The contribution of GABAergic dysfunction to neurodevelopmental disorders

Trends in Molecular Medicine

Volumn 17, Issue 8, 2011, Pages 452-462

  Ramamoorthi, Kartik ^a,b   Lin, Yingxi ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CYSTEINE; FRAGILE X MENTAL RETARDATION PROTEIN; MEMBRANE PROTEIN; NEUROLIGIN 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; AUTISM; DEVELOPMENTAL DISORDER; DOWN SYNDROME; EPILEPSY; FRAGILE X SYNDROME; GABAERGIC SYSTEM; GENE MUTATION; GILLES DE LA TOURETTE SYNDROME; HUMAN; NERVE CELL PLASTICITY; NEURODEVELOPMENTAL DISORDER; NEUROFIBROMATOSIS; NEUROLOGIC DISEASE; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; RETT SYNDROME; REVIEW; SCHIZOPHRENIA; SYNAPSE;

ANIMALS; CELL MOVEMENT; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; HUMANS; NEURODEGENERATIVE DISEASES; NEURONS; SYNAPSES;

EID: 79961082953     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2011.03.003     Document Type: Review

References (108)

1. Lewis D.A., Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci. 2002, 25:409-432.
2. Rubenstein J.L., Merzenich M.M. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2003, 2:255-267.
3. Brenner R.P. EEG in convulsive and nonconvulsive status epilepticus. J. Clin. Neurophysiol. 2004, 21:319-331.
4. Casanova M.F., et al. Minicolumnar pathology in autism. Neurology 2002, 58:428-432.
5. Kalanithi P.S., et al. Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:13307-13312.
6. Kataoka Y., et al. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J. Comp. Neurol. 2010, 518:277-291.
7. Levitt P., et al. Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci. 2004, 27:400-406.
8. Lewis D.A., et al. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 2005, 6:312-324.
9. Letinic K., et al. Origin of GABAergic neurons in the human neocortex. Nature 2002, 417:645-649.
10. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
11. Xu Q., et al. Origins of cortical interneuron subtypes. J. Neurosci. 2004, 24:2612-2622.
12. Gelman D.M., et al. The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J. Neurosci. 2009, 29:9380-9389.
13. Anderson S.A., et al. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 1997, 19:27-37.
14. Fode C., et al. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev. 2000, 14:67-80.
15. Batista-Brito R., Fishell G. The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 2009, 87:81-118.
16. Yun K., et al. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 2001, 128:193-205.
17. Sussel L., et al. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 1999, 126:3359-3370.
18. Markram H., et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 2004, 5:793-807.
19. Batista-Brito R., et al. Gene expression in cortical interneuron precursors is prescient of their mature function. Cereb. Cortex 2008, 18:2306-2317.
20. Miyoshi G., et al. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J. Neurosci. 2007, 27:7786-7798.
21. Butt S.J., et al. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48:591-604.
22. Lavdas A.A., et al. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 1999, 19:7881-7888.
23. Anderson S.A., et al. Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb. Cortex 2002, 12:702-709.
24. Hernandez-Miranda L.R., et al. Molecules and mechanisms involved in the generation and migration of cortical interneurons. ASN Neuro 2010, 2:e00031.
25. Martinowich K., et al. New insights into BDNF function in depression and anxiety. Nat. Neurosci. 2007, 10:1089-1093.
26. Stefansson H., et al. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 2002, 71:877-892.
27. Flames N., et al. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 2004, 44:251-261.
28. Corfas G., et al. Neuregulin 1-erbB signaling and the molecular/cellular basis of schizophrenia. Nat. Neurosci. 2004, 7:575-580.
29. Anderson S.A., et al. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278:474-476.
30. Alifragis P., et al. Lhx6 regulates the migration of cortical interneurons from the ventral telencephalon but does not specify their GABA phenotype. J. Neurosci. 2004, 24:5643-5648.
31. Azim E., et al. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 2009, 12:1238-1247.
32. Colasante G., et al. Arx is a direct target of Dlx2 and thereby contributes to the tangential migration of GABAergic interneurons. J. Neurosci. 2008, 28:10674-10686.
33. Nobrega-Pereira S., et al. Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 2008, 59:733-745.
34. Lopez-Bendito G., et al. Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J. Neurosci. 2008, 28:1613-1624.
35. Li G., et al. Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J. Neurosci. 2008, 28:1085-1098.
36. Wang Y., et al. CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 2011, 69:61-76.
37. Olson E.C., Walsh C.A. Smooth, rough and upside-down neocortical development. Curr. Opin. Genet. Dev. 2002, 12:320-327.
38. Ben-Ari Y. Seizures beget seizures: the quest for GABA as a key player. Crit. Rev. Neurobiol. 2006, 18:135-144.
39. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 2002, 3:728-739.
40. Ben-Ari Y., et al. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 2007, 87:1215-1284.
41. Lu B., et al. Molecular mechanisms underlying neural circuit formation. Curr. Opin. Neurobiol. 2009, 19:162-167.
42. Sudhof T.C. Neuroligins and neurexins link synaptic function to cognitive disease. Nature 2008, 455:903-911.
43. Varoqueaux F., et al. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 2004, 83:449-456.
44. Chubykin A.A., et al. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007, 54:919-931.
45. Jamain S., et al. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 2003, 34:27-29.
46. Kim H.G., et al. Disruption of neurexin 1 associated with autism spectrum disorder. Am. J. Hum. Genet. 2008, 82:199-207.
47. Yan J., et al. Neurexin 1alpha structural variants associated with autism. Neurosci. Lett. 2008, 438:368-370.
48. Tabuchi K., et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 2007, 318:71-76.
49. Jamain S., et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:1710-1715.
50. Chadman K.K., et al. Minimal aberrant behavioral phenotypes of neuroligin-3 R451C knockin mice. Autism Res. 2008, 1:147-158.
51. Mei L., Xiong W.C. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 2008, 9:437-452.
52. Fazzari P., et al. Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464:1376-1380.
53. Ting A.K., et al. Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J. Neurosci. 2011, 31:15-25.
54. Karam C.S., et al. Signaling pathways in schizophrenia: emerging targets and therapeutic strategies. Trends Pharmacol. Sci. 2010, 31:381-390.
55. Terauchi A., et al. Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 2010, 465:783-787.
56. Knott G.W., et al. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 2002, 34:265-273.
57. Chattopadhyaya B., et al. Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 2004, 24:9598-9611.
58. Lin Y., et al. Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 2008, 455:1198-1204.
59. Morrow E.M., et al. Identifying autism loci and genes by tracing recent shared ancestry. Science 2008, 321:218-223.
60. Lu B. BDNF and activity-dependent synaptic modulation. Learn. Mem. 2003, 10:86-98.
61. Bolton M.M., et al. Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J. Neurosci. 2000, 20:3221-3232.
62. Huang Z.J., et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
63. Marty S., et al. Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci. 2000, 20:8087-8095.
64. Hong E.J., et al. Transcriptional control of cognitive development. Curr. Opin. Neurobiol. 2005, 15:21-28.
65. Soliman F., et al. A genetic variant BDNF polymorphism alters extinction learning in both mouse and human. Science 2010, 327:863-866.
66. Neves G., et al. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat. Rev. Neurosci. 2008, 9:65-75.
67. Kleschevnikov A.M., et al. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 2004, 24:8153-8160.
68. Cui Y., et al. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 2008, 135:549-560.
69. Fernandez F., Garner C.C. Over-inhibition: a model for developmental intellectual disability. Trends Neurosci. 2007, 30:497-503.
70. Fernandez F., et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 2007, 10:411-413.
71. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
72. Gardiner K., et al. Down syndrome: from understanding the neurobiology to therapy. J. Neurosci. 2010, 30:14943-14945.
73. Reeves R.H., et al. A mouse model for Down syndrome exhibits learning and behaviour deficits. Nat. Genet. 1995, 11:177-184.
74. Rueda N., et al. Chronic pentylenetetrazole but not donepezil treatment rescues spatial cognition in Ts65Dn mice, a model for Down syndrome. Neurosci. Lett. 2008, 433:22-27.
75. Belichenko P.V., et al. Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J. Comp. Neurol. 2004, 480:281-298.
76. Costa R.M., Silva A.J. Mouse models of neurofibromatosis type I: bridging the GAP. Trends Mol. Med. 2003, 9:19-23.
77. Costa R.M., et al. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 2002, 415:526-530.
78. Bitanihirwe B.K., et al. Glutamatergic deficits and parvalbumin-containing inhibitory neurons in the prefrontal cortex in schizophrenia. BMC Psychiatry 2009, 9:71.
79. Woo T.U., et al. Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder. Arch. Gen. Psychiatry 2004, 61:649-657.
80. Torrey E.F., et al. Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol. Psychiatry 2005, 57:252-260.
81. Belforte J.E., et al. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat. Neurosci. 2010, 13:76-83.
82. Chen Y.J., et al. ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21818-21823.
83. Wen L., et al. Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:1211-1216.
84. Alvarez-Dolado M., et al. Cortical inhibition modified by embryonic neural precursors grafted into the postnatal brain. J. Neurosci. 2006, 26:7380-7389.
85. Baraban S.C., et al. Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:15472-15477.
86. Martinez-Cerdeno V., et al. Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats. Cell Stem Cell 2010, 6:238-250.
87. Southwell D.G., et al. Cortical plasticity induced by inhibitory neuron transplantation. Science 2010, 327:1145-1148.
88. Sebe J.Y., Baraban S.C. The promise of an interneuron-based cell therapy for epilepsy. Dev. Neurobiol. 2010, 71:107-117.
89. Zhang C., et al. A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J. Neurosci. 2009, 29:10843-10854.
90. Etherton M.R., et al. Mouse neurexin-1alpha deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:17998-18003.
91. Chen R.Z., et al. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 2001, 27:327-331.
92. Guy J., et al. A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 2001, 27:322-326.
93. Chahrour M., Zoghbi H.Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 2007, 56:422-437.
94. Shahbazian M., et al. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 2002, 35:243-254.
95. Collins A.L., et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 2004, 13:2679-2689.
96. Chao H.T., et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 2010, 468:263-269.
97. Shilyansky C., et al. Neurofibromin regulates corticostriatal inhibitory networks during working memory performance. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13141-13146.
98. Mohn A.R., et al. Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 1999, 98:427-436.
99. Pletnikov M.V., et al. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol. Psychiatry 2008, 13:173-186. 115.
100. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat. Neurosci. 2010, 13:1161-1169.
101. Noebels J.L. The biology of epilepsy genes. Annu. Rev. Neurosci. 2003, 26:599-625.
102. D'Antuono M., et al. Involvement of cholinergic and gabaergic systems in the fragile X knockout mice. Neuroscience 2003, 119:9-13.
103. Dolen G., et al. Correction of fragile X syndrome in mice. Neuron 2007, 56:955-962.
104. Selby L., et al. Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein. Neurosci. Lett. 2007, 412:227-232.
105. Gibson J.R., et al. Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol. 2008, 100:2615-2626.
106. Curia G., et al. Downregulation of tonic GABAergic inhibition in a mouse model of fragile X syndrome. Cereb. Cortex 2009, 19:1515-1520.
107. The Dutch-Belgian Fragile X Consortium Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 1994, 78:23-33.
108. Hall J., et al. A neuregulin 1 variant associated with abnormal cortical function and psychotic symptoms. Nat. Neurosci. 2006, 9:1477-1478.