Disruption of Slc4a10 augments neuronal excitability and modulates synaptic short-term plasticity

Frontiers in Cellular Neuroscience

Volumn 9, Issue June, 2015, Pages 1-9

  Sinning, Anne ^a,b   Liebmann, Lutz ^a   Hübner, Christian A ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

Field potential; GABAergic inhibition; LTP; Slc4a10; Synaptic plasticity

Indexed keywords

ANIMAL TISSUE; ARTICLE; ELECTROPHYSIOLOGICAL PROCEDURES; EVOKED RESPONSE; GENE DELETION; GENE DISRUPTION; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MOUSE; NERVE CELL EXCITABILITY; NONHUMAN; PROTEIN EXPRESSION; SPIKE WAVE; SYNAPTIC SHORT TERM PLASTICITY; SYNAPTIC TRANSMISSION;

EID: 84935858386     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00223     Document Type: Article

References (49)

1. Belengeanu, V., Gamage, T. H., Farcas, S., Stoian, M., Andreescu, N., Belengeanu, A., et al. (2014). A de novo 2.3 Mb deletion in 2q24.2q24.3 in a 20-month-old developmentally delayed girl. Gene 539, 168-172. doi: 10.1016/j.gene.2014.01.060
2. Ben-Ari, Y. (2002). Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
3. Blaesse, P., Airaksinen, M. S., Rivera, C., and Kaila, K. (2009). Cation-chloride cotransporters and neuronal function. Neuron 61, 820-838. doi: 10.1016/j.neuron.2009.03.003
4. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39. doi: 10.1038/361031a0
5. Burette, A. C., Weinberg, R. J., Sassani, P., Abuladze, N., Kao, L., and Kurtz, I. (2012). The sodium-driven chloride/bicarbonate exchanger in presynaptic terminals. J. Comp. Neurol. 520, 1481-1492. doi: 10.1002/cne.22806
6. Chapman, C. A., Perez, Y., and Lacaille, J. C. (1998). Effects of GABAA inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters. Hippocampus 8, 289-298. doi: 10.1002/(sici)1098-1063(1998)8:3<289::aid-hipo10>3.0.co;2-x
7. Chen, L. M., Kelly, M. L., Parker, M. D., Bouyer, P., Gill, H. S., Felie, J. M., et al. (2008). Expression and localization of Na-driven Cl-/HCO3−exchanger (SLC4A8) in rodent CNS. Neuroscience 153, 162-174. doi: 10.1016/j.neuroscience.2008.02.018
8. Chesler, M. (2003). Regulation and modulation of pH in the brain. Physiol. Rev. 83, 1183-1221. doi: 10.1152/physrev.00010.2003
9. Chesler, M., and Kaila, K. (1992). Modulation of pH by neuronal activity. Trends Neurosci. 15, 396-402. doi: 10.1016/0166-2236(92)90191-a
10. Damkier, H. H., Nielsen, S., and Praetorius, J. (2007). Molecular expression of SLC4-derived Na+-dependent anion transporters in selected human tissues. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R2136-R2146. doi: 10.1152/ajpregu.00356.2007
11. Daoudal, G., Hanada, Y., and Debanne, D. (2002). Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U S A 99, 14512-14517. doi: 10.1073/pnas.222546399
12. Davies, C. H., Davies, S. N., and Collingridge, G. L. (1990). Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol. 424, 513-531. doi: 10.1113/jphysiol.1990.sp018080
13. Davies, C. H., Starkey, S. J., Pozza, M. F., and Collingridge, G. L. (1991). GABA autoreceptors regulate the induction of LTP. Nature 349, 609-611. doi: 10.1038/349609a0
14. Debray, C., Diabira, D., Gaiarsa, J. L., Ben-Ari, Y., and Gozlan, H. (1997). Contributions of AMPA and GABAA receptors to the induction of NMDAR-dependent LTP in CA1. Neurosci. Lett. 238, 119-122. doi: 10.1016/s0304-3940(97)00865-3
15. Deisz, R. A., and Prince, D. A. (1989). Frequency-dependent depression of inhibition in guinea-pig neocortex in vitro by GABAB receptor feed-back on GABA release. J. Physiol. 412, 513-541. doi: 10.1113/jphysiol.1989.sp017629
16. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70. doi: 10.1038/19978
17. Farrant, M., and Kaila, K. (2007). The cellular, molecular and ionic basis of GABAA receptor signalling. Prog. Brain Res. 160, 59-87. doi: 10.1016/s0079-6123(06)60005-8
18. Gurnett, C. A., Veile, R., Zempel, J., Blackburn, L., Lovett, M., and Bowcock, A. (2008). Disruption of sodium bicarbonate transporter SLC4A10 in a patient with complex partial epilepsy and mental retardation. Arch. Neurol. 65, 550-553. doi: 10.1001/archneur.65.4.550
19. Hentschke, M., Wiemann, M., Hentschke, S., Kurth, I., Hermans-Borgmeyer, I., Seidenbecher, T., et al. (2006). Mice with a targeted disruption of the Cl−/HCO3−exchanger AE3 display a reduced seizure threshold. Mol. Cell. Biol. 26, 182-191. doi: 10.1128/mcb.26.1.182-191.2006
20. Hilgen, G., Huebner, A. K., Tanimoto, N., Sothilingam, V., Seide, C., Garrido, M. G., et al. (2012). Lack of the sodium-driven chloride bicarbonate exchanger NCBE impairs visual function in the mouse retina. PLoS One 7:e46155. doi: 10.1371/journal.pone.0046155
21. Hübner, C. A., Hentschke, M., Jacobs, S., and Hermans-Borgmeyer, I. (2004). Expression of the sodium-driven chloride bicarbonate exchanger NCBE during prenatal mouse development. Gene Expr. Patterns 5, 219-223. doi: 10.1016/j.modgep.2004.08.002
22. Hübner, C. A., and Holthoff, K. (2013). Anion transport and GABA signaling. Front. Cell. Neurosci. 7:177. doi: 10.3389/fncel.2013.00177
23. Jacobs, S., Ruusuvuori, E., Sipilä, S. T., Haapanen, A., Damkier, H. H., Kurth, I., et al. (2008). Mice with targeted Slc4a10 gene disruption have small brain ventricles and show reduced neuronal excitability. Proc. Natl. Acad. Sci. U S A 105, 311-316. doi: 10.1073/pnas.0705487105
24. Kaila, K., and Voipio, J. (1987). Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330, 163-165. doi: 10.1038/330163a0
25. Katz, B., and Miledi, R. (1968). The role of calcium in neuromuscular facilitation. J. Physiol. 195, 481-492. doi: 10.1113/jphysiol.1968.sp008469
26. Krepischi, A. C., Knijnenburg, J., Bertola, D. R., Kim, C. A., Pearson, P. L., Bijlsma, E., et al. (2010). Two distinct regions in 2q24.2-q24.3 associated with idiopathic epilepsy. Epilepsia 51, 2457-2460. doi: 10.1111/j.1528-1167.2010.02742.x
27. Leniger, T., Thöne, J., Bonnet, U., Hufnagel, A., Bingmann, D., and Wiemann, M. (2004). Levetiracetam inhibits Na+-dependent Cl−/HCO3− exchange of adult hippocampal CA3 neurons from guinea-pigs. Br. J. Pharmacol. 142, 1073-1080. doi: 10.1038/sj.bjp.0705836
28. Liebmann, L., Karst, H., Sidiropoulou, K., van Gemert, N., Meijer, O. C., Poirazi, P., et al. (2008). Differential effects of corticosterone on the slow afterhyperpolarization in the basolateral amygdala and CA1 region: possible role of calcium channel subunits. J. Neurophysiol. 99, 958-968. doi: 10.1152/jn.01137.2007
29. Lu, Y. M., Mansuy, I. M., Kandel, E. R., and Roder, J. (2000). Calcineurin- mediated LTD of GABAergic inhibition underlies the increased excitability of CA1 neurons associated with LTP. Neuron 26, 197-205. doi: 10.1016/s0896-6273(00)81150-2
30. Malenka, R. C., and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21. doi: 10.1016/j.neuron.2004.09.012
31. Markram, H., and Tsodyks, M. (1996). Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382, 807-810. doi: 10.1038/382807a0
32. Megías, M., Emri, Z., Freund, T., and Gulyás, A. (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527-540. doi: 10.1016/s0306-4522(00)00496-6
33. Pfeffer, C. K., Stein, V., Keating, D. J., Maier, H., Rinke, I., Rudhard, Y., et al. (2009). NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J. Neurosci. 29, 3419-3430. doi: 10.1523/JNEUROSCI.1377-08.2009
34. Praetorius, J., Nejsum, L. N., and Nielsen, S. (2004). A SCL4A10 gene product maps selectively to the basolateral plasma membrane of choroid plexus epithelial cells. Am. J. Physiol. Cell Physiol. 286, C601-C610. doi: 10.1152/ajpcell.00240.2003
35. Raimondo, J. V., Markram, H., and Akerman, C. J. (2012) Short-term ionic plasticity at GABAergic synapses. Front. Synaptic Neurosci. 4:5. doi: 10.3389/fnsyn.2012.00005
36. Redecker, C., Luhmann, H. J., Hagemann, G., Fritschy, J. M., and Witte, O. W. (2000) Differential downregulation of GABAA receptor subunits in widespread brain regions in the freeze-lesion model of focal cortical malformations. J. Neurosci. 20, 5045-5053.
37. Rivera, C., Voipio, J., and Kaila, K. (2005) Two developmental switches in GABAergic signalling: the K+-Cl‑ cotransporter KCC2 and carbonic anhydrase CAVII. J. Physiol. 562, 27-36. doi: 10.1113/jphysiol.2004.077495
38. Rivera, C., Voipio, J., Payne, J. A., Ruusuvuori, E., Lahtinen, H., Lamsa, K., et al. (1999). The K+/Cl− co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397, 251-255.
39. Romero, M. F., Chen, A. P., Parker, M. D., and Boron, W. F. (2013) The SLC4 family of bicarbonate HCO3− transporters. Mol. Aspects Med. 34, 159-182. doi: 10.1016/j.mam.2012.10.008
40. Sinning, A., and Hübner, C. A. (2013). Minireview: pH and synaptic transmission. FEBS Lett. 587, 1923-1928. doi: 10.1016/j.febslet.2013.04.045
41. Sinning, A., Liebmann, L., Kougioumtzes, A., Westermann, M., Bruehl, C., and Hübner, C. A. (2011). Synaptic glutamate release is modulated by the Na+-driven Cl−/HCO3− exchanger Slc4a8. J. Neurosci. 31, 7300-7311. doi: 10.1523/JNEUROSCI.0269-11.2011
42. Song, X., Yamasaki, M., Miyazaki, T., Konno, K., Uchigashima, M., and Watanabe, M. (2014). Neuron type- and input pathway-dependent expression of Slc4a10 in adult mouse brains. Eur. J. Neurosci. 40, 2797-2810. doi: 10.1111/ejn.12636
43. Staff, N. P., and Spruston, N. (2003). Intracellular correlate of EPSP-spike potentiation in CA1 pyramidal neurons is controlled by GABAergic modulation. Hippocampus 13, 801-805. doi: 10.1002/hipo.10129
44. Steffensen, S. C., and Henriksen, S. J. (1991). Effects of baclofen and bicuculline on inhibition in the fascia dentata and hippocampus regio superior. Brain Res. 538, 46-53. doi: 10.1016/0006-8993(91)90374-5
45. Stein, V., Hermans-Borgmeyer, I., Jentsch, T. J., and Hübner, C. A. (2004). Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J. Comp. Neurol. 468, 57-64. doi: 10.1002/cne.10983
46. Takesian, A. E., Kotak, V. C., and Sanes, D. H. (2010). Presynaptic GABAB receptors regulate experience-dependent development of inhibitory short-term plasticity. J. Neurosci. 30, 2716-2727. doi: 10.1523/JNEUROSCI.3903-09.2010
47. Wehr, M., and Zador, A. M. (2005) Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47, 437-445. doi: 10.1016/j.neuron.2005.06.009
48. Wigström, H., and Gustafsson, B. (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301, 603-604. doi: vcc10.1038/301603a0
49. Zucker, R., and Regehr, W. (2002) Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405. doi: 10.1146/annurev.physiol.64.092501.114547