Both NKCC1 and anion exchangers contribute to Cl - accumulation in postnatal forebrain neuronal progenitors

European Journal of Neuroscience

Volumn 35, Issue 5, 2012, Pages 661-672

  Sun, Lin ^a,b   Yu, Zhiyuan ^c   Wang, Wei ^c   Liu, Xiuxin ^a,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHANDONG UNIVERSITY   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d UNIVERSITY OF ROCHESTER   (United States)

Author keywords

GABA A receptor; Na + K + 2Cl transporter; Neuronal progenitor

Indexed keywords

4 (2 HYDROXYETHYL) 1 PIPERAZINEETHANESULFONIC ACID; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; ACETAZOLAMIDE; BICARBONATE; BROXURIDINE; BUMETANIDE; CALCIUM ION; CARBON DIOXIDE; CHLORIDE; GRAMICIDIN; LITHIUM; SODIUM; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ANION EXCHANGE; ARTICLE; BIOACCUMULATION; BRAIN DEVELOPMENT; CALCIUM SIGNALING; CHLORIDE TRANSPORT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; GABAERGIC TRANSMISSION; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PHARMACOLOGICAL BLOCKING; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; ANTIPORTERS; CHLORIDES; HOMEOSTASIS; MICE; NEURAL STEM CELLS; NEURONS; PROSENCEPHALON; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS;

EID: 84863257419     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08007.x     Document Type: Article

References (70)

1. +-2Cl cotransport in immature rat neocortical neurons. J. Neurosci., 27, 8616-8827.
2. Alvarez, B.V., Kieller, D.M., Quon, A.L., Markovich, D. & Casey, J.R. (2004) Slc26a6: a cardiac chloride-hydroxyl exchanger and predominant chloride-bicarbonate exchanger of the mouse heart. J. Physiol. (Lond), 561, 721-734.
3. Becker, M., Nothwang, H.G. & Friauf, E. (2003) Differential expression pattern of chloride transporters NCC, NKCC2, KCC1, KCC3, KCC4, and AE3/ in the developing rat auditory brainstem. Cell Tissue Res., 312, 155-165.
4. Behar, T.N., Li, Y.X., Tran, H.T., Ma, W., Dunlap, V., Scott, C. & Barker, J.L. (1996) GABA stimulates chemotaxis and chemokinesis of embryonic cortical neurons via calcium-dependent mechanisms. J. Neurosci., 16, 1808-1818.
5. Ben Ari, Y. (2002) Excitatory actions of GABA during development: the nature of the Nurture. Nat. Rev. Neurosci., 3, 728-739.
6. Bernstein, M., Lyons, S.A., Moller, T. & Kettenmann, H. (1996) Receptor-mediated calcium signalling in glial cells from mouse corpus callosum slices. J. Neurosci. Res., 46, 152-163.
7. Bolteus, A.J. & Bordey, A. (2004) GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J. Neurosci., 24, 7623-7631.
8. Bordey, A. & Sontheimer, H. (1997) Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J. Neurophysiol., 78, 461-477.
9. Bouzinova, E.V., Praetorius, J., Virkki, L.V., Nielsen, S., Boron, W.F. & Aalkjaer, C. (2005) Na+-dependent HCO3- uptake into the rat choroid plexus epithelium is partially DIDS sensitive. Am. J. Physiol. Cell Physiol., 289, C1448-C1456.
10. varez-Buylla, A. & Lim, D.A. (2004) For the long run: maintaining germinal niches in the adult brain. Neuron, 41, 683-686.
11. varez-Buylla, A. & Temple, S. (1998) Stem cells in the developing and adult nervous system. J. Neurobiol., 36, 105-110.
12. Casey, J.R., Morgan, P.E., Vullo, D., Scozzafava, A., Mastrolorenzo, A. & Supuran, C.T. (2004) Carbonic anhydrase inhibitors. Design of selective, membrane-impermeant inhibitors targeting the human tumor-associated isozyme IX. J. Med. Chem., 47, 2337-2347.
13. Chub, N., Mentis, G.Z. & O'donovan, M.J. (2006) Chloride-sensitive MEQ fluorescence in chick embryo motoneurons following manipulations of chloride and during spontaneous network activity. J. Neurophysiol., 95, 323-330.
14. Delpy, A., Allain, A.E., Meyrand, P. & Branchereau, P. (2008) NKCC1 cotransporter inactivation underlies embryonic development of chloride-mediated inhibition in mouse spinal motoneuron. J. Physiol., 586, 1059-1075.
15. Doetsch, F., Garcia- Verdugo, J.M. & Alvarez-Buylla, A. (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci., 17, 5046-5061.
16. Durand, S.H., Flacher, V., Romeas, A., Carrouel, F., Colomb, E., Vincent, C., Magloire, H., Couble, M.L., Bleicher, F., Staquet, M.J., Lebecque, S. & Farges, J.C. (2006) Lipoteichoic acid increases TLR and functional chemokine expression while reducing dentin formation in in vitro differentiated human odontoblasts. J. Immunol., 176, 2880-2887.
17. Everett, L.A. & Green, E. (1999) A family of mammalian anion transportersand their involvement in human genetic diseases. Hum. Mol. Genet., 8, 1883-1891.
18. Gamba, G. (2005) Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol. Rev., 85, 423-493.
19. Ge, S., Goh, E.L., Sailor, K.A., Kitabatake, Y., Ming, G.L. & Song, H. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature, 439, 589-593.
20. Gerencser, G.A., Purushotham, K.R. & Meng, H.B. (1996) An electrogenic chloride pump in a zoological membrane. J. Exp. Zool., 275, 256-261.
21. Gijon, E., Valencia, A., Contreras- Barrios, M.A., Verdugo, L. & Garcia, X. (1998) Homologous transplant in vivo of uterine smooth muscle cells in cardiac muscle of guinea pig. Proc. West. Pharmacol. Soc., 41, 159-160.
22. Gomez, T.M. & Spitzer, N.C. (1999) In vivo regulation of axon extension and pathfinding by growth-cone calcium transients. Nature, 397, 350-355.
23. Gonzalez-Islas, C.E., Chub, N.L. & Wenner, P. (2009) NKCC1 and AE3 appear to accumulate chloride in embryonic motoneurons. J. Neurophysiol., 101, 507-518.
24. 2+ transients. Nature, 375, 784-787.
25. Havenga, M.J.E., Bosman, G.J.C.G., Appelhans, H. & De Grip, W.J. (1994) Expression of the anion exchanger (AE) gene family in human brain. Identification of a new AE protein: AE0. Brain Res. Mol. Brain Res., 25, 97-104.
26. Haydar, T.F., Wang, F., Schwartz, M.L. & Rakic, P. (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci., 20, 5764-5774.
27. Heck, N., Kilb, W., Reiprich, P., Kubota, H., Furukawa, T., Fukuda, A. & Luhmann, H.J. (2006) GABA-A receptors regulate neocortical neuronal migration in vitro and in vivo. Cereb. Cortex, 17, 138-148.
28. Hentschke, M., Wiemann, M., Hentschke, S., Kurth, I., Hermans-Borgmeyer, I., Seidenbecher, T., Jentsch, T.J., Gal, A. & Hubner, C.A. (2006) Mice with a targeted disruption of the Cl-/HCO3- exchanger AE3 display a reduced seizure threshold. Mol. Cell. Biol., 26, 182-191.
29. Ihrie, R.A. & varez-Buylla, A. (2008) Cells in the astroglial lineage are neural stem cells. Cell Tissue Res., 331, 179-191.
30. Ko, S.B.H., Luo, X., Hager, H., Rojek, A., Young Choi, J., Licht, C., Suzuki, M., Muallem, S., Nielsen, S. & Ishibashi, K. (2002) AE4 is a DIDS-sensitive Cl-/HCO3- exchanger in the basolateral membrane of the renal CCD and the SMG duct. Am. J. Physiol. Cell Physiol., 283, C1206-C1218.
31. Komuro, H. & Rakic, P. (1993) Modulation of neuronal migration by Nmda receptors. Science, 260, 95-97.
32. Komuro, H. & Rakic, P. (1996) Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron, 17, 275-285.
33. Levison, S.W. & Goldman, J.E. (1997) Multipotential and lineage restricted precursors coexist in the mammalian perinatal subventricular zone. J. Neurosci. Res., 48, 83-94.
34. Li, H., Tornberg, J., Kaila, K., Airaksinen, M.S. & Rivera, C. (2002) Patterns of cation-chloride cotransporter expression during embryonic rodent CNS development. Eur. J. Neurosci., 16, 2358-2370.
35. Liu, X., Wang, Q., Haydar, T.F. & Bordey, A. (2005) Nonsynaptic GABA signaling in postnatal subventricular zone controls proliferation of GFAP-expressing progenitors. Nat. Neurosci., 8, 1179-1187.
36. Liu, X., Bolteus, A.J., Balkin, D.M., Henschel, O. & Bordey, A. (2006) GFAP-expressing cells in the postnatal subventricular zone display a unique glial phenotype intermediate between radial glia and astrocytes. Glia, 54, 394-410.
37. Lledo, P.M. & Gheusi, G. (2006) Adult neurogenesis: from basic research to clinical applications. Bull. Acad. Natl Med., 190, 385-400.
38. LoTurco, J.J., Owens, D.F., Heath, M.J.S., Davis, M.B.E. & Kriegstein, A.R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron, 15, 1287-1298.
39. Luhmann, H.J. & Prince, D.A. (1991) Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol., 65, 247-263.
40. - cotransporter expression and inhibitory synaptogenesis in the rat hippocampus: an immunocytochemical analysis. Eur. J. Neurosci., 15, 233-245.
41. Mejia-Gervacio, S., Murray, K. & Lledo, P.M. (2011) NKCC1 controls GABAergic signaling and neuroblast migration in the postnatal forebrain. Neural Dev., 6, 4.
42. Mikawa, S., Wang, C., Shu, F., Wang, T., Fukuda, A. & Sato, K. (2002) Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res. Dev. Brain Res., 136, 93-100.
43. Munsch, T. & Pape, H.C. (1999) Upregulation of the hyperpolarization-activated cation current in rat thalamic relay neurones by acetazolamide. J. Physiol. (Lond), 519, 505-514.
44. Nguyen, L., Malgrange, B., Breuskin, I., Bettendorff, L., Moonen, G., Belachew, S. & Rigo, J.M. (2003) Autocrine/Paracrine activation of the GABAA receptor inhibits the proliferation of Neurogenic Polysialylated Neural Cell Adhesion Molecule-Positive (PSA-NCAM+) precursor cells from postnatal striatum. J. Neurosci., 23, 3278-3294.
45. 2+]i increase in salivary acinar cells. Am. J. Physiol. Gastrointest. Liver Physiol., 286, G312-G320.
46. Owens, D.F. & Kriegstein, A.R. (2002) Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci., 3, 715-727.
47. Owens, D.F., Boyce, L.H., Davis, M.B. & Kriegstein, A.R. (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci., 16, 6414-6423.
48. - cotransport by different mitogens in synchronized human skin fibroblasts is essential for cell proliferation. J. Cell Biol., 114, 337-342.
49. Panet, R., Markus, M. & Atlan, H. (1994) Bumetanide and furosemide inhibited vascular endothelial cell proliferation. J. Cell. Physiol., 158, 121-127.
50. Panet, R., Marcus, M. & Atlan, H. (2000) Overexpression of the Na(+)/K(+)/Cl(-) cotransporter gene induces cell proliferation and phenotypic transformation in mouse fibroblasts. J. Cell. Physiol., 182, 109-118.
51. Panet, R., Eliash, M., Pick, M. & Atlan, H. (2002) Na(+)/K(+)/Cl(-) cotransporter activates mitogen-activated protein kinase in fibroblasts and lymphocytes. J. Cell. Physiol., 190, 227-237.
52. - cotransporter activates MAP-kinase cascade downstream to protein kinase C, and upstream to MEK. J. Cell. Physiol., 206, 578-585.
53. Payne, J.A., Rivera, C., Voipio, J. & Kaila, K. (2003) Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci., 26, 199-206.
54. Pearson, R.A., Dale, N., Llaudet, E. & Mobbs, P. (2005) ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron, 46, 731-744.
55. Romero, M.F., Fulton, C.M. & Boron, W.F. (2004) The SLC4 family of HCO 3 - transporters. Pflugers Arch., 447, 495-509.
56. Russell, J.M. (2000) Sodium-Potassium-Chloride cotransport. Physiol. Rev., 80, 211-276.
57. Shimizu-Okabe, C., Yokokura, M., Okabe, A., Ikeda, M., Sato, K., Kilb, W., Luhmann, H.J. & Fukuda, A. (2002) Layer-specific expression of Cl- transporters and differential [Cl-]i in newborn rat cortex. Neuroreport, 13, 2433-2437.
58. Singer, W. (1995) Development and plasticity of cortical processing architectures. Science, 270, 758-764.
59. Sipila, S.T., 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.
60. Spoerri, P.E. (1988) Neurotrophic effects of GABA in cultures of embryonic chick brain and retina. Synapse, 2, 11-22.
61. Sterling, D. & Casey, J.R. (2002) Bicarbonate transport proteins. Biochem. Cell Biol., 80, 483-497.
62. Stewart, R.R., Hoge, G.J., Zigova, T. & Luskin, M.B. (2002) Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J. Neurobiol., 50, 305-322.
63. Tozuka, Y., Fukuda, S., Namba, T., Seki, T. & Hisatsune, T. (2005) GABAergic excitation promotes neuronal differentiation in adult Hippocampal progenitor cells. Neuron, 47, 803-815.
64. Tsuganezawa, H., Kobayashi, K., Iyori, M., Araki, T., Koizumi, A., Watanabe, S.I., Kaneko, A., Fukao, T., Monkawa, T., Yoshida, T., Kim, D.K., Kanai, Y., Endou, H., Hayashi, M. & Saruta, T. (2001) A new member of the HCO3- transporter superfamily is an apical anion exchanger of beta -intercalated cells in the kidney. J. Biol. Chem., 276, 8180-8189.
65. Wang, C., Shimizu-Okabe, C., Watanabe, K., Okabe, A., Matsuzaki, H., Ogawa, T., Mori, N., Fukuda, A. & Sato, K. (2002) Developmental changes in KCC1, KCC2, and NKCC1 mRNA expressions in the rat brain. Brain Res. Dev. Brain Res., 139, 59-66.
66. Wang, D.D., Krueger, D.D. & Bordey, A. (2003) GABA depolarizes neuronal progenitors of the postnatal subventricular zone via GABAA receptor activation. J. Physiol. (Lond), 550, 785-800.
67. Weissman, T.A., Riquelme, P.A., Ivic, L., Flint, A.C. & Kriegstein, A.R. (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron, 43, 647-661.
68. Xu, J., Barone, S., Petrovic, S., Wang, Z., Seidler, U., Riederer, B., Ramaswamy, K., Dudeja, P.K., Shull, G.E. & Soleimani, M. (2003) Identification of an apical Cl-/HCO3- exchanger in gastric surface mucous and duodenal villus cells. Am. J. Physiol. Gastrointest. Liver Physiol., 285, G1225-G1234.
69. Yamada, J., Okabe, A., Toyoda, H., Kilb, W., Luhmann, H.J. & Fukuda, A. (2004) Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. (Lond), 557, 829-841.
70. Zhao, Y. & Baltz, J.M. (1996) Bicarbonate/chloride exchange and intracellular pH throughout preimplantation mouse embryo development. Am. J. Physiol. Cell Physiol., 271, C1512-C1520.