Astrocytic gap junction blockade markedly increases extracellular potassium without causing seizures in the mouse neocortex

Neurobiology of Disease

Volumn 101, Issue , 2017, Pages 1-7

  Bazzigaluppi, Paolo ^a,b   Weisspapir, Iliya ^a   Stefanovic, Bojana ^b,c   Leybaert, Luc ^d   Carlen, Peter L ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b Institute of Clinical Evaluative Sciences   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

4 AP; Extracellular potassium; GAP27; in vivo; Seizures; TAT GAP19

Indexed keywords

CARBENOXOLONE; CONNEXIN 43; FAMPRIDINE; POTASSIUM; MONOVALENT CATION; POTASSIUM CHANNEL;

ADULT; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CONTROLLED STUDY; ELECTRICAL SYNAPSE; EXTRACELLULAR POTASSIUM; EXTRACELLULAR SPACE; MOUSE; NEOCORTEX; NERVE CELL EXCITABILITY; NONHUMAN; SEIZURE; SOMATOSENSORY CORTEX; YOUNG ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GAP JUNCTION; METABOLISM; PHYSIOLOGY; SOMATOSENSORY EVOKED POTENTIAL;

ANIMALS; ASTROCYTES; CATIONS, MONOVALENT; CONNEXIN 43; EVOKED POTENTIALS, SOMATOSENSORY; GAP JUNCTIONS; MICE; NEOCORTEX; POTASSIUM; POTASSIUM CHANNELS; SEIZURES;

EID: 85010683031     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.12.017     Document Type: Article

References (64)

1. Abudara, V., Bechberger, J., Freitas-Andrade, M., De Bock, M., Wang, N., Bultynck, G., Naus, C.C., Leybaert, L., Giaume, C., The Connexin43 mimetic peptide Gap19 inhibits hemichannels without altering gap junctional communication in astrocytes. Front. Cell. Neurosci., 8(306), 2014.
2. Alonso, E., Vale, C., Sasaki, M., Fuwa, H., Konno, Y., Perez, S., Vieytes, M.R., Botana, L.M., Calcium oscillations induced by gambierol in cerebellar granule cells. J. Cell. Biochem. 110 (2010), 497–508.
3. Ammann, D., Ion-Selective Microelectrodes: Principles, Design and Application. 1986, Springer-Verlag, Berlin.
4. Avoli, M., de Curtis, M., Gabaergic synchronization in the limbic system and its role in the generation of epileptiform activity. Prog. Neurobiol. 95 (2011), 104–132.
5. Avoli, M., Barbarosie, M., Lucke, A., Nagao, T., Lopantsev, V., Kohling, R., Synchronous GABA-mediated potentials and epileptiform discharges in the rat limbic system in vitro. J. Neurosci. 16 (1996), 3912–3924.
6. Avoli, M., Louvel, J., Kurcewicz, Pumain, R., Barbarosie, M., Extracellular free potassium and calcium during synchronous activity induced by 4-aminopyridine in the juvenile rat hippocampus. J. Physiol. 493 (1996), 707–717.
7. Bazzigaluppi, P., Dufour, S., Carlen, P.L., Wide field fluorescent imaging of extracellular spatiotemporal potassium dynamics in vivo. NeuroImage 104 (2015), 110–116.
8. Blomstrand, F., Giaume, C., Kinetics of endothelin-induced inhibition and glucose permeability of astrocyte gap junctions. J. Neurosci. Res. 83 (2006), 996–1003.
9. Boitano, S., Evans, W.H., Connexin mimetic peptides reversibly inhibit Ca(2 +) signaling through gap junctions in airway cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 279 (2000), L623–L630.
10. Brand-Schieber, E., Werner, P., Iacobas, D.A., Iacobas, S., Beelitz, M., Lowery, S.L., Spray, D.C., Scemes, E., Connexin43, the major gap junction protein of astrocytes, is down-regulated in inflamed white matter in an animal model of multiple sclerosis. J. Neurosci. Res. 80 (2005), 798–808.
11. 2 + oscillations in cerebrocortical neurons. J. Pharmacol. Exp. Ther. 350 (2014), 615–623.
12. Connors, B.W., Tales of a dirty drug: carbenoxolone, gap junctions, and seizures. Epilepsy Currents/American Epilepsy Society 12 (2012), 66–68.
13. 2 + entry pathway. J. Biol. Chem. 287 (2012), 12250–12266.
14. Decrock, E., De Vuyst, E., Vinken, M., Van Moorhem, M., Vranckx, K., Wang, N., Van Laeken, L., De Bock, M., D'Herde, K., Lai, C.P., Rogiers, V., Evans, W.H., Naus, C.C., Leybaert, L., Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ. 16 (2009), 151–163.
15. Dufour, S., Dufour, P., Chever, O., Vallee, R., Amzica, F., In vivo simultaneous intra- and extracellular potassium recordings using a micro-optrode. J. Neurosci. Methods 194 (2011), 206–217.
16. Evans, W.H., Boitano, S., Connexin mimetic peptides: specific inhibitors of gap-junctional intercellular communication. Biochem. Soc. Trans. 29 (2001), 606–612.
17. Evans, W.H., Leybaert, L., Mimetic peptides as blockers of connexin channel-facilitated intercellular communication. Cell Commun. Adhes. 14 (2007), 265–273.
18. Fertziger, A.P., Ranck, J.B. Jr., Potassium accumulation in interstitial space during epileptiform seizures. Exp. Neurol. 26 (1970), 571–585.
19. Florence, G., Dahlem, M.A., Almeida, A.C., Bassani, J.W., Kurths, J., The role of extracellular potassium dynamics in the different stages of ictal bursting and spreading depression: a computational study. J. Theor. Biol. 258 (2009), 219–228.
20. Frohlich, F., Bazhenov, M., Iragui-Madoz, V., Sejnowski, T.J., Potassium dynamics in the epileptic cortex: new insights on an old topic. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry 14 (2008), 422–433.
21. Giaume, C., Leybaert, L., Naus, C.C., Saez, J.C., Connexin and pannexin hemichannels in brain glial cells: properties, pharmacology, and roles. Front. Pharmacol., 17, 2013, 4 (88).
22. 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., Effects of gap junction blockers on human neocortical synchronization. Neurobiol. Dis. 22 (2006), 496–508.
23. Green, J.D., The hippocampus. Physiol. Rev. 44 (1964), 561–608 [PubMed].
24. Haas, H.L., Jefferys, J.G., Low-calcium field burst discharges of CA1 pyramidal increas in rat hippocampal slices. J. Physiol. 354 (1984), 185–201.
25. Heinemann, U., Lux, H.D., Gutnick, M.J., Extracellular free calcium and potassium during increasing activity in the cerebral cortex of the cat. Exp. Brain Res. 27 (1977), 237–243.
26. Jahromi, S.S., Wentlandt, K., Piran, S., Carlen, P.L., Anticonvulsant actions of gap junctional blockers in an in vitro seizure model. J. Neurophysiol. 88:4 (2002), 1893–1902.
27. Jefferys, J.G., Haas, H.L., Synchronized bursting of CA1 hippocampal pyramidal cells in the absence of synaptic transmission. Nature 300 (1982), 448–450.
28. Judge, S.I., Bever, C.T. Jr., Potassium channel blockers in multiple sclerosis: neuronal Kv channels and effects of symptomatic treatment. Pharmacol. Ther. 111 (2006), 224–259.
29. Kofuji, P., Newman, E.A., Potassium buffering in the central nervous system. Neuroscience 129 (2004), 1045–1056.
30. Kohling, R., Lucke, A., Nagao, T., Speckmann, E.J., Avoli, M., Extracellular potassium elevations in the hippocampus of rats with long-term pilocarpine seizures. Neurosci. Lett. 201 (1995), 87–91.
31. Kunzelmann, P., Schroder, W., Traub, O., Steinhauser, C., Dermietzel, R., Willecke, K., Late onset and increasing expression of the gap junction protein Connexin30 in adult murine brain and long-term cultured astrocytes. Glia 25 (1999), 111–119.
32. Leybaert, L., Braet, K., Vandamme, W., Cabooter, L., Martin, P.E., Evans, W.H., Connexin channels, connexin mimetic peptides and ATP release. Cell Commun. Adhes. 10 (2003), 251–257.
33. Martin, P.E., Wall, C., Griffith, T.M., Effects of connexin-mimetic peptides on gap junction functionality and connexin expression in cultured vascular cells. Br. J. Pharmacol. 144 (2005), 617–627.
34. Mathie, A., Wooltorton, J.R., Watkins, C.S., Voltage-activated potassium channels in mammalian neurons and their block by novel pharmacological agents. Gen. Pharmacol. 30 (1998), 13–24.
35. Moody, W.J., Futamachi, K.J., Prince, D.A., Extracellular potassium activity during epileptogenesis. Exp. Neurol. 42 (1974), 248–263.
36. Nagy, J.I., Rash, J.E., Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Brain Res. Rev. 32 (2000), 29–44.
37. Newman, E.A., Regional specialization of retinal glial cell membrane. Nature 309 (1984), 155–157.
38. Newman, E.A., Inward-rectifying potassium channels in retinal glial (Muller) cells. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 13 (1993), 3333–3345.
39. Orkand, R.K., Nicholls, J.G., Kuffler, S.W., Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29 (1966), 788–806.
40. Pannasch, U., Freche, D., Dallerac, G., Ghezali, G., Escartin, C., Ezan, P., Cohen-Salmon, M., Benchenane, K., Abudara, V., Dufour, A., Lubke, J.H., Deglon, N., Knott, G., Holcman, D., Rouach, N., Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat. Neurosci. 17 (2014), 549–558.
41. Pedley, T.A., Fisher, R.S., Moody, W.J., Futamachi, K.J., Prince, D.A., Extracellular potassium activity during epileptogenesis: a comparison between neocortex and hippocampus. Trans. Am. Neurol. Assoc. 99 (1974), 41–45.
42. Raimondo, J.V., Burman, R.J., Katz, A.A., Akerman, C.J., Ion dynamics during seizures. Front. Cell. Neurosci., 9(419), 2015.
43. Rausche, G., Igelmund, P., Heinemann, U., Effects of changes in extracellular potassium, magnesium and calcium concentration on synaptic transmission in area CA1 and the dentate gyrus of rat hippocampal slices. Pflugers Arch. - Eur. J. Physiol. 415 (1990), 588–593.
44. Reddy, D.S., Kuruba, R., Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions. Int. J. Mol. Sci. 14 (2013), 18284–18318.
45. Rouach, N., Segal, M., Koulakoff, A., Giaume, C., Avignone, E., Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions. J. Physiol. 553 (2003), 729–745.
46. Rutecki, P.A., Lebeda, F.J., Johnston, D., Epileptiform activity induced by changes in extracellular potassium in hippocampus. J. Neurophysiol. 54 (1985), 1363–1374.
47. Sagar, G.D., Larson, D.M., Carbenoxolone inhibits junctional transfer and upregulates Connexin43 expression by a protein kinase A-dependent pathway. J. Cell. Biochem. 98 (2006), 1543–1551.
48. Samoilova, M., Wentlandt, K., Adamchik, Y., Velumian, A.A., Carlen, P.L., Connexin 43 mimetic peptides inhibit spontaneous epileptiform activity in organotypic hippocampal slice cultures. Exp. Neurol. 210 (2008), 762–775.
49. Scemes, E., Spray, D.C., Extracellular K(+) and astrocyte signaling via connexin and pannexin channels. Neurochem. Res. 37 (2012), 2310–2316.
50. Sohl, G., Maxeiner, S., Willecke, K., Expression and functions of neuronal gap junctions. Nat. Rev. Neurosci. 6 (2005), 191–200.
51. Somjen, G.G., Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. Physiol. Rev. 81 (2001), 1065–1096.
52. Tapia, R., Sitges, M., Effect of 4-aminopyridine on transmitter release in synaptosomes. Brain Res. 250 (1982), 291–299.
53. Taylor, C.P., Dudek, F.E., Synchronous neural afterdischarges in rat hippocampal slices without active chemical synapses. Science 218 (1982), 810–812.
54. Thompson, R.J., Jackson, M.F., Olah, M.E., Rungta, R.L., Hines, D.J., Beazely, M.A., MacDonald, J.F., MacVicar, B.A., Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322 (2008), 1555–1559.
55. Thomsen, R.H., Wilson, D.F., Effects of 4-aminopyridine and 3,4-diaminopyridine on transmitter release at the neuromuscular junction. J. Pharmacol. Exp. Ther. 227 (1983), 260–265.
56. Tong, X., Ao, Y., Faas, G.C., Nwaobi, S.E., Xu, J., Haustein, M.D., Anderson, M.A., Mody, I., Olsen, M.L., Sofroniew, M.V., Khakh, B.S., Astrocyte Kir4.1 ion channel deficits contribute to neuronal dysfunction in Huntington's disease model mice. Nat. Neurosci. 17 (2014), 694–703.
57. Traynelis, S.F., Dingledine, R., Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J. Neurophysiol. 59 (1988), 259–276.
58. Vessey, J.P., Lalonde, M.R., Mizan, H.A., Welch, N.C., Kelly, M.E., Barnes, S., Carbenoxolone inhibition of voltage-gated Ca channels and synaptic transmission in the retina. J. Neurophysiol. 92 (2004), 1252–1256.
59. Wallraff, A., Kohling, R., Heinemann, U., Theis, M., Willecke, K., Steinhauser, C., The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 26 (2006), 5438–5447.
60. 2 + elevation. Basic Res. Cardiol., 107, 2012, 304.
61. 2 +-triggered Cx43 hemichannel opening. Neuropharmacology 75 (2013), 506–516.
62. Wang, N., et al. Selective inhibition of Cx43 hemichannels by Gap19 and its impact on myocardial ischemia/reperfusion injury. Basic Res. Cardiol., 108, 2013, 309.
63. Wang, L., Dufour, S., Valiante, T.A., Carlen, P.L., Extracellular Potassium and seizures: excitation, inhibition and the role of Ih. Int. J. Neural Syst., 26(8), 2016, 14.
64. Xu, L., Zeng, L.H., Wong, M., Impaired astrocytic gap junction coupling and potassium buffering in a mouse model of tuberous sclerosis complex. Neurobiol. Dis. 34 (2009), 291–299.