Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling

Journal of Neuroscience

Volumn 27, Issue 30, 2007, Pages 8101-8111

  Szabadits, Eszter ^a   Cserép, Csaba ^a   Ludányi, Anikó ^a   Katona, István ^a   Gracia Llanes, Javier ^b   Freund, Tamás F ^a   Nyíri, Gábor ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

cGMP; GABAergic plasticity; Interneuron; Mouse; Rat; Retrograde signaling

Indexed keywords

CHOLECYSTOKININ; CYCLIC GMP; GUANYLATE CYCLASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PARVALBUMIN; SOMATOSTATIN; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2;

ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BETA CHAIN; CELL TYPE; CONTROLLED STUDY; DENDRITE; GABAERGIC SYSTEM; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER; NITRIC OXIDE SIGNALING; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; GUANYLATE CYCLASE; HIPPOCAMPUS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 34547475403     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1912-07.2007     Document Type: Article

References (93)

1. Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
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. Ando M, Tatematsu T, Kunii S, Nagata Y (1994) The intercellular communication via nitric oxide and its regulation in coupling of cyclic GMP synthesis upon stimulation of muscarinic cholinergic receptors in rat superior cervical sympathetic ganglia. Brain Res 650:283-288.
4. Arancio O, Antonova I, Gambaryan S, Lohmann SM, Wood JS, Lawrence DS, Hawkins RD (2001) Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation. J Neurosci 21:143-149.
5. Bellamy TC, Garthwaite J (2001) Sub-second kinetics of the nitric oxide receptor, soluble guanylyl cyclase, in intact cerebellar cells. J Biol Chem 276:4287-4292.
6. Bellamy TC, Wood J, Goodwin DA, Garthwaite J (2000) Rapid desensitization of the nitric oxide receptor, soluble guanylyl cyclase, underlies diversity of cellular cGMP responses. Proc Natl Acad Sci USA 97:2928-933.
7. Blackshaw S, Eliasson MJ, Sawa A, Watkins CC, Krug D, Gupta A, Arai T, Ferrante RJ, Snyder SH (2003) Species, strain and developmental variations in hippocampal neuronal and endothelial nitric oxide synthase clarify discrepancies in nitric oxide-dependent synaptic plasticity. Neuroscience 119:979-90.
8. Bon CL, Garthwaite J (2003) On the role of nitric oxide in hippocampal long-term potentiation. J Neurosci 23:1941-1948.
9. Borda E, Berra A, Saravia M, Ganzinelli S, Sterin-Borda L (2005) Correlations between neuronal nitric oxide synthase and muscarinic M3/M1 receptors in the rat retina. Exp Eye Res 80:391-399.
10. Boulton CL, Irving AJ, Southam E, Potier B, Garthwaite J, Collingridge GL (1994) The nitric oxide-cyclic GMP pathway and synaptic depression in rat hippocampal slices. Eur J Neurosci 6:1528-1535.
11. Bredt DS, Snyder SH (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
12. Brenman JE, Chao DS, Gee SH, McGee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia H, Peters MF, Froehner SC, Bredt DS (1996) Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84:757-767.
13. Burette A, Zabel U, Weinberg RJ, Schmidt HH, Valtschanoff JG (2002) Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J Neurosci 22:8961-8970.
14. Burgunder JM, Cheung PT (1994) Expression of soluble guanylyl cyclase gene in adult rat brain. Eur J Neurosci 6:211-217.
15. Castoldi AF, Manzo L, Costa LG (1993) Cyclic GMP formation induced by muscarinic receptors is mediated by nitric oxide synthesis in rat cortical primary cultures. Brain Res 610:57-61.
16. Charych EI, Yu W, Li R, Serwanski DR, Miralles CP, Li X, Yang BY, Pinal N, Walikonis R, De Blas AL (2004) A four PDZ domain-containing splice variant form of GRIP1 is localized in GABAergic and glutamatergic synapses in the brain. J Biol Chem 279:38978-38990.
17. Christopherson KS, Hillier BJ, Lim WA, Bredt DS (1999) PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 274:27467-27473.
18. Cuadra AE, El-Fakahany EE (2005) Mechanisms of M(1) muscarinic receptor-mediated up-regulation of neuronal nitric oxide synthase in N1E-115 neuroblastoma cells. Brain Res Mol Brain Res 134:198-204.
19. Daniel H, Levenes C, Crepel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci 21:401-407.
20. de Vente J, Asan E, Gambaryan S, Markerink-van Ittersum M, Axer H, Gallatz K, Lohmann SM, Palkovits M (2001) Localization of cGMP-dependent protein kinase type II in rat brain. Neuroscience 108:27-49.
21. Ding JD, Burette A, Nedvetsky PI, Schmidt HH, Weinberg RJ (2004) Distribution of soluble guanylyl cyclase in the rat brain. J Comp Neurol 472:437-448.
22. Domek-Lopacinska K (2005) Cyclic GMP metabolism and its role in brain physiology. J Physiol Pharmacol 56 [Suppl 2]:15-34.
23. Doyle C, Holscher C, Rowan MJ, Anwyl R (1996) The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J Neurosci 16:418-424.
24. Edwards TM, Rickard NS (2007) New perspectives on the mechanisms through which nitric oxide may affect learning and memory processes. Neurosci Biobehav Rev 31:413-425.
25. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290:1364-1368.
26. Feil S, Zimmermann P, Knorn A, Brummer S, Schlossmann J, Hofmann F, Feil R (2005) Distribution of cGMP-dependent protein kinase type I and its isoforms in the mouse brain and retina. Neuroscience 135:863-868.
27. Forstermann U, Schmidt HH, Pollock JS, Sheng H, Mitchell JA, Warner TD, Nakane M, Murad F (1991) Isoforms of nitric oxide synthase. Characterization and purification from different cell types. Biochem Pharmacol 42:1849-1857.
28. Freund TF (2003) Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
29. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
30. Friebe A, Mergia E, Dangel O, Lange A, KoeslingD (2007) Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase. Proc Natl Acad Sci USA 104:7699-7704.
31. Garthwaite J, Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706.
32. Gibb BJ, Garthwaite J (2001) Subunits of the nitric oxide receptor, soluble guanylyl cyclase, expressed in rat brain. Eur J Neurosci 13:539-544.
33. Gibb BJ, Wykes V, Garthwaite J (2003) Properties of NO-activated guanylyl cyclases expressed in cells. Br J Pharmacol 139:1032-1040.
34. Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239-3249.
35. Hawkins RD, Son H, ArancioO (1998) Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
36. Hobbs AJ (1997) Soluble guanylate cyclase: the forgotten sibling. Trends Pharmacol Sci 18:484-491.
37. Hu J, el-Fakahany EE (1993) Role of intercellular and intracellular communication by nitric oxide in coupling of muscarinic receptors to activation of guanylate cyclase in neuronal cells. J Neurochem 61:578-585.
38. 2+-dependent inositol 1,4,5-trisphosphate and nitric oxide signaling in cerebellar neurons. J Pharmacol Sci 100:538-544.
39. Jinno S, Kosaka T (2000) Colocalization of parvalbumin and somatostatin-like immunoreactivity in the mouse hippocampus: quantitative analysis with optical dissector. J Comp Neurol 428:377-388.
40. Jinno S, Kosaka T (2002) Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 449:1-25.
41. Jinno S, Kosaka T (2004) Patterns of colocalization of neuronal nitric oxide synthase and somatostatin-like immunoreactivity in the mouse hippocampus: quantitative analysis with optical disector. Neuroscience 124:797-808.
42. Jinno S, Kosaka T (2006) Cellular architecture of the mouse hippocampus: a quantitative aspect of chemically defined GABAergic neurons with stereology. Neurosci Res 56:229-245.
43. Kali S, Freund TF (2005) Distinct properties of two major excitatory inputs to hippocampal pyramidal cells: a computational study. Eur J Neurosci 22:2027-2048.
44. 1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558.
45. Kingston PA, Zufall F, Barnstable CJ (1996) Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function. Proc Natl Acad Sci USA 93:10440-10445.
46. Kittler JT, Arancibia-Carcamo IL, Moss SJ (2004) Association of GRIP1 with a GABA(A) receptor associated protein suggests a role for GRIP1 at inhibitory synapses. Biochem Pharmacol 68:1649-1654.
47. Kleppisch T, Pfeifer A, Klatt P, Ruth P, Montkowski A, Fassler R, Hofmann F (1999) Long-term potentiation in the hippocampal CA1 region of mice lacking cGMP-dependent kinases is normal and susceptible to inhibition of nitric oxide synthase. J Neurosci 19:48-55.
48. Klyachko VA, Ahern GP, Jackson MB (2001) cGMP-mediated facilitation in nerve terminals by enhancement of the spike afterhyperpolarization. Neuron 31:1015-1025.
49. Kobialka M, Gorczyca WA (2000) Particulate guanylyl cyclases: multiple mechanisms of activation. Acta Biochim Pol 47:517-528.
50. Koesling D (1999) Studying the structure and regulation of soluble guanylyl cyclase. Methods 19:485-493.
51. Koesling D, Russwurm M, Mergia E, Mullershausen F, Friebe A (2004) Nitric oxide-sensitive guanylyl cyclase: structure and regulation. Neurochem Int 45:813-819.
52. Kosaka T, Kosaka K, Tateishi K, Hamaoka Y, Yanaihara N, Wu JY, Hama K (1985) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J Comp Neurol 239:420-430.
53. Koylu EO, Kanit L, Taskiran D, Dagci T, Balkan B, Pogun S (2005) Effects of nitric oxide synthase inhibition on spatial discrimination learning and central DA2 and mACh receptors. Pharmacol Biochem Behav 81:32-40.
54. Kraus MM, Prast H (2002) Involvement of nitric oxide, cyclic GMP and phosphodiesterase 5 in excitatory amino acid and GABA release in the nucleus accumbens evoked by activation of the hippocampal fimbria. Neuroscience 112:331-343.
55. Krumenacker JS, Hanafy KA, Murad F (2004) Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res Bull 62:505-515.
56. Levey AI (1996) Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc Natl Acad Sci USA 93:13541-13546.
57. Levey AI, Edmunds SM, Koliatsos V, Wiley RG, Heilman CJ (1995) Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation. J Neurosci 15:4077-4092.
58. Li DP, Chen SR, Finnegan TF, Pan HL (2004) Signalling pathway of nitric oxide in synaptic GABA release in the rat paraventricular nucleus. J Physiol (Lond) 554:100-110.
59. Liu C, Ding JM, Faiman LE, Gillette MU (1997) Coupling of muscarinic cholinergic receptors and cGMP in nocturnal regulation of the suprachiasmatic circadian clock. J Neurosci 17:659-666.
60. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185-1193.
61. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol (Lond) 497:119-130.
62. Magee J, Hoffman D, Colbert C, Johnston D (1998) Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60:327-346.
63. Makhinson M, Opazo P, Carlisle HJ, Godsil B, Grant SG, O'Dell TJ (2006) A novel role for cyclic guanosine 3′,5′ monophosphate signaling in synaptic plasticity: a selective suppressor of protein kinase A-dependent forms of long-term potentiation. Neuroscience 140:415-431.
64. 2+ influx. J Neurosci 16:1702-1709.
65. Mergia E, Friebe A, Dangel O, Russwurm M, Koesling D (2006) Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J Clin Invest 116:1731-1737.
66. Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43:109-142.
67. Monfort P, Munoz MD, Kosenko E, Felipo V (2002) Long-term potentiation in hippocampus involves sequential activation of soluble guanylate cyclase, cGMP-dependent protein kinase, and cGMP-degrading phosphodiesterase. J Neurosci 22:10116-10122.
68. Monfort P, Munoz MD, Kosenko E, Llansola M, Sanchez-Perez A, Cauli O, Felipo V (2004) Sequential activation of soluble guanylate cyclase, protein kinase G and cGMP-degrading phosphodiesterase is necessary for proper induction of long-term potentiation in CA1 of hippocampus. Alterations in hyperammonemia. Neurochem Int 45:895-901.
69. Muller BM, Kistner U, Veh RW, Cases-Langhoff C, Becker B, Gundelfinger ED, Garner CC (1995) Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J Neurosci 15:2354-2366.
70. Namiki S, Kakizawa S, Hirose K, Iino M (2005) NO signalling decodes frequency of neuronal activity and generates synapse-specific plasticity in mouse cerebellum. J Physiol (Lond) 566:849-863.
71. Nugent FS, Penick EC, Kauer JA (2007) Opioids block long-term potentiation of inhibitory synapses. Nature 446:1086-1090.
72. Nyiri G, Freund TF, Somogyi P (2001) Input-dependent synaptic targeting of alpha(2)-subunit-containing GABA(A) receptors in synapses of hippocampal pyramidal cells of the rat. Eur J Neurosci 13:428-442.
73. Ozaki M, Shibuya I, Kabashima N, Isse T, Noguchi J, Ueta Y, Inoue Y, Shigematsu A, Yamashita H (2000) Preferential potentiation by nitric oxide of spontaneous inhibitory postsynaptic currents in rat supraoptic neurones. J Neuroendocrinol 12:273-281.
74. Pifarre P, Garcia A, Mengod G (2007) Species differences in the localization of soluble guanylyl cyclase subunits in monkey and rat brain. J Comp Neurol 500:942-957.
75. Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64:51-68.
76. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
77. Russwurm M, Koesling D (2002) Isoforms of NO-sensitive guanylyl cyclase. Mol Cell Biochem 230:159-164.
78. Russwurm M, Behrends S, Harteneck C, Koesling D (1998) Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem J 335:125-130.
79. Russwurm M, Wittau N, Koesling D (2001) Guanylyl cyclase/PSD-95 interaction: targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J Biol Chem 276:44647-44652.
80. Schnell SA, Staines WA, Wessendorf MW (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47:719-730.
81. Schulz S (2005) C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides 26:1024-1034.
82. Seress L, Abraham H, Hajnal A, Lin H, Totterdell S (2005) NOS-positive local circuit neurons are exclusively axo-dendritic cells both in the neoand archi-cortex of the rat brain. Brain Res 1056:183-190.
83. Tai C, Kuzmiski JB, MacVicar BA (2006) Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons. J Neurosci 26:6249-6258.
84. Teunissen C, Steinbusch H, Markerink-van Ittersum M, Koesling D, de Vente J (2001) Presence of soluble and particulate guanylyl cyclase in the same hippocampal astrocytes. Brain Res 891:206-212.
85. Tochio H, Mok YK, Zhang Q, Kan HM, Bredt DS, Zhang M (2000) Formation of nNOS/PSD-95 PDZ dimer requires a preformed beta-finger structure from the nNOS PDZ domain. J Mol Biol 303:359-370.
86. Van Staveren WC, Glick J, Markerink-van Ittersum M, Shimizu M, Beavo JA, Steinbusch HW, de Vente J (2002) Cloning and localization of the cGMP-specific phosphodiesterase type 9 in the rat brain. J Neurocytol 31:729-741.
87. Van Staveren WC, Steinbusch HW, Markerink-Van Ittersum M, Repaske DR, Goy MF, Kotera J, Omori K, Beavo JA, De Vente J (2003) mRNA expression patterns of the cGMP-hydrolyzing phosphodiesterases types 2, 5, and 9 during development of the rat brain. J Comp Neurol 467:566-580.
88. Vruwink M, Schmidt HH, Weinberg RJ, Burette A (2001) Substance P and nitric oxide signaling in cerebral cortex: anatomical evidence for reciprocal signaling between two classes of interneurons. J Comp Neurol 441:288-301.
89. Wendland B, Schweizer FE, Ryan TA, Nakane M, Murad F, Scheller RH, Tsien RW (1994) Existence of nitric oxide synthase in rat hippocampal pyramidal cells. Proc Natl Acad Sci USA 91:2151-2155.
90. Zabel U, Weeger M, La M, Schmidt HH (1998) Human soluble guanylate cyclase: functional expression and revised isoenzyme family. Biochem J 335:51-57.
91. Zagotta WN, Siegelbaum SA (1996) Structure and function of cyclic nucleotide-gated channels. Annu Rev Neurosci 19:235-263.
92. Zhuo M, Hu Y, Schultz C, Kandel ER, Hawkins RD (1994) Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 368:635-639.
93. Zorumski CF, Izumi Y (1998) Modulation of LTP induction by NMDA receptor activation and nitric oxide release. Prog Brain Res 118:173-182.