA(C) receptor rho-subunits in the rat retina. Eur J Neurosci 10: 115-127.
35. Kovacs R, Rabanus A, Otahal J, Patzak A, Kardos J, Albus K, et al,. (2009). Endogenous nitric oxide is a key promoting factor for initiation of seizure-like events in hippocampal and entorhinal cortex slices. J Neurosci 29: 8565-8577.
36. Ledo A, Barbosa RM, Gerhardt GA, Cadenas E, Laranjinha J, (2005). Concentration dynamics of nitric oxide in rat hippocampal subregions evoked by stimulation of the NMDA glutamate receptor. Proc Natl Acad Sci U S A 102: 17483-17488.
37. Lipton SA, Choi YB, Takahashi H, Zhang D, Li W, Godzik A, et al,. (2002). Cysteine regulation of protein function-as exemplified by NMDA-receptor modulation. Trends Neurosci 25: 474-480.
38. Lukasiewicz PD, Eggers ED, Sagdullaev BT, McCall MA, (2004). GABAC receptor-mediated inhibition in the retina. Vision Res 44: 3289-3296.
39. McGrath J, Drummond G, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
40. Maggesissi RS, Gardino PF, Guimaraes-Souza EM, Paes-de-Carvalho R, Silva RB, Calaza KC, (2009). Modulation of GABA release by nitric oxide in the chick retina: different effects of nitric oxide depending on the cell population. Vision Res 49: 2494-2502.
41. Matthews G, Ayoub GS, Heidelberger R, (1994). Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology. J Neurosci 14 (3 Pt 1): 1079-1090.
42. Means GE, Feeney RE, (1971). Alkylating and similar reagents. In:, Means GE, Feeney RE, (eds). Chemical Modification of Proteins. Holden-Day: San Francisco, CA, pp. 105-132.
43. Miledi R, Woodward RM, (1989). Effects of defolliculation on membrane current responses of Xenopus oocytes. J Physiol 416: 601-621.
44. Moncada S, Bolanos JP, (2006). Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97: 1676-1689.
45. Moss SJ, Smart TG, (2001). Constructing inhibitory synapses. Nat Rev Neurosci 2: 240-250.
46. Pan ZH, Zhang X, Lipton SA, (2000). Redox modulation of recombinant human GABA(A) receptors. Neuroscience 98: 333-338.
47. Poteser M, Romanin C, Schreibmayer W, Mayer B, Groschner K, (2001). S-nitrosation controls gating and conductance of the alpha 1 subunit of class C L-type Ca(2+) channels. J Biol Chem 276: 14797-14803.
48. Sedelnikova A, Smith CD, Zakharkin SO, Davis D, Weiss DS, Chang Y, (2005). Mapping the rho1 GABA(C) receptor agonist binding pocket. Constructing a complete model. J Biol Chem 280: 1535-1542.
49. Stamler JS, Lamas S, Fang FC, (2001). Nitrosylation. The prototypic redox-based signaling mechanism. Cell 106: 675-683.
50. Steinert JR, Chernova T, Forsythe ID, (2011). Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 16: 435-452.
51. Szabadits E, Cserep C, Ludanyi A, Katona I, Gracia-Llanes J, Freund TF, et al,. (2007). Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J Neurosci 27: 8101-8111.
52. Takahashi H, Shin Y, Cho SJ, Zago WM, Nakamura T, Gu Z, et al,. (2007). Hypoxia enhances S-nitrosylation-mediated NMDA receptor inhibition via a thiol oxygen sensor motif. Neuron 53: 53-64.
53. Wall MJ, (2003). Endogenous nitric oxide modulates GABAergic transmission to granule cells in adult rat cerebellum. Eur J Neurosci 18: 869-878.
54. Wang GY, van der List DA, Nemargut JP, Coombs JL, Chalupa LM, (2007). The sensitivity of light-evoked responses of retinal ganglion cells is decreased in nitric oxide synthase gene knockout mice. J Vis 7: 7. 1-13.
55. Wegelius K, Pasternack M, Hiltunen JO, Rivera C, Kaila K, Saarma M, et al,. (1998). Distribution of GABA receptor rho subunit transcripts in the rat brain. Eur J Neurosci 10: 350-357.
56. Wexler EM, Stanton PK, Nawy S, (1998). Nitric oxide depresses GABAA receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J Neurosci 18: 2342-2349.
57. Xu M, Akabas MH, (1993). Amino acids lining the channel of the gamma-aminobutyric acid type A receptor identified by cysteine substitution. J Biol Chem 268: 21505-21508.
58. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, et al,. (2006). Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2: 596-607.
59. Yu D, Eldred WD, (2005). Gycine and GABA interact to regulate the nitric oxide/cGMP signaling pathway in the turtle retina. Vis Neurosci 22: 825-838.
60. Zanelli S, Naylor M, Kapur J, (2009). Nitric oxide alters GABAergic synaptic transmission in cultured hippocampal neurons. Brain Res 1297: 23-31.
61. Zhang D, Pan ZH, Awobuluyi M, Lipton SA, (2001). Structure and function of GABA(C) receptors: a comparison of native versus recombinant receptors. Trends Pharmacol Sci 22: 121-132.