Development and regulation of chloride homeostasis in the central nervous system

Frontiers in Cellular Neuroscience

Volumn 9, Issue September, 2015, Pages

  Watanabe, Miho ^a   Fukuda, Atsuo ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; OXYTOCIN; POTASSIUM CHLORIDE COTRANSPORTER 2; SODIUM POTASSIUM CHLORIDE COTRANSPORTER 1;

CENTRAL NERVOUS SYSTEM; CHLORIDE HOMEOSTASIS; EMBRYO DEVELOPMENT; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; NONHUMAN; OLFACTORY BULB; ONTOGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; SYNAPTOGENESIS; TEMPORAL LOBE EPILEPSY;

EID: 84942933933     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00371     Document Type: Review

References (131)

1. Achilles, K., Okabe, A., Ikeda, M., Shimizu-Okabe, C., Yamada, J., Fukuda, A., et al. (2007). Kinetic properties of Cl-uptake mediated by Na+-dependent K+-2Cl-cotransport in immature rat neocortical neurons. J. Neurosci. 27, 8616-8627. doi: 10.1523/jneurosci.5041-06.2007
2. Aguado, F., Carmona, M. A., Pozas, E., Aguiló, A., Martínez-Guijarro, F. J., Alcantara, S., et al. (2003). BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl-co-transporter KCC2. Development 130, 1267-1280. doi: 10.1242/dev.00351
3. Alessi, D. R., Zhang, J., Khanna, A., Hochdorfer, T., Shang, Y., and Kahle, K. T. (2014). The WNK-SPAK/OSR1 pathway: Master regulator of cation-chloride cotransporters. Sci. Signal. 7, 1-11. doi: 10.1126/scisignal.2005365
4. Alvarez-Leefmans, F. J., León-Olea, M., Mendoza-Sotelo, J., Alvarez, F. J., Antón, B., and Garduo, R. (2001). Immunolocalization of the Na+-K+-2Cl-cotransporter in peripheral nervous tissue of vertebrates. Neuroscience 104, 569-582. doi: 10.1016/s0306-4522(01)00091-4
5. Banke, T. G., and Gegelashvili, G. (2008). Tonic activation of group I mGluRs modulates inhibitory synaptic strength by regulating KCC2 activity. J. Physiol. 586, 4925-4934. doi: 10.1113/jphysiol.2008.157024
6. Bayer, S.A., and Altman, J. (1995). ‘‘Neurogenesis and neuronal migration,’’ in The Rat Nervous System. (Second Edition), ed. G. Paxinos (SanDiego, CA: Academic Press), 1041-1078
7. Bazhenov, M., Timofeev, I., Steriade, M., and Sejnowski, T. J. (1999). Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAa receptor potentials. Nat. Neurosci. 2, 168-174. doi: 10.1038/5729
8. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J. L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303-325. doi: 10.1113/jphysiol.1989.sp017762
9. 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
10. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284. doi: 10.1152/physrev.00017.2006
11. Besser, L., Chorin, E., Sekler, I., Silverman, W. F., Atkin, S., Russell, J. T., et al. (2009). Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J. Neurosci. 29, 2890-2901. doi: 10.1523/jneurosci.5093-08.2009
12. Binder, D. K., and Scharfman, H. E. (2004). Brain-derived neurotrophic factor. Growth Factors 22, 123-131. doi: 10.1080/08977190410001723308
13. Blaesse, P., Airaksinen, M. S., Rivera, C., and Kaila, K. (2009). Cation-Chloride cotransporters and neuronal function. Neuron 61, 820-830. doi: 10.1016/j.neuron.2009.03.003
14. Blaesse, P., Guillemin, I., Schindler, J., Schweizer, M., Delpire, E., Khiroug, L., et al. (2006). Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J. Neurosci. 26, 10407-10419. doi: 10.1523/jneurosci.3257-06.2006
15. Blum, H., Balschi, J. A., and Johnson, R. G. (1991). Coupled in vivo activity of creatine phosphokinase and the membrane-bound (Na+, K+)-ATPase in the resting and stimulated electric organ of the electric fish Narcine brasiliensis. J. Biol. Chem. 266, 10254-10259
16. Bondy, C. A. (1991). Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J. Neurosci. 11, 3442-3455
17. Bos, R., Sadlaoud, K., Boulenguez, P., Buttigieg, D., Liabeuf, S., Brocard, C., et al. (2013). Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc. Natl. Acad. Sci. USA 110, 348-353. doi: 10.1073/pnas.1213680110
18. Branchereau, P., Chapron, J., and Meyrand, P. (2002). Descending 5-hydroxytryptamine raphe inputs repress the expression of serotonergic neurons and slow the maturation of inhibitory systems in mouse embryonic spinal cord. J. Neurosci. 22, 2598-2606
19. Burazin, T. C. D., and Gundlach, A. L. (1999). Localization of GDNF/neurturin receptor (c-ret, GFRa-1 and a-2) mRNAs in postnatal rat brain: Differential regional and temporal expression in hippocampus, cortex and cerebellum. Mol Brain Res. 73, 151-171. doi: 10.1016/S0169-328X(99)00217-X
20. Carmona, M. A., Pozas, E., Martinez, A., Espinosa-Parrilla, J. F., Soriano, E., and Aguado, F. (2006). Age-dependent spontaneous hyperexcitability and impairment of GABAergic function in the hippocampus of mice lacking trkB. Cereb. Cortex 16, 47-63. doi: 10.1093/cercor/bhi083
21. Caviness, V. S., Takahashi, T., and Nowakowski, R. S. (1995). Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18, 379-383. doi: 10.1016/0166-2236(95)93933-o
22. Ceanga, M., Spataru, A., and Zagrean, A. M. (2010). Oxytocin is neuroprotective against oxygen-glucose deprivation and reoxygenation in immature hippocampal cultures. Neurosci.Lett. 477, 15-18. doi: 10.1016/j.neulet.2010.04.024
23. Chen, W. G., West, A. E., Tao, X., Corfas, G., Szentirmay, M. N., Sawadogo, M., et al. (2003). Upstream stimulatory factors are mediators of Ca2+-responsive transcription in neurons. J. Neurosci. 23, 2572-2581
24. Chorin, E., Vinograd, O., Fleidervish, I., Gilad, D., Herrmann, S., Sekler, I., et al. (2011). Upregulation of KCC2 activity by zinc-mediated neurotransmission via the mZnR/GPR39 receptor. J.Neurosci. 31, 12916-12926. doi: 10.1523/jneurosci.2205-11.2011
25. Conner, J. M., Lauterborn, J. C., Yan, Q., Gall, C. M., and Varon, S. (1997). Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17, 2295-2313
26. Dzhala, V. I., Talos, D. M., Sdrulla, D. A., Brumback, A. C., Mathews, G. C., Benke, T. A., et al. (2005). NKCC1 transporter facilitates seizures in the developing brain. Nat Med. 11, 1205-1213. doi: 10.1038/nm1301
27. Delpy, A., Allain, A. E., Meyrand, P., and Branchereau, P. (2008). NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. J. Physiol. 586, 1059-1075. doi: 10.1113/jphysiol.2007.146993
28. Dolapchieva, S. (1996). Developmental changes of K+-dependent paranitrophenylphosphatase (Na+-K+-ATPase) distribution in the synaptic regions in the cerebral cortex of rats. Neurosci.Res. 24, 309-312. doi: 10.1016/0168-0102(95)01004-1
29. Douyard, J., Shen, L., Huganir, R. L., and Rubio, M. E. (2007). Differential neuronal and glial expression of GluR1 AMPA receptor subunit and the scaffolding proteins SAP97 and 4.1N during rat cerebellar development. J.Comp.Neurol. 502, 141-156. doi: 10.1002/cne.21294
30. Eftekhari, S., Mehrabi, S., Soleimani, M., and Hassanzadeh, G. (2014). BDNF modifies hippocampal KCC2 and NKCC1 expression in a temporal lobe epilepsy model. Acta Neurobiol. Exp. (Wars) 74, 276-287
31. Egawa, K., and Fukuda, A. (2013). Pathophysiological power of improper tonic GABAA conductances in mature and immature models. Front. Neural Circuits 7:170. doi: 10.3389/fncir.2013.00170
32. Flint, A. C., Liu, X., and Kriegstein, A. R. (1998). Nonsynaptic glycine receptor activation during early neocortical development. Neuron. 20, 43-53. doi: 10.1016/s0896-6273(00)80433-x
33. Friauf, E., Wenz, M., Oberhofer, M., Nothwang, H. G., Balakrishnan, V., Knipper, M., et al. (2008). Hypothyroidism impairs chloride homeostasis and onset of inhibitory neurotransmission in developing auditory brainstem and hippocampal neurons. Eur. J. Neurosci. 28, 2371-2380. doi: 10.1111/j.1460-9568.2008.06528.x
34. Friedel, P., Kahle, K. T., Zhang, J., Hertz, N., Pisella, L. I., Buhler, E., et al. (2015). WNK1-regulated inhibitory phosphorylation of the KCC2 cotransporter maintains the depolarizing action of GABA in immature neurons. Sci. Signal. 8, 23-26. doi: 10.1126/scisignal.aaa0354
35. Fukuda, A., Mody, I., and Prince, D. A. (1993). Differential ontogenesis of presynaptic and postsynaptic GABAB inhibition in rat somatosensory cortex. J. Neurophysiol. 70, 448-452
36. Fukuda, A., Muramatsu, K., Okabe, A., Shimano, Y., Hida, H., Fujimoto, I., et al. (1998). Changes in intracellular Ca2+ induced by GABAa receptor activation and reduction in Cl-gradient in neonatal rat neocortex. J. Neurophysiol. 79, 439-446
37. Fukuda, A., and Prince, D. A. (1992). Postnatal development of electrogenic sodium pump activity in rat hippocampal pyramidal neurons. Dev. Brain Res. 65, 101-114. doi: 10.1016/0165-3806(92)90013-m
38. Galanopoulou, A. S. (2006). Sex-and cell-type-specific patterns of GABAA receptor and estradiol-mediated signaling in the immature rat substantia nigra. Eur. J. Neurosci. 23, 2423-2430. doi: 10.1111/j.1460-9568.2006.04778.x
39. Galanopoulou, A. S., Kyrozis, A., Claudio, O. I., Stanton, P. K., and Moshé, S. L. (2003). Sex-specific KCC2 expression and GABAA receptor function in rat substantia nigra. Exp. Neurol. 183, 628-637. doi: 10.1016/s0014-4886(03)00213-9
40. Galanopoulou, A. S., and Moshé, S. L. (2003). Role of sex hormones in the sexually dimorphic expression of KCC2 in rat substantia nigra. Exp. Neurol. 184, 1003-1009. doi: 10.1016/s0014-4886(03)00387-x
41. Gamba, G. (2005). WNK lies upstream of kinases involved in regulation of ion transporters. Biochem.J. 391, e1-e3. doi: 10.1042/bj20051345
42. Ganguly, K., Schinder, A. F., Wong, S. T., and Poo, M. M. (2001). GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105, 521-532. doi: 10.1016/s0092-8674(01)00341-5
43. Gao, X. B., and van den Pol, A. N. (2001). GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons. J. Neurophysiol. 85, 425-434
44. Gilad, D., Shorer, S., Ketzef, M., Friedman, A., Sekler, I., Aizenman, E., et al. (2015). Homeostatic regulation of KCC2 activity by the zinc receptor mZnR/GPR39 during seizures. Neurobiol.Dis. doi: 10.1016/j.nbd.2014.12.020 [Epub ahead of print].
45. Gimpl, G., and Fahrenholz, F. (2001). The oxytocin receptor system: structure, function and regulation. Physiol. Rev. 81, 629-683
46. Hatten, M. E., Alder, J., Zimmerman, K., and Heintz, N. (1997). Genes involved in cerebellar cell specification and differentiation. Curr. Opin. Neurobiol. 7,40-47. doi: 10.1016/s0959-4388(97)80118-3
47. Herrera, V. L., Cova, T., Sassoon, D., and Ruiz-Opazo, N. (1994). Developmental cell-specific regulation of Na+-K+-ATPase a1-, a2-and a3-isoform gene expression. Am. J. Physiol. 266, C1301-C1312
48. Hubner, C. A., Lorke, D. E., and Hermans-Borgmeyer, I. (2001). Expression of the Na-K-2Cl-cotransporter NKCC1 during mouse development. Mech. Dev. 102, 267-269. doi: 10.1016/s0925-4773(01)00309-4
49. Ikeda, K., Onimaru, H., Yamada, J., Inoue, K., Ueno, S., Onaka, T., et al. (2004). Malfunction of respiratory related neuronal activity in Na+, K+ -ATPase alpha2 subunit-deficient mice is due to abnormal Cl-homeostasis in brainstem neurons. J.Neurosci. 24, 10693-10701. doi: 10.1523/jneurosci.2909-04.2004
50. Ikeda, M., Toyoda, H., Yamada, J., Okabe, A., Sato, K., Hotta, Y., et al. (2003). Differential development of cation-chloride cotransporters and Cl-homeostasis contributes to differential GABAergic actions between developing rat visual cortex and dorsal lateral geniculate nucleus. Brain Res. 984, 149-159. doi: 10.1016/s0006-8993(03)03126-3
51. Inoue, K., Ueno, S., and Fukuda, A. (2004). Interaction of neuron-specific K+-Cl-cotransporter, KCC2, with brain-type creatine kinase. FEBS Lett. 564, 131-135. doi: 10.1016/s0014-5793(04)00328-x
52. Inoue, K., Yamada, J., Ueno, S., and Fukuda, A. (2006). Brain-type creatine kinase activates neuron-specific K+ -Cl-cotransporter KCC2. J.Neurochem. 96, 598-608. doi: 10.1111/j.1471-4159.2005.03560.x
53. Inoue, K., Furukawa, T., Kumada, T., Yamada, J., Wang, T., Inoue, R., et al. (2012). Taurine inhibits K+-Cl-cotransporter KCC2 to regulate embryonic Cl-homeostasis via with-no-lysine (WNK) protein kinase signaling pathway. J.Biol.Chem. 287, 20839-20850. doi: 10.1074/jbc.m111.319418
54. Ivakine, E. A., Acton, B. A., Mahadevan, V., Ormond, J., Tang, M., Pressey, J. C., et al. (2013). Neto2 is a KCC2 interacting protein required for neuronal Cl-regulation in hippocampal neurons. Proc. Natl. Acad. Sci. USA 110, 3561-3566. doi: 10.1073/pnas.1212907110
55. Kahle, K. T., Deeb, T. Z., Puskarjov, M., Silayeva, L., Liang, B., Kaila, K., et al. (2013). Modulation of neuronal activity by phosphorylation of the K-Cl cotransporter KCC2. Trends Neurosci. 36, 726-737. doi: 10.1016/j.tins.2013.08.006
56. Kahle, K. T., Rinehart, J., de Los Heros, P., Louvi, A., Meade, P., Vazquez, N., et al. (2005). WNK3 modulates transport of Cl-in and out of cells: implications for control of cell volume and neuronal excitability. Proc. Natl. Acad. Sci. USA 102, 16783-16788. doi: 10.1073/pnas.0508307102
57. Kaila, K., Price, T. J., Payne, J. A., Puskarjov, M., and Voipio, J. (2014). Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat. Rev. Neurosci. 15, 637-654. doi: 10.1038/nrn3819
58. Kar, S., Chabot, J. G., and Quirion, R. (1993). Quantitative autoradiographic localization of [125I]insulin-like growth factor I, [125I]insulin-like growth factor II and [125I]insulin receptor binding sites in developing and adult rat brain. J. Comp. Neurol. 333, 375-397. doi: 10.1002/cne.903330306
59. Kelsch, W., Hormuzdi, S., Straube, E., Lewen, A., Monyer, H., and Misgeld, U. (2001). Insulin-like growth factor 1 and a cytosolic tyrosine kinase activate chloride outward transport during maturation of hippocampal neurons. J. Neurosci. 21, 8339-8347
60. Khirug, S., Ahmad, F., Puskarjov, M., Afzalov, R., Kaila, K., and Blaesse, P. (2010). A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J. Neurosci. 30, 12028-12035. doi: 10.1523/jneurosci.3154-10.2010
61. Khirug, S., Huttu, K., Ludwig, A., Smirnov, S., Voipio, J., Rivera, C., et al. (2005). Distinct properties of functional KCC2 expression in immature mouse hippocampal neurons in culture and in acute slices. Eur. J. Neurosci. 21, 899-904. doi: 10.1111/j.1460-9568.2005.03886.x
62. Kim, J. S., Kim, W. B., Kim, Y. B., Lee, Y., Kim, Y. S., Shen, F. Y., et al. (2011). Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat. J. Neurosci. 31, 13312-13322. doi: 10.3410/f.13371991.14742102
63. Lee, H. H. C., Jurd, R., and Moss, S. J. (2010). Tyrosine phosphorylation regulates the membrane trafficking of the potassium chloride co-transporter KCC2. Mol Cell. Neurosci. 45, 173-179. doi: 10.1016/j.mcn.2010.06.008
64. Lee, H. H. C., Walker, J. A., Williams, J. R., Goodier, R. J., Payne, J. A., and Moss, S. J. (2007). Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J. Biol. Chem. 282,29777-29784. doi: 10.1074/jbc.m705053200
65. Lenhard, T., and Suter-Crazzolara, C. (1998). Developmental expression ofGDNF, neurturin and their receptors in rat hippocampus. Neuroreport 9, 2927-2931. doi: 10.1097/00001756-199809140-00002
66. Li, H., Khirug, S., Cai, C., Ludwig, A., Blaesse, P., Kolikova, J., et al. (2007). KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56, 1019-1033. doi: 10.1016/j.neuron.2007.10.039
67. Li, H., Tornberg, J., Kaila, K., Airaksinen, M. S., and Rivera, C. (2002). Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur. J. Neurosci. 16, 2358-2370. doi: 10.1046/j.1460-9568.2002.02419.x
68. Liu, J., Spéder, P., and Brand, A. H. (2014). Control of brain development and homeostasis by local and systemic insulin signalling. Diabetes, Obes. Metab. 16, 16-20. doi: 10.1111/dom.12337
69. Ludwig, A., Li, H., Saarma, M., Kaila, K., and Rivera, C. (2003). Developmental up-regulation of KCC2 in the absence of GABAergic and glutamatergic transmission. Eur. J. Neurosci. 18, 3199-3206. doi: 10.1111/j.1460-9568.2003.03069.x
70. Ludwig, A., Uvarov, P., Soni, S., Thomas-Crusells, J., Airaksinen, M. S., and Rivera, C. (2011). Early growth response 4 mediates BDNF induction of potassium chloride cotransporter 2 transcription. J. Neurosci. 31, 644-649. doi: 10.1523/jneurosci.2006-10.2011
71. Luhmann, H. J., Fukuda, A., and Kilb, W. (2015). Control of cortical neuronal migration by glutamate and GABA. Front. Cell. Neurosci. 9:4. doi: 10.3389/fncel.2015.00004
72. Luhmann, H. J., and Prince, D. A. (1991). Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65, 247-263
73. Manos, P., Bryan, G. K., and Edmond, J. (1991). Creatine kinase activity in postnatal rat brain development and in cultured neurons, astrocytes and oligodendrocytes. J. Neurochem. 56, 2101-2107. doi: 10.1111/j.1471-4159.1991.tb03472.x
74. Maisonpierre, P. C., Belluscio, L., Friedman, B., Alderson, R. F., Wiegand, S. J., Furth, M. E., et al. (1990). NT-3, BDNF and NGF in the developing rat nervous system: parallel as well as reciprocal patterns ofexpression. Neuron 5, 501-509. doi: 10.1016/0896-6273(90)90089-x
75. Markkanen, M., Uvarov, P., and Airaksinen, M. S. (2008). Role of upstream stimulating factors in the transcriptional regulation of the neuron-specific K-Cl cotransporter KCC2. Brain Res. 1236, 8-15. doi: 10.1016/j.brainres.2008.08.007
76. Marty, S., Wehrlé, R., Alvarez-Leefmans, F. J., Gasnier, B., and Sotelo, C. (2002). Postnatal maturation of Na+, K+, 2Cl-cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: An immunocytochemical analysis. Eur. J. Neurosci. 15, 233-245. doi: 10.1046/j.0953-816x.2001.01854.x
77. Medina, I., Friedel, P., Rivera, C., Kahle, K. T., Kourdougli, N., Uvarov, P., et al. (2014). Current view on the functional regulation of the neuronal K+-Cl-cotransporter KCC2. Front. Cell. Neurosci. 8:27. doi: 10.3389/fncel.2014.00027
78. Michishita, M., Ikeda, T., Nakashiba, T., Ogawa, M., Tashiro, K., Honjo, T., et al. (2004). Expression of Btcl2, a novel member of Btcl gene family, during development of the central nervous system. Dev. Brain Res. 153, 135-142. doi: 10.1016/j.devbrainres.2004.06.012
79. Mikawa, S., Wang, C., Shu, F., Wang, T., Fukuda, A., and Sato, K. (2002). Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Dev. Brain Res. 136, 93-100. doi: 10.1016/s0165-3806(02)00345-0
80. Minami, H., Owada, Y., Suzuki, R., Handa, Y., and Kondo, H. (2000). Localization of mRNAs for novel, atypical as well as conventional protein kinase C (PKC) isoforms in the brain of developing and mature rats. J. Mol. Neurosci. 15, 121-135. doi: 10.1385/jmn:15:2:121
81. Moseley, A. E., Lieske, S. P., Wetzel, R. K., James, P. F., He, S., Shelly, D. A., et al. (2003). The Na, K-ATPase a2 isoform is expressed in neurons and its absence disrupts neuronal activity in newborn mice. J. Biol. Chem. 278, 5317-5324. doi: 10.1074/jbc.M211315200
82. Niimi, K., Harada, I., Kusaka, Y., and Kishi, S. (1961). The ontogenetic development of the diencephalon of the mouse. Tokushima. J. Exp. Med. 8, 203-238
83. Nitzan, Y. B., Sekler, I., Hershfinkel, M., Moran, A., and Silverman, W. F. (2002). Postnatal regulation of ZnT-1 expression in the mouse brain. Dev. Brain Res. 137, 149-157. doi: 10.1016/s0165-3806(02)00437-6
84. Nugent, B. M., Valenzuela, C. V., Simons, T. J., and McCarthy, M. M. (2012). Kinases SPAK and OSR1 are upregulated by estradiol and activate NKCC1 in the developing hypothalamus. J.Neurosci. 32, 593-598. doi: 10.1523/jneurosci.5415-11.2012
85. Ostroumov, A., Simonetti, M., and Nistri, A. (2011). Cystic fibrosis transmembrane conductance regulator modulates synaptic chloride homeostasis in motoneurons of the rat spinal cord during neonatal development. Dev. Neurobiol. 71, 253-268. doi: 10.1002/dneu.20855
86. Owens, D. F., and Kriegstein, A. R. (2002). Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3, 715-727. doi: 10.1038/nrn919
87. Pangratz-Fuehrer, S., Rudolph, U., and Huguenard, J. R. (2007). Giant spontaneous depolarizing potentials in the developing thalamic reticular nucleus. J. Neurophysiol. 97, 2364-2372. doi: 10.1152/jn.00646.2006
88. Payne, J. A., Rivera, C., Voipio, J., and Kaila, K. (2003). Cation-chloride co¬transporters in neuronal communication, development and trauma. Trends Neurosci. 26, 199-206. doi: 10.1016/s0166-2236(03)00068-7
89. Paxinos, G. (1995). The Rat Nervous System 2nd Edn. NewYork: Academic Press, Sydney.
90. Perez-Castillo, A., Bernal, J., Ferreiro, B., and Pans, T. (1985). The early ontogenesis of thyroid hormone receptor in the rat fetus. Endocrinology 117, 2457-2461. doi: 10.1210/endo-117-6-2457
91. Perrot-Sinal, T. S., Davis, A. M., Gregerson, K. A., Kao, J. P. Y., and McCarthy, M. M. (2001). Estradiol enhances excitatory gamma-aminobutyric acid mediated calcium signaling in neonatal hypothalamic neurons. Endocrinology 142,2238-2243. doi: 10.1210/endo.142.6.8180
92. Perrot-Sinal, T. S., Sinal, C. J., Reader, J. C., Speert, D. B., and McCarthy, M. M. (2007). Sex differences in the chloride cotransporters, NKCC1 and KCC2, in the developing hypothalamus. J.Neuroendocrinol. 19, 302-308. doi: 10.1111/j.1365-2826.2007.01530.x
93. Popken, G. J., Dechert-Zeger, M., Ye, P., and D’Ercole, A. J. (2005). ‘‘Brain development,” in The Growth Hormone/Insulin-Like Growth FactorAxis during Development, eds I. Varela-Nieto and J. A. Chowen (Springer US press), 187-220
94. Puskarjov, M., Ahmad, F., Khirug, S., Sivakumaran, S., Kaila, K., and Blaesse, P. (2015). BDNF is required for seizure-induced but not developmental up-regulation of KCC2 in the neonatal hippocampus. Neuropharmacology 88, 103-109. doi: 10.1016/j.neuropharm.2014.09.005
95. Qian, T., Chen, R., Nakamura, M., Furukawa, T., Kumada, T., Akita, T., et al. (2014). Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats. Front.Cell.Neurosci. 8:33. doi: 10.3389/fncel.2014.00033
96. Ravizza, T., Galanopoulou, A. S., Velísková, J., and Moshé, S. L. (2002). Sex differences in androgen and estrogen receptor expression in rat substantia nigra during development: an immunohistochemical study. Neuroscience 115, 685-696. doi: 10.1016/s0306-4522(02)00491-8
97. Rinehart, J., Maksimova, Y. D., Tanis, J. E., Stone, K. L., Hodson, C. A., Zhang, J., et al. (2009). Sites of regulated phosphorylation that control K-Cl cotransporter activity. Cell 138, 525-536. doi: 10.1016/j.cell.2009.05.031
98. Rinehart, J., Vázquez, N., Kahle, K. T., Hodson, C. A., Ring, A. M., Gulcicek, E. E., et al. (2011). WNK2 kinase is a novel regulator of essential neuronal cation-chloride cotransporters. J.Biol.Chem. 286, 30171-30180. doi: 10.1074/jbc.m111.222893
99. Ritter, B., and Zhang, W. (2000). Early postnatal maturation of GABAA-mediated inhibition in the brainstem respiratory rhythm-generating network of the mouse. Eur. J. Neurosci. 12, 2975-2984. doi: 10.1046/j.1460-9568.2000.00152.x
100. Rivera, C., Li, H., Thomas-Crusells, J., Lahtinen, H., Viitanen, T., Nanobashvili, A., et al. (2002). BDNF-induced TrkB activation down-regulates the K+-Cl-cotransporter KCC2 and impairs neuronal Cl-extrusion. J. Cell Biol. 159, 747-752. doi: 10.1083/jcb.200209011
101. Rivera, C., Ludwig, A., Uvarov, P., Pellegrino, C., Thomas-Crusells, J., Schuchmann, S., et al. (2011). Neurturin evokes MAPK-dependent upregulation of Egr4 and KCC2 in developing neurons. Neural Plast. 2011, 1-8. doi: 10.1155/2011/641248
102. Rivera, C., Voipio, J., Thomas-Crusells, J., Li, H., Emri, Z., Sipila, S., et al. (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl cotransporter KCC2. J. Neurosci. 24, 4683-4691. doi: 10.1523/jneurosci.5265-03.2004
103. Rotwein, P., Burgess, S. K., Milbrandt, J. D., and Krause, J. E. (1988). Differential expression of insulin-like growth factor genes in rat central nervous system. Proc. Natl. Acad. Sci. U S A 85, 265-269. doi: 10.1073/pnas.85.1.265
104. Russo, V. C., Gluckman, P. D., Feldman, E. L., and Werther, G. A. (2005). The insulin-like growth factor system and its pleiotropic functions in brain. Endocr. Rev. 26, 916-943. doi: 10.1210/er.2004-0024
105. Saadi, R. A., He, K., Hartnett, K. A., Kandler, K., Hershfinkel, M., and Aizenman, E. (2012). SNARE-dependent upregulation of potassium chloride co-transporter 2 activity after metabotropic zinc receptor activation in rat cortical neurons in vitro. Neuroscience 210, 38-46. doi: 10.1016/j.neuroscience.2012.03.001
106. Sawano, E., Takahashi, M., Negishi, T., and Tashiro, T. (2013). Thyroid hormone-dependent development of the GABAergic pre-and post-synaptic components in the rat hippocampus. Int. J. Dev. Neurosci. 31, 751-761. doi: 10.1016/j.ijdevneu.2013.09.007
107. Shimada, M., Shimono, R., Watanabe, M., Imahayashi, T., Ozaki, H. S., Kihara, T., et al. (1984). Distribution of 35S-taurine in rat neonates and adults. A whole-body autoradiographic study. Histochemistry 80, 225-230. doi: 10.1007/bf00495770
108. Shimizu-Okabe, C., Yokokura, M., Okabe, A., Ikeda, M., Sato, K., Kilb, W., et al. (2002). Layer-specific expression of Cl-transporters and differential [Cl-]i in newborn rat cortex. Neuroreport 13, 2433-2437. doi: 10.1097/01.wnr.0000048007.96487.82
109. Sibilla, S., and Ballerini, L. (2009). GABAergic and glycinergic interneuron expression during spinal cord development: Dynamic interplay between inhibition and excitation in the control of ventral network outputs. Prog. Neurobiol. 89, 46-60. doi: 10.1016/j.pneurobio.2009.06.001
110. Sirito, M., Lin, Q., Deng, J. M., Behringer, R. R., and Sawadogo, M. (1998). Overlapping roles and asymmetrical cross-regulation of the USF proteins in mice. Proc. Natl. Acad. Sci. U S A 95, 3758-3763. doi: 10.1073/pnas.95.7.3758
111. Slomianka, L., and Geneser, F. A. (1997). Postnatal development of zinc-containing cells and neuropil in the hippocampal region of the mouse. Hippocampus 7, 321-340. doi: 10.1002/(sici)1098-1063(1997)7:3<321::aid-hipo7>3.0.co;2-n
112. Steiger, J. L., Bandyopadhyay, S., Farb, D. H., and Russek, S. J. (2004). cAMP response element-binding protein, activating transcription factor-4 and upstream stimulatory factor differentially control hippocampal GABAeR1a and GABABR1b subunit gene expression through alternative promoters. J.Neurosci. 24, 6115-6126. doi: 10.1523/jneurosci.1200-04.2004
113. Stein, V., Hermans-Borgmeyer, I., Jentsch, T. J., and Hubner, 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
114. Stil, A., Liabeuf, S., Jean-Xavier, C., Brocard, C., Viemari, J. C., and Vinay, L. (2009). Developmental up-regulation of the potassium-chloride cotransporter type 2 in the rat lumbar spinal cord. Neuroscience 164, 809-821. doi: 10.1016/j.neuroscience.2009.08.035
115. Sturman, J. A. (1988). Taurine in development. J. Nutr. 118, 1169-1176
116. Sun, Y. G., Wu, C. S., Renger, J. J., Uebele, V. N., Lu, H. C., and Beierlein, M. (2012). GABAergic synaptic transmission triggers action potentials in thalamic reticular nucleus neurons. J.Neurosci. 32, 7782-7790. doi: 10.1523/jneurosci.0839-12.2012
117. Swann, J. W., Brady, R. J., and Martin, D. L. (1989). Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus. Neuroscience 28, 551-561. doi: 10.1016/0306-4522(89)90004-3
118. Tabuchi, A., Sakaya, H., Kisukeda, T., Fushiki, H., and Tsuda, M. (2002). Involvement of an upstream stimulatory factor as well as cAMP-responsive element-binding protein in the activation of brain-derived neurotrophic factor gene promoter I. J.Biol.Chem. 277, 35920-35931. doi: 10.1074/jbc.m204784200
119. Takayama, C., and Inoue, Y. (2010). Developmental localization of potassium chloride co-transporter 2 (KCC2), GABA and vesicular GABA transporter (VGAT) in the postnatal mouse somatosensory cortex. Neurosci. Res. 67, 137-148. doi: 10.1016/j.neures.2010.02.010
120. Trask, R. V., and Billadello, J. J. (1990). Tissue-specific distribution and developmental regulation of M and B creatine kinase mRNAs. Biochim. Biophys. Acta 1049, 182-188. doi: 10.1016/0167-4781(90)90039-5
121. Tyzio, R., Cossart, R., Khalilov, I., Minlebaev, M., Hubner, C. A., Represa, A., et al. (2006). Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science. 314, 1788-1792. doi: 10.1126/science.1133212
122. Walensky, L. D., Blackshaw, S., Liao, D., Watkins, C. C., Weier, H. U., Parra, M., et al. (1999). A novel neuron-enriched homolog of the erythrocyte membrane cytoskeletal protein 4.1. J. Neurosci. 19, 6457-6467
123. Wang, C., Ohno, K., Furukawa, T., Ueki, T., Ikeda, M., Fukuda, A., et al. (2005). Differential expression of KCC2 accounts for the differential GABA responses between relay and intrinsic neurons in the early postnatal rat olfactory bulb. Eur. J. Neurosci. 21, 1449-1455. doi: 10.1111/j.1460-9568.2005.03975.x
124. Wang, C., Shimizu-Okabe, C., Watanabe, K., Okabe, A., Matsuzaki, H., Ogawa, T., et al. (2002). Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat brain. Dev. Brain Res. 139, 59-66. doi: 10.1016/s0165-3806(02)00536-9
125. Watanabe, M., Fukuda, A., and Nabekura, J. (2014). The role of GABA in the regulation of GnRH neurons. Front.Neurosci. 28:e387. doi: 10.3389/fnins.2014.00387
126. Westerholz, S., de Lima, A. D., and Voigt, T. (2013). Thyroid hormone-dependent development of early cortical networks: temporal specificity and the contribution of trkB and mTOR pathways. Front.Cell.Neurosci. 7:121. doi: 10.3389/fncel.2013.00121
127. Wu, W. L., Ziskind-Conhaim, L., and Sweet, M. A. (1992). Early development of glycine-and GABA-mediated synapses in rat spinal cord. J. Neurosci. 12, 3935-3945
128. Wyss, M., and Kaddurah-Daouk, R. (2000). Creatine and creatinine metabolism. Physiol. Rev. 80, 1107-1213
129. Yamada, J., Okabe, A., Toyoda, H., Kilb, W., Luhmann, H. J., and Fukuda, A. (2004). Cl-uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 557, 829-841. doi: 10.1113/jphysiol.2004.062471
130. Yan, Q., Radeke, M. J., Matheson, C. R., Talvenheimo, J., Welcher, A. A., and Feinstein, S. C. (1997a). Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J. Comp. Neurol. 378, 135-157. doi: 10.1002/(SICI)1096-9861(19970203)378:1<135::AID-CNE8>3.0.CO;2-5
131. Yan, Q., Rosenfeld, R., Matheson, C. R., Hawkins, N., Lopez, O. T., Bennett, L., et al. (1997b). Expression of brain-derived neurotrophic factor protein in the adult rat central nervous system. Neuroscience 78, 431-448. doi: 10.1016/s0306-4522(96)00613-6