GABA receptors in brain development, function, and injury

Metabolic Brain Disease

Volumn 30, Issue 2, 2015, Pages 367-379

  Wu, Connie ^a   Sun, Dandan ^b,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Anoxic ischemic injury; Chloride transporters; Periventricular leukomalacia; Schizophrenia; Stroke; aminobutyric acid receptors

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL; BRAIN; BRAIN DISEASE; BRAIN INJURY; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; BRAIN; BRAIN DISEASES; BRAIN INJURIES; HUMANS; NEUROGENESIS; RECEPTORS, GABA;

EID: 84939873845     PISSN: 08857490     EISSN: 15737365     Source Type: Journal    
DOI: 10.1007/s11011-014-9560-1     Document Type: Article

References (93)

1. Akbarian S, Huang H-S (2006) Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders. Brain Res Rev 52(2):293–304. doi:10.1016/j.brainresrev.2006.04.001
2. Allain A-E, Baїri A, Meyrand P, Branchereau P (2004) Ontogenic changes of the GABAergic system in the embryonic mouse spinal cord. Brain Res 1000(1–2):134–147. doi:10.1016/j.brainres.2003.11.071
3. Anderson SA (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278(5337):474–476. doi:10.1126/science.278.5337.474
4. Anderson SA, Volk DW, Lewis DA (1996) Increased density of microtubule associated protein 2-immunoreactive neurons in the prefrontal white matter of schizophrenic subjects. Schizophr Res 19(2–3):111–119. doi:10.1016/0920-9964(96)88521-5
5. Anderson SA, Kaznowski CE, Horn C, Rubenstein JLR, McConnell SK (2002) Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb Cortex 12(7):702–709
6. Antonopoulos J, Pappas IS, Parnavelas JG (1997) Activation of the GABAA receptor inhibits the proliferative effects of bFGF in cortical progenitor cells. Eur J Neurosci 9(2):291–298
7. Barnard EA, Skolnick P, Olsen RW, Mohler H, Sieghart W, Biggio G, Braestrup C, Bateson AN, Langer SZ (1998) International Union of Pharmacology. XV. Subtypes of Γ-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol Rev 50(2):291–314
8. Barres BA, Koroshetz WJ, Swartz KJ, Chun LL, Corey DP (1990) Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 4(4):507–524
9. Behar TN, Schaffner AE, Scott CA, O’Connell C, Barker JL (1998) Differential response of cortical plate and ventricular zone cells to GABA as a migration stimulus. J Neurosci 18(16):6378–6387
10. Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R, Gaiarsa JL (1994) Gamma-aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog Brain Res 102:261–273. doi:10.1016/S0079-6123(08)60545-2
11. Ben-Ari Y, Khalilov I, Represa A, Gozlan H (2004) Interneurons set the tune of developing networks. Trends Neurosci 27(7):422–427. doi:10.1016/j.tins.2004.05.002
12. Benes FM, Vincent SL, Marie A, Khan Y (1996) Up-regulation of GABAA receptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience 75(4):1021–1031
13. Billiards SS, Haynes RL, Folkerth RD, Borenstein NS, Trachtenberg FL, Rowitch DH, Ligon KL, Volpe JJ, Kinney HC (2008) Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 18(2):153–163. doi:10.1111/j.1750-3639.2007.00107.x
14. Blednov YA, Benavidez JM, Black M, Leiter CR, Osterndorff-Kahanek E, Johnson D, Borghese CM et al (2014) GABAA receptors containing ρ1 subunits contribute to in vivo effects of ethanol in mice. PLoS ONE 9(1)
15. Boue-Grabot E, Roudbaraki M, Bascles L, Tramu G, Bloch B, Garret M (1998) Expression of GABA receptor rho subunits in rat brain. J Neurochem 70(3):899–907
16. Cancedda L, Fiumelli H, Chen K, Poo M (2007) Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J Neurosci 27(19):5224–5235. doi:10.1523/JNEUROSCI.5169-06.2007
17. Chagnac-Amitai Y, Connors BW (1989) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61(4):747–758
18. Chen G, Trombley PQ, van den Pol AN (1995) GABA receptors precede glutamate receptors in hypothalamic development; differential regulation by astrocytes. J Neurophysiol 74(4):1473–1484
19. Chun JM, Shatz CJ (1989) Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. J Comp Neurol 282(4):555–569
20. Clarkson AN, Huang BS, MacIsaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABAergic tonic inhibition promotes post-stroke functional recovery. Nature 468(7321):305–309
21. Connor CM, Crawford BC, Akbarian S (2011) White matter neuron alterations in schizophrenia and related disorders. Int J Dev Neurosci Off J Int Soc Dev Neurosci 29(3):325–334. doi:10.1016/j.ijdevneu.2010.07.236
22. Costa E, Davis J, Grayson DR, Guidotti A, Pappas GD, Pesold C (2001) Dendritic spine hypoplasticity and downregulation of reelin and GABAergic tone in schizophrenia vulnerability. Neurobiol Dis 8(5):723–742. doi:10.1006/nbdi.2001.0436
23. Couve A, Moss SJ, Pangalos MN (2000) GABAB receptors: a new paradigm in G protein signaling. Mol Cell Neurosci 16(4):296–312. doi:10.1006/mcne.2000.0908
24. Del Rio JA, Soriano E, Ferrer I (1992) Development of GABA-immunoreactivity in the neocortex of the mouse. J Comp Neurol 326(4):501–526
25. Druga R (2009) Neocortical inhibitory system. Folia Biol 55(6):201–217
26. Eastwood SL, Harrison PJ (2003) Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis. Mol Psychiatry 8(9):821–831. doi:10.1038/sj.mp.4001371
27. Fern R, Waxman SG, Ransom BR (1994) Modulation of anoxic injury in CNS white matter by adenosine and interaction between adenosine and GABA. J Neurophysiol 72(6):2609–2616
28. Fern R, Waxman SG, Ransom BR (1995) Endogenous GABA attenuates CNS white matter dysfunction following anoxia. J Neurosci Off J Soc Neurosci 15(1 Pt 2):699–708
29. Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, Viegi A, Berardi N, Maffei L (2010) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30(1):361–371
30. Harayama N, Shibuya I, Tanaka K, Kabashima N, Ueta Y, Yamashita H (1998) Inhibition of N- and P/Q-type calcium channels by postsynaptic GABAB receptor activation in rat supraoptic neurones. J Physiol 509(2):371–383. doi:10.1111/j.1469-7793.1998.371bn.x
31. Haydar TF, Wang F, Schwartz ML, Rakic P (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J Neurosci 20(15):5764–5774
32. Haynes RL, Gang X, Folkerth RD, Trachtenberg FL, Volpe JJ, Kinney HC (2011) Potential neuronal repair in cerebral white matter injury in the human neonate. Pediatr Res 69(1):62–67. doi:10.1203/PDR.0b013e3181ff3792
33. Hennou S, Khalilov I, Diabira D, Ben-Ari Y, Gozlan H (2002) Early sequential formation of functional GABAA and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci 16(2):197–208. doi:10.1046/j.1460-9568.2002.02073.x
34. Hensch TK, Stryker MP (2004) Columnar architecture sculpted by GABA circuits in developing cat visual cortex. Science 303(5664):1678–1681. doi:10.1126/science.1091031
35. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30(2):515–524. doi:10.1016/S0896-6273(01)00297-5
36. Hunt RF, Boychuk JA, Smith BN (2013) Neural circuit mechanisms of post-traumatic epilepsy. Front Cell Neurosci 7:89. doi:10.3389/fncel.2013.00089
37. Hyde TM, Lipska BK, Ali T, Mathew SV, Law AJ, Metitiri OE, Straub RE et al (2011) Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci 31(30):11088–11095
38. Iwai Y, Fagiolini M, Obata K, Hensch TK (2003) Rapid critical period induction by tonic inhibition in visual cortex. J Neurosci 23(17):6695–6702
39. Joshi D, Fung SJ, Rothwell A, Weickert CS (2012) Higher gamma-aminobutyric acid neuron density in the white matter of orbital frontal cortex in schizophrenia. Biol Psychiatry 72(9):725–733
40. Jovanovic JN, Thomson AM (2011) Development of cortical GABAergic innervation. Front Cell Neurosci 5:14. doi:10.3389/fncel.2011.00014
41. Judaš M, Sedmak G, Pletikos M, Jovanov-Milošević N (2010) Populations of subplate and interstitial neurons in fetal and adult human telencephalon. J Anat 217(4):381–399. doi:10.1111/j.1469-7580.2010.01284.x
42. Káradóttir R, Attwell D (2007) Neurotransmitter receptors in the life and death of oligodendrocytes. Neuroscience 145(4):1426–1438. doi:10.1016/j.neuroscience.2006.08.070
43. Kasyanov AM, Safiulina VF, Voronin LL, Cherubini E (2004) GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A 101(11):3967–3972. doi:10.1073/pnas.0305974101
44. Kilb W (2012) Development of the GABAergic system from birth to adolescence. Neuroscientist Rev J Bringing Neurobiol Neurol Psychiatry 18(6):613–630. doi:10.1177/1073858411422114
45. Kinney HC, Haynes RL, Xu G, Andiman SE, Folkerth RD, Sleeper LA, Volpe JJ (2012) Neuron deficit in the white matter and subplate in periventricular leukomalacia. Ann Neurol 71(3):397–406
46. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2(5):467–472. doi:10.1038/8138
47. Lee V, Maguire J (2014) The impact of tonic GABAA receptor-mediated inhibition on neuronal excitability varies across brain region and cell type. Front Neural Circ 8. doi:10.3389/fncir.2014.00003
48. Letinic K, Zoncu R, Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417(6889):645–649. doi:10.1038/nature00779
49. Leto K, Bartolini A, Yanagawa Y, Obata K, Magrassi L, Schilling K, Rossi F (2009) Laminar fate and phenotype specification of cerebellar GABAergic interneurons. J Neurosci 29(21):7079–7091. doi:10.1523/JNEUROSCI.0957-09.2009
50. Li Y, Lei Z, Xu ZC (2009) Enhancement of inhibitory synaptic transmission in large aspiny neurons after transient cerebral ischemia. Neuroscience 159(2):670–681. doi:10.1016/j.neuroscience.2008.12.046
51. Li Y, Blanco GD, Lei Z, Xu ZC (2010) Increased GAD expression in the striatum after transient cerebral ischemia. Mol Cell Neurosci 45(4):370–377
52. Lin S, Bergles DE (2004) Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 7(1):24–32. doi:10.1038/nn1162
53. Lipton P (1999) Ischemic cell death in brain neurons. Physiol Rev 79(4):1431–1568
54. López-Bendito G, Luján R, Shigemoto R, Ganter P, Paulsen O, Molnár Z (2003) Blockade of GABAB receptors alters the tangential migration of cortical neurons. Cereb Cortex 13(9):932–942. doi:10.1093/cercor/13.9.932
55. LoTurco JJ, Owens DF, Heath MJS, Davis MBE, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15(6):1287–1298
56. Luhmann HJ, Prince DA (1990) Control of NMDA receptor-mediated activity by GABAergic mechanisms in mature and developing rat neocortex. Dev Brain Res 54(2):287–290. doi:10.1016/0165-3806(90)90152-O
57. Luján R, Shigemoto R, López-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130(3):567–580. doi:10.1016/j.neuroscience.2004.09.042
58. Luyt K, Slade TP, Dorward JJ, Durant CF, Yue W, Shigemoto R, Mundell SJ, Váradi A, Molnár E (2007) Developing oligodendrocytes express functional GABAB receptors that stimulate cell proliferation and migration. J Neurochem 100(3):822–840. doi:10.1111/j.1471-4159.2006.04255.x
59. Macdonald RL, Olsen RW (1994) Gabaa receptor channels. Annu Rev Neurosci 17(1):569–602
60. Maloku E, Covelo IR, Hanbauer I, Guidotti A, Kadriu B, Hu Q, Davis JM, Costa E (2010) Lower number of cerebellar purkinje neurons in psychosis is associated with reduced reelin expression. Proc Natl Acad Sci U S A 107(9):4407–4411
61. Mangin J-M, Gallo V (2011) The curious case of NG2 cells: transient trend or game changer? ASN Neuro 3(1):37–49. doi:10.1042/AN20110001
62. Marín O, Rubenstein JLR (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2(11):780–790. doi:10.1038/35097509
63. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Caizhi W (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5(10):793–807. doi:10.1038/nrn1519
64. Miller LG, Galpern WR, Dunlap K, Dinarello CA, Turner TJ (1991) Interleukin-1 augments gamma-aminobutyric acidA receptor function in brain. Mol Pharmacol 39(2):105–108
65. Misgeld U, Bijak M, Jarolimek W (1995) A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol 46(4):423–462
66. Mtchedlishvili Z, Lepsveridze E, Xu H, Kharlamov EA, Lu B, Kelly KM (2010) Increase of GABAA receptor-mediated tonic inhibition in dentate granule cells after traumatic brain injury. Neurobiol Dis 38(3):464–475. doi:10.1016/j.nbd.2010.03.012
67. Obrietan K, van den Pol AN (1998) GABAB receptor-mediated inhibition of GABAA receptor calcium elevations in developing hypothalamic neurons. J Neurophysiol 79(3):1360–1370
68. Owens DF, Kriegstein AR (2002) Is there more to gaba than synaptic inhibition? Nat Rev Neurosci 3(9):715–727. doi:10.1038/nrn919
69. Pesold C, Impagnatiello F, Pisu MG, Uzunov DP, Costa E, Guidotti A, Caruncho HJ (1998) Reelin is preferentially expressed in neurons synthesizing γ-aminobutyric acid in cortex and hippocampus of adult rats. Proc Natl Acad Sci U S A 95(6):3221–3226
70. Petanjek Z, Dujmović A, Kostović I, Esclapez M (2008) Distinct origin of GABA-ergic neurons in forebrain of man, nonhuman primates and lower mammals. Coll Antropol 32(Suppl 1):9–17
71. Petanjek Z, Berger B, Esclapez M (2009) Origins of cortical GABAergic neurons in the cynomolgus monkey. Cereb Cortex 19(2):249–262. doi:10.1093/cercor/bhn078
72. Pfeffer CK, Stein V, Keating DJ, Maier H, Rinke I, Rudhard Y, Hentschke M, Rune GM, Jentsch TJ, Hübner CA (2009) NKCC1-dependent GABAergic excitation drives synaptic network maturation during early hippocampal development. J Neurosci 29(11):3419–3430. doi:10.1523/JNEUROSCI.1377-08.2009
73. Riccio O, Murthy S, Szabo G, Vutskits L, Kiss JZ, Vitalis T, Lebrand C, Dayer AG (2012) New pool of cortical interneuron precursors in the early postnatal dorsal white matter. Cereb Cortex 22(1):86–98. doi:10.1093/cercor/bhr086
74. Rice DS, Curran T (2001) Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24(1):1005–1039. doi:10.1146/annurev.neuro.24.1.1005
75. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl|[minus]| co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397(6716):251–255. doi:10.1038/16697
76. Robinson S, Li Q, DeChant A, Cohen ML (2006) Neonatal loss of Γ–aminobutyric acid pathway expression after human perinatal brain injury. J Neurosurg 104(6 Suppl):396
77. Rudy B, Fishell G, Lee SH, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100 % of neocortical GABAergic neurons. Dev Neurobiol 71(1):45–61. doi:10.1002/dneu.20853
78. Segovia KN, McClure M, Moravec M, Luo NL, Wan Y, Gong X, Riddle A et al (2008) Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann Neurol 63(4):520–530
79. Strata F, Atzori M, Molnar M, Ugolini G, Tempia F, Cherubini E (1997) A pacemaker current in dye-coupled hilar interneurons contributes to the generation of giant GABAergic potentials in developing hippocampus. J Neurosci 17(4):1435–1446
80. Suárez-Solá ML, González-Delgado FJ, Pueyo-Morlans M, Medina-Bolívar OC, Hernández-Acosta NC, González-Gómez M, Meyer G (2009) Neurons in the white matter of the adult human neocortex. Front Neuroanat 3:7. doi:10.3389/neuro.05.007.2009
81. Sun D, Murali SG (1999) Na+−K+−2Cl−cotransporter in immature cortical neurons: a role in intracellular Cl−regulation. J Neurophysiol 81(4):1939–1948
82. Takesian AE, Hensch TK (2013) Chapter 1 - Balancing plasticity/stability across brain development. In: Nahum M, Van Vleet T, Merzenich MM (eds) Progress in brain research, vol 207. Changing brains applying brain plasticity to advance and recover human ability. Elsevier, 3–34. http://www.sciencedirect.com/science/article/pii/B9780444633279000011
83. Tan S-S, Kalloniatis M, Sturm K, Tam PL, Reese BE, Faulkner-Jones B (1998) Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron 21(2):295–304
84. Tao R, Li C, Newburn EN, Ye T, Lipska BK, Herman MM, Weinberger DR, Kleinman JE, Hyde TM (2012) Transcript-specific associations of SLC12A5 (KCC2) in human prefrontal cortex with development, schizophrenia, and affective disorders. J Neurosci 32(15):5216–5222. doi:10.1523/JNEUROSCI.4626-11.2012
85. van den Pol AN, Gao XB, Patrylo PR, Ghosh PK, Obrietan K (1998) Glutamate inhibits GABA excitatory activity in developing neurons. J Neurosci 18(24):10749–10761
86. Wang DD, Kriegstein AR (2009) Defining the role of GABA in cortical development. J Physiol 587(9):1873–1879. doi:10.1113/jphysiol.2008.167635
87. Wang H, Yan Y, Kintner DB, Lytle C, Sun D (2003) GABA-mediated trophic effect on oligodendrocytes requires Na-K-2Cl cotransport activity. J Neurophysiol 90(2):1257–1265. doi:10.1152/jn.01174.2002
88. Williams JR, Sharp JW, Kumari VG, Wilson M, Payne JA (1999) The neuron-specific K-Cl cotransporter, KCC2 antibody development and initial characterization of the protein. J Biol Chem 274(18):12656–12664. doi:10.1074/jbc.274.18.12656
89. Xu G, Broadbelt KG, Haynes RL, Folkerth RD, Borenstein NS, Belliveau RA, Trachtenberg FL, Volpe JJ, Kinney HC (2011) Late development of the GABAergic system in the human cerebral cortex and white matter. J Neuropathol Exp Neurol 70(10):841–858. doi:10.1097/NEN.0b013e31822f471c
90. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A (2004) Cl− uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557(3):829–841. doi:10.1113/jphysiol.2004.062471
91. Yan XX, Jen LS, Garey LJ (1996) NADPH-diaphorase-positive neurons in primate cerebral cortex colocalize with GABA and calcium-binding proteins. Cereb Cortex 6(3):524–529. doi:10.1093/cercor/6.3.524
92. Yang Y, Fung SJ, Rothwell A, Tianmei S, Weickert CS (2011) Increased interstitial white matter neuron density in the DLPFC of people with schizophrenia. Biol Psychiatry 69(1):63–70
93. Yu Z, Fang Q, Xiao X, Wang Y-Z, Cai Y-Q, Cao H, Hu G et al (2013) GABA transporter-1 deficiency confers schizophrenia-like behavioral phenotypes. PLoS ONE 8(7):e69883. doi:10.1371/journal.pone.0069883