Is connexin36 critical for GABAergic hypersynchronization in the hippocampus?

Journal of Physiology

Volumn 589, Issue 7, 2011, Pages 1663-1680

  Beaumont, Michael ^a   Maccaferri, Gianmaria ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOPYRIDINE; BETA CARBOLINE; CARBENOXOLONE; CONNEXIN 36; MEFLOQUINE; PREGNENOLONE;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; DRUG TARGETING; EPILEPSY; EPILEPTIC DISCHARGE; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GAP JUNCTION; GENOTYPE; HIPPOCAMPUS; IN VITRO STUDY; INTERNEURON; KNOCKOUT MOUSE; MOUSE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL DETECTION; STIMULUS RESPONSE; STRATUM LACUNOSUM MOLECULARE; SYNAPTIC TRANSMISSION; WILD TYPE;

4-AMINOPYRIDINE; ANIMALS; ANTICONVULSANTS; CARBENOXOLONE; CONNEXINS; EPILEPSY; GAMMA-AMINOBUTYRIC ACID; GAP JUNCTIONS; HIPPOCAMPUS; INTERNEURONS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PREGNENOLONE; RECEPTORS, GABA-A;

EID: 79953138392     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.201491     Document Type: Article

References (85)

1. Avoli M (1996). GABA-mediated synchronous potentials and seizure generation. Epilepsia 37, 1035-1042.
2. Avoli M, Barbarosie M, Lücke A, Nagao T, Lopantsev V & Köhling R (1996). Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J Neurosci 16, 3912-3924.
3. Avoli M, D'Antuono, Louvel J, Kohling R, Biagini G, Pumain R, D'Arcangelo G & Tancredi V (2002). Network and pharmacological mechanisms leading to epileptiform synchronization in the limbic system in vitro. Prog Neurobiol 68, 167-207.
4. A receptor. Nat Rev Neurosci 6, 565-575.
5. Bennett MVL (1977). Electrical transmission: a functional analysis and comparison to chemical transmission. In Handbook of Physiology, section 1, The Nervous System, vol. I, Cellular Biology of Neurons, ed. Kandel EK, pp. 357-416. Williams & Wilkins, Baltimore.
6. Bennett MV & Pereda A (2006). Pyramid power: principal cells of the hippocampus unite! Brain Cell Biol 35, 5-11.
7. Belluardo N, Mudò G, Trovato-Salinaro A, Le Gurun S, Charollais A, Serre Beinier V, Amato G, Haefliger JA, Meda P & Condorelli DF (2000). Expression of connexin36 in the adult and developing rat brain. Brain Res 865, 121-138.
8. Buhl DL, Harris KD, Hormuzdi SG, Monyer H & Buzsáki G (2003). Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 23, 1013-1018.
9. Chepkova AN, Sergeeva OA & Haas HL (2008). Carbenoxolone impairs LTP and blocks NMDA receptors in murine hippocampus. Neuropharmacology 55, 139-147.
10. Cohen I, Navarro C, Clemenceau S, Baulac M & Miles R (2002). On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418-1421.
11. Cruikshank SJ, Hopperstad M, Younger M, Connors BW, Spray DC & Srinivas M (2004). Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc Natl Acad Sci U S A 101, 12364-12369.
12. A receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 127, 1626-1640.
13. Davidson JS & Baumgarten IM (1988). Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. Structure-activity relationships. J Pharmacol Exp Ther 246, 1104-1107.
14. Deans MR, Gibson JR, Sellitto C, Connors BW & Paul DL (2001). Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31, 477-485.
15. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
16. A receptor-mediated current. J Physiol 550, 679-691.
17. 2+/calmodulin-dependent kinase II at mixed synapses on the mauthner cell: colocalization and association with connexin 35. J Neurosci 30, 9488-9499.
18. Freund TF & Buzsaki G (1996). Interneurons of the Hippocampus. Hippocampus 6, 347-470.
19. Fujiwara-Tsukamoto Y, Isomura Y, Imanishi M, Ninomiya T, Tsukada M, Yanagawa Y, Fukai T & Takada M (2010). Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J Neurosci 30, 13679-13689.
20. Gajda Z, Gyengesi E, Hermesz E, Ali KS & Szente M (2003). Involvement of gap junctions in the manifestation and control of the duration of seizures in rats in vivo. Epilepsia 44, 1596-1600.
21. Gajda Z, Szupera Z, Blazso G & Szente M (2005). Quinine, a blocker of neuronal Cx36 chennels, suppresses seizure activity in rat neocortex in vivo. Epilepsia 46, 1581-1591.
22. Gajda Z, Hermesz E, Gyengesi E, Szupera Z & Szente M (2006). The functional significance of gap junction channels in the epileptogenicity and seizure susceptibility of juvenile rats. Epilepsia 47, 1009-1022.
23. Galarreta M & Hestrin S (1999). A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72-75.
24. Galarreta M & Hestrin S (2001). Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2, 425-433.
25. Gibson JR, Beierlein M & Connors BW (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79.
26. Gigout S, Louvel J, Kawasaki H, D'Antuono M, Armand V, Kurcewicz I, Olivier A, Laschet J, Turak B, Devaux B, Pumain R & Avoli M (2006). Effects of gap junction blockers on human neocortical synchronization. Neurobiol Dis 22, 496-508.
27. Glykys J, Dzhala VI, Kuchibhotla KV, Feng G, Kuner T, Augustine G, Bacskai BJ & Staley KJ (2009). Differences in cortical versus subcortical GABAergic signaling: a candidate mechanism of electroclinical uncoupling of neonatal seizures. Neuron 63, 657-672.
28. Gonzalez-Sulser A, Wang J, Motamedi GK, Avoli M, Vicini S & Dzakpasu R (2011). The 4-aminopyridine in vitro epilepsy model analyzed with a perforated multi-electrode array. Neuropharmacology (in press).
29. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA & Monyer H (2001). Impaired electrical signaling disrupts gamma frequency oscillations in connexin36-deficient mice. Neuron 31, 487-495.
30. Huberfeld G, Wittner L, Clemenceau S, Baulac M, Kaila K, Miles R & Rivera C (2007). Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J Neurosci 27, 9866-9873.
31. Hunkeler W, Möhler H, Pieri L, Polc P, Bonetti EP, Cumin R, Schaffner R & Haefely W (1981). Selective antagonists of benzodiazepines. Nature 290, 514-516.
32. Jahromi SS, Wentlandt K, Piran S & Carlen PL (2002). Anticonvulsant actions of gap junctional blockers in an in vitro seizure model. J Neurophysiol 88, 1893-1902.
33. Juszczak GR & Swiergiel AH (2009). Properties of gap junction blockers and their behavioural, cognitive and electrophysiological effects: animal and human studies. Prog Neuropsychopharmacol Biol Psychiatry 33, 181-198.
34. B receptors are blocked. J Neurophysiol 93, 2656-2667.
35. Kettenmann H & Ransom BR (1988). Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia 1, 64-73.
36. Klaassen A, Glykys J, Maguire J, Labarca C, Mody I & Boulter J (2006). Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy. Proc Natl Acad Sci U S A 103, 19152-19157.
37. Lamsa K & Kaila K (1997). Ionic mechanisms of spontaneous GABAergic events in rat hippocampal slices exposed to 4-aminopyridine. J Neurophysiol 78, 2582-2591.
38. A receptor action in SP-O interneurons in the rat hippocampal CA3 area. J Neurophsiol 90, 1983-1995.
39. Maccaferri G & Lacaille JC (2003). Interneuron Diversity series: Hippocampal interneuron classifications - making things as simple as possible, not simpler. Trends Neurosci 26, 564-571.
40. MacVicar BA & Dudek FE (1981). Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213, 782-785.
41. Maier N, Güldenagel M, Söhl G, Siegmund H, Willecke K & Draguhn A (2002). Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin36-deficient mice. J Physiol 541, 521-528.
42. Majewska MD, Mienville JM & Vicini S (1988). Neurosteroid pregnenolone sulfate antagonizes electrophysiological responses to GABA in neurons. Neurosci Lett 90, 279-284.
43. Mancilla JG, Lewis TJ, Pinto DJ, Rinzel J & Connors BW (2007). Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J Neurosci 27, 2058-2073.
44. Margineanu DG & Klitgaard H (2001). Can gap-junction blockade preferentially inhibit neuronal hypersynchrony vs. excitability? Neuropharmacology 41, 377-383.
45. Medina-Ceja L, Cordero-Romero A & Morales-Villagrán A (2008). Antiepileptic effect of carbenoxolone on seizures induced by 4-aminopyridine: a study in the rat hippocampus and entorhinal cortex. Brain Res 1187, 74-81.
46. Meldrum BS & Rogawski MA (2007). Molecular targets for antiepileptic drug development. Neurotherapeutics 4, 18-61.
47. Meme W, Vandecasteele M, Giaume C & Venance L (2009). Electrical coupling between hippocampal astrocytes in rat brain slices. Neurosci Res 63, 236-243.
48. Menichella DM, Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS & Paul DL (2006). Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 26, 10984-10991.
49. Mercer A, Bannister AP & Thomson AM (2006). Electrical coupling between pyramidal cells in adult cortical regions. Brain Cell Biol 35, 13-27.
50. A receptor-mediated currents via a reduction of channel opening frequency. Brain Res 489, 190-194.
51. Motulsky H (2010). Intuitive Biostatistic, 2nd edn. Oxford University Press, New York.
52. Nagy JI, Dudek FE & Rash JE (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res Brain Res Rev 47, 191-215.
53. A receptor pharmacology and subtype mRNA expression in human neuronal NT2-N cells. J Neurosci 18, 4993-5007.
54. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Büssow H, Schilling K, Steinhäuser C & Willecke K (2003). Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci 23, 4549-4559.
55. Pais I, Hormuzdi SG, Monyer H, Traub RD, Wood IC, Buhl EH, Whittington MA & LeBeau FE (2003). Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin36. J Neurophysiol 89, 2046-2054.
56. A receptor function through distinct sites. Brain Res 830, 72-87.
57. Perkins KL (2002). GABA application to hippocampal CA3 or CA1 stratum lacunosum-moleculare excites and interneuron network. J Neurophysiol 87, 1404-1414.
58. Perrault P & Avoli M (1992). 4-Aminopyridine-induced epileptiform activity and a GABA-mediated long-lasting depolarization in the rat hippocampus. J Neurosci 12, 104-115.
59. Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R & Capogna M (2005). Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25, 6775-6786.
60. Ross FM, Gwyn P, Spanswick D & Davies SN (2000). Carbenoxolone depresses spontaneous epileptiform activity in the CA1 region of rat hippocampal slices. Neuroscience 100, 789-796.
61. Rekling JC, Shao XM & Feldman JL (2000). Electrical coupling and excitatory synaptic transmission between rhythmogenic respiratory neurons in the preBötzinger complex. J Neurosci 20, RC113.
62. Rouach N, Segal M, Koulakoff A, Giaume C & Avignone E (2003). Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions. J Physiol 553, 729-745.
63. Rouach N, Koulakoff A, Abudara V, Willecke K & Giaume C (2008). Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322, 1551-1551.
64. Rutecki PA, Lebeda FJ & Johnston D (1987). 4-Aminopyridine produces epileptiform activity in hippocampus and enhances synaptic excitation and inhibition. J Neurophysiol 57, 1911-1924.
65. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U & Traub RD (2001). Axo-axonal coupling. A novel mechanism for ultrafast neuronal communication. Neuron 31, 831-840.
66. A receptor desensitization. J Neurosci 20, 3571-3579.
67. A receptor subtypes. Pharmacol Rev 47, 181-234.
68. A-dependent spontaneous synchronized activity mediated by the hippocampal interneuron network. J Neurophysiol 86, 381-391.
69. Staley KJ (2004). Role of the depolarizing GABA response in epilepsy. Adv Exp Med Biol 548, 104-109.
70. Szente M & Pongrácz F (1979). Aminopyridine-induced seizure activity. Electroencephalogr Clin Neurophysiol 46, 605-608.
71. Szente M, Gajda Z, Said Ali K & Hermesz E (2002). Involvement of electrical coupling in the in vivo ictal epileptiform activity induced by 4-aminopyridine in the neocortex. Neuroscience 115, 1067-1078.
72. Tovar KR, Maher BJ & Westbrook GL (2009). Direct actions of carbenoxolone on synaptic transmission and neuronal membrane properties. J Neurophysiol 102, 974-978.
73. Traub RD, Bibbig R, Piechotta A, Draguhn R & Schmitz D (2001). Synaptic and nonsynaptic contributions to giant IPSPs and ectopic spikes induced by 4-aminopyridine in the hippocampus in vitro. J Neurophysiol 85, 1246-1256.
74. Urschel S, Honer T, Schubert T, Alev C, Sohl G, Worsdorfer P, Asahara T, Dermietzel R, Weiler R & Willecke K (2006). Protein kinase A-mediated phosphorylation of connexin36 in mouse retina results in decreased gap junctional communication between AII amacrine cells. J Biol Chem 281, 33163-33171.
75. Venance L, Rozov A, Blatow M, Burnashev N, Feldmayer D & Monyer H (2000). Connexin expression in electrically coupled postnatal rat brain neurons. Proc Natl Acad Sci U S A 97, 10260-10265.
76. Vessey JP, Lalonde MR, Mizan HA, Welch NC, Kelly ME & Barnes S (2004). Carbenoxolone inhibitionof voltage-gated Ca channels and synaptic transmission in the retina. J Neurophysiol 92, 1252-1256.
77. Wallraff A, Köhling R, Heinemann U, Theis M, Willecke K & Steinhäuser C (2006). The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26, 5438-5447.
78. Wang Y, Barakat A & Zhou H (2010). Electrotonic coupling between pyramidal neurons in the neocortex. PLoS One 5, e10253.
79. Weickert S, Ray A, Zoidl G & Dermietzel R (2005). Expression of neural connexins and pannexin1 in the hippocampus and inferior olive: a quantitative approach. Brain Res Mol Brain Res, 133, 102-109.
80. Yamamoto T, Ochalski A, Hertzberg EL & Nagy JI (1990). On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. J Comp Neurol 302, 853-883.
81. Yang Q & Michelson HB (2001). Gap junctions synchronize the firing of inhibitory interneurons in guinea pig hippocampus. Brain Res 907, 139-143.
82. A receptor on the response to a neurosteroid. Eur J Pharmacol 225, 321-330.
83. Ziburkus J, Cressman JR, Barreto E & Schiff SJ (2006). Interneuron and pyramidal cell interplay during in vitro seizure-like events. J Neurophysiol 95, 3948-3954.
84. Zsiros V & Maccaferri G (2005). Electrical coupling between interneurons with different excitable properties in stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J Neurosci 25, 8686-8695.
85. Zsiros V, Aradi I & Maccaferri G (2007). Propagation of postsynaptic currents and potentials via gap junctions in GABAergic networks of the rat hippocampus. J Physiol 578, 527-544.