Nitric oxide signaling modulates synaptic transmission during early postnatal development

Cerebral Cortex

Volumn 21, Issue 9, 2011, Pages 2065-2074

  Cserép, Csaba ^a   Sznyi, András ^a   Veres, Judit M ^a   Németh, Beáta ^a   Szabadits, Eszter ^a   De Vente, Jan ^b   Hájos, Norbert ^a   Freund, Tamás F ^a   Nyiri, Gábor ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

GABAergic synapse; hippocampus; nNOS; retrograde signaling; synchronous activity

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CELLULAR DISTRIBUTION; ELECTRON MICROSCOPY; FEMALE; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION; WHOLE CELL;

ANIMALS; CALCIUM; CYCLIC GMP; ELECTROPHYSIOLOGICAL PHENOMENA; FLUORESCENT ANTIBODY TECHNIQUE; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GUANYLATE CYCLASE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NERVE NET; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 80051721946     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhq281     Document Type: Article

References (47)

1. Akerman CJ, Cline HT. 2007. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 30:382-389. (Pubitemid 47088714)
2. Allene C, Cattani A, Ackman J, Bonifazi P, Aniksztejn L, Ben-Ari Y, Cossart R. 2008. Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J Neurosci. 28:12851-12863.
3. 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. 97:2928-2933. (Pubitemid 30159274)
4. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. 2007. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev. 87:1215-1284. (Pubitemid 350041471)
5. Bernard C, Milh M, Morozov YM, Ben-Ari Y, Freund TF, Gozlan H. 2005. Altering cannabinoid signaling during development disrupts neuro-nal activity. Proc Natl Acad Sci USA. 102:9388-9393. (Pubitemid 40923573)
6. Blankenship A, Feller M. 2010. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci. 11:18-29.
7. Bon CL, Garthwaite J. 2003. On the role of nitric oxide in hippocampal long-term potentiation. J Neurosci. 23:1941-1948. (Pubitemid 36314749)
8. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, Represa A, Ben-Ari Y, Cossart R. 2009. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science. 326:1419-1424.
9. 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. (Pubitemid 35379066)
10. Cancedda L, Fiumelli H, Chen K, Poo MM. 2007. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci. 27:5224-5235. (Pubitemid 46741781)
11. Chang YC, Gottlieb DI. 1988. Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J Neurosci. 8:2123-2130.
12. Chung YH, Kim YS, Lee WB. 2004. Distribution of neuronal nitric oxide synthase-immunoreactive neurons in the cerebral cortex and hippocampus during postnatal development. J Mol Histol. 35:765-770. (Pubitemid 41404622)
13. Crepel V, Aronov D, Jorquera I, Represa A, Ben-Ari Y, Cossart R. 2007. A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron. 54:105-120. (Pubitemid 46522500)
14. de Vente J, Steinbusch HW, Schipper J. 1987. A new approach to immunocytochemistry of 3#,5#-cyclic guanosine monophosphate: preparation, specificity, and initial application of a new antiserum against formaldehyde-fixed 3#,5#-cyclic guanosine monophosphate. Neuroscience. 22:361-373. (Pubitemid 17106784)
15. Demyanenko GP, Halberstadt AI, Pryzwansky KB, Werner C, Hofmann F, Maness PF. 2005. Abnormal neocortical development in mice lacking cGMP-dependent protein kinase I. Brain Res Dev Brain Res. 160:1-8. (Pubitemid 41512801)
16. Dupuy ST, Houser CR. 1996. Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. J Neurosci. 16:6919-6932. (Pubitemid 26359373)
17. Dzhala V, Talos D, Sdrulla D, Brumback A, Mathews G, Benke T, Delpire E, Jensen F, Staley K. 2005. NKCC1 transporter facilitates seizures in the developing brain. Nat Med. 11:1205-1213. (Pubitemid 43093668)
18. Eilers J, Plant T, Marandi N, Konnerth A. 2001. GABA-mediated Ca2+ signalling in developing rat cerebellar Purkinje neurones. J Physiol. 536:429-437. (Pubitemid 32976124)
19. Garthwaite J. 2008. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci. 27:2783-2802. (Pubitemid 351832227)
20. Garthwaite J, Southam E, Boulton C, Nielsen E, Schmidt K, Mayer B. 1995. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol. 48:184-188.
21. Ge S, Goh E, Sailor K, Kitabatake Y, Ming G, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 439:589-593. (Pubitemid 43185382)
22. Giuili G, Luzi A, Poyard M, Guellaen G. 1994. Expression of mouse brain soluble guanylyl cyclase and NO synthase during ontogeny. Brain Res Dev Brain Res. 81:269-283. (Pubitemid 24277201)
23. Groneberg D, Koesling D, Friebe A. 2008. Evaluation of ODQ as specific inhibitor of NO-sensitive guanylyl cyclase using mice deficient for the enzyme. Basic Clin Pharmacol Toxicol. 102:40.
24. Hajos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O. 2009. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci. 29:319-327.
25. Khazipov R, Esclapez M, Caillard O, Bernard C, Khalilov I, Tyzio R, Hirsch J, Dzhala V, Berger B, Ben-Ari Y. 2001. Early development of neuronal activity in the primate hippocampus in utero. J Neurosci. 21:9770-9781. (Pubitemid 34184062)
26. Koesling D, Russwurm M, Mergia E, Mullershausen F, Friebe A. 2004. Nitric oxide-sensitive guanylyl cyclase: structure and regulation. Neurochem Int. 45:813-819. (Pubitemid 39108053)
27. 2+ responses in neonatal lateral superior olive neurons elicited by glycinergic/GABAergic synapses and action potentials. Neuroscience. 154:338-345.
28. Makara JK, Katona I, Nyiri G, Nemeth B, Ledent C, Watanabe M, de Vente J, Freund TF, Hajos N. 2007. Involvement of nitric oxide in depolarization-induced suppression of inhibition in hippocampal pyramidal cells during activation of cholinergic receptors. J Neurosci. 27:10211-10222. (Pubitemid 47450455)
29. McLean HA, Caillard O, Khazipov R, Ben-Ari Y, Gaiarsa JL. 1996. Spontaneous release of GABA activates GABAB receptors and controls network activity in the neonatal rat hippocampus. J Neurophysiol. 76:1036-1046. (Pubitemid 26284587)
30. Mohajerani MH, Cherubini E. 2006. Role of giant depolarizing potentials in shaping synaptic currents in the developing hippocampus. Crit Rev Neurobiol. 18:13-23. (Pubitemid 350194066)
31. Morales-Medina J, Mejorada A, Romero-Curiel A, Flores G. 2007. Alterations in dendritic morphology of hippocampal neurons in adult rats after neonatal administration of N-omega-nitro-L-arginine. Synapse. 61:785-789. (Pubitemid 47122752)
32. Murray AJ, Peace AG, Shewan DA. 2009. cGMP promotes neurite outgrowth and growth cone turning and improves axon regeneration on spinal cord tissue in combination with cAMP. Brain Res. 1294:12-21.
33. 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. 566:849-863. (Pubitemid 41122666)
34. Nikonenko I, Boda B, Steen S, Knott G, Welker E, Muller D. 2008. PSD-95 promotes synaptogenesis and multiinnervated spine formation through nitric oxide signaling. J Cell Biol. 183:1115-1127.
35. Nikonenko I, Jourdain P, Muller D. 2003. Presynaptic remodeling contributes to activity-dependent synaptogenesis. J Neurosci. 23:8498-8505. (Pubitemid 37158749)
36. Prast H, Philippu A. 2001. Nitric oxide as modulator of neuronal function. Prog Neurobiol. 64:51-68. (Pubitemid 32201889)
37. Sanchez-Islas E, Leon-Olea M. 2004. Nitric oxide synthase inhibition during synaptic maturation decreases synapsin I immunoreactivity in rat brain. Nitric Oxide. 10:141-149. (Pubitemid 38668663)
38. Sipila ST, Huttu K, Soltesz I, Voipio J, Kaila K. 2005. Depolarizing GABA acts on intrinsically bursting pyramidal neurons to drive giant depolarizing potentials in the immature hippocampus. J Neurosci. 25:5280-5289. (Pubitemid 40770906)
39. Sipila ST, Schuchmann S, Voipio J, Yamada J, Kaila K. 2006. The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J Physiol. 573:765-773. (Pubitemid 43852771)
40. Szabadits E, Cserep C, Ludanyi A, Katona I, Gracia-Llanes J, Freund TF, Nyiri G. 2007. Hippocampal GABAergic synapses possess the molecular machinery for retrograde nitric oxide signaling. J Neurosci. 27:8101-8111. (Pubitemid 47173310)
41. Tanaka J, Markerink-van Ittersum M, Steinbusch HW, De Vente J. 1997. Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia. 19:286-297. (Pubitemid 27165236)
42. 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. (Pubitemid 32115509)
43. 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 phos-phodiesterases types 2, 5, and 9 during development of the rat brain. J Comp Neurol. 467:566-580. (Pubitemid 37467131)
44. Vanhatalo S, Palva JM, Andersson S, Rivera C, Voipio J, Kaila K. 2005. Slow endogenous activity transients and developmental expression of K+-Cl-cotransporter 2 in the immature human cortex. Eur J Neurosci. 22:2799-2804. (Pubitemid 41811277)
45. Wang D, Kriegstein A. 2008. GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J Neurosci. 28:5547-5558.
46. Zhang P, Yu P, Tsang A, Chen Y, Fu A, Fu W, Chung K, Ip N. 2010. S-nitrosylation of cyclin-dependent kinase 5 (cdk5) regulates its kinase activity and dendrite growth during neuronal development. J Neurosci. 30:14366-14370.
47. Zufall F, Shepherd GM, Barnstable CJ. 1997. Cyclic nucleotide gated channels as regulators of CNS development and plasticity. Curr Opin Neurobiol. 7:404-412. (Pubitemid 27321034)