Altered cortical expression of GABA-related genes in schizophrenia: Illness progression vs developmental disturbance

Schizophrenia Bulletin

Volumn 41, Issue 1, 2015, Pages 180-191

  Hoftman, Gil D ^a   Volk, David W ^a   Bazmi, H Holly ^a   Li, Siyu ^b   Sampson, Allan R ^b   Lewis, David A ^a  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

GABA; neurodevelopment; parvalbumin; prefrontal cortex; schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; CALRETININ; GABA TRANSPORTER 1; GLUTAMATE DECARBOXYLASE 67; MESSENGER RNA; PARVALBUMIN; SOMATOSTATIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; CALB2 PROTEIN, HUMAN; GABRA1 PROTEIN, HUMAN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; SLC32A1 PROTEIN, HUMAN; SLC6A1 PROTEIN, HUMAN;

ADULTHOOD; ANIMAL TISSUE; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE COURSE; DISEASE DURATION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; NONHUMAN; PERINATAL PERIOD; PREFRONTAL CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; SCHIZOPHRENIA; ADULT; ANIMAL; CASE CONTROL STUDY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MIDDLE AGED; PSYCHOSIS;

ADULT; ANIMALS; CALBINDIN 2; CASE-CONTROL STUDIES; DISEASE PROGRESSION; FEMALE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMATE DECARBOXYLASE; HUMANS; MACACA MULATTA; MALE; MIDDLE AGED; PARVALBUMINS; PREFRONTAL CORTEX; PSYCHOTIC DISORDERS; RECEPTORS, GABA-A; RNA, MESSENGER; SCHIZOPHRENIA; SOMATOSTATIN; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84928807059     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbt178     Document Type: Article

References (63)

1. Barch DM, Ceaser A. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci. 2012;16:27-34.
2. Benes FM, Berretta S. GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology. 2001;25:1-27.
3. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 2005;6:312-324.
4. Akbarian S, Kim JJ, Potkin SG, et al. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry. 1995;52:258-266.
5. Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA. Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry. 2000;57:237-245.
6. Guidotti A, Auta J, Davis JM, et al. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry. 2000;57:1061-1069.
7. Duncan CE, Webster MJ, Rothmond DA, Bahn S, Elashoff M, Shannon Weickert C. Prefrontal GABA(A) receptor alpha-subunit expression in normal postnatal human development and schizophrenia. J Psychiatr Res. 2010;44:673-681.
8. Hyde TM, Lipska BK, Ali T, et al. Expression of GABA signaling molecules KCC2, NKCC1, and GAD1 in cortical development and schizophrenia. J Neurosci. 2011;31:11088-11095.
9. Vawter MP, Crook JM, Hyde TM, et al. Microarray analysis of gene expression in the prefrontal cortex in schizophrenia: a preliminary study. Schizophr Res. 2002;58:11-20.
10. Straub RE, Lipska BK, Egan MF, et al. Allelic variation in GAD1 (GAD67) is associated with schizophrenia and influences cortical function and gene expression. Mol Psychiatry. 2007;12:854-869.
11. Volk D, Austin M, Pierri J, Sampson A, Lewis D. GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: decreased expression in a subset of neurons. Am J Psychiatry. 2001;158:256-265.
12. Fung SJ, Webster MJ, Weickert CS, Weicker CS. Expression of VGluT1 and VGAT mRNAs in human dorsolateral prefrontal cortex during development and in schizophrenia. Brain Res. 2011;1388:22-31.
13. Akbarian S, Huntsman MM, Kim JJ, et al. GABAA receptor subunit gene expression in human prefrontal cortex: comparison of schizophrenics and controls. Cereb Cortex. 1995;5:550-560.
14. Beneyto M, Abbott A, Hashimoto T, Lewis DA. Laminaspecific alterations in cortical GABA(A) receptor subunit expression in schizophrenia. Cereb Cortex. 2011;21:999-1011.
15. Volk DW, Pierri JN, Fritschy JM, Auh S, Sampson AR, Lewis DA. Reciprocal alterations in pre-and postsynaptic inhibitory markers at chandelier cell inputs to pyramidal neurons in schizophrenia. Cereb Cortex. 2002;12:1063-1070.
16. Mellios N, Huang HS, Baker SP, Galdzicka M, Ginns E, Akbarian S. Molecular determinants of dysregulated GABAergic gene expression in the prefrontal cortex of subjects with schizophrenia. Biol Psychiatry. 2009;65:1006-1014.
17. Fung SJ, Webster MJ, Sivagnanasundaram S, Duncan C, Elashoff M, Weickert CS. Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry. 2010;167:1479-1488.
18. Hashimoto T, Volk DW, Eggan SM, et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci. 2003;23:6315-6326.
19. Volk DW, Matsubara T, Li S, et al. Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia. Am J Psychiatry. 2012;169:1082-1091.
20. Curley AA, Arion D, Volk DW, et al. Cortical deficits of glutamic acid decarboxylase 67 expression in schizophrenia: clinical, protein, and cell type-specific features. Am J Psychiatry. 2011;168:921-929.
21. Woo TU, Miller JL, Lewis DA. Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry. 1997;154:1013-1015.
22. Morris HM, Hashimoto T, Lewis DA. Alterations in somatostatin mRNA expression in the dorsolateral prefrontal cortex of subjects with schizophrenia or schizoaffective disorder. Cereb Cortex. 2008;18:1575-1587.
23. Hashimoto T, Arion D, Unger T, et al. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry. 2008;13:147-161.
24. Reynolds GP, Abdul-Monim Z, Neill JC, Zhang ZJ. Calcium binding protein markers of GABA deficits in schizophrenia-postmortem studies and animal models. Neurotox Res. 2004;6:57-61.
25. Sakai T, Oshima A, Nozaki Y, et al. Changes in density of calcium-binding-protein-immunoreactive GABAergic neurons in prefrontal cortex in schizophrenia and bipolar disorder. Neuropathology. 2008;28:143-150.
26. Beasley CL, Cotter DR, Everall IP. Density and distribution of white matter neurons in schizophrenia, bipolar disorder and major depressive disorder: no evidence for abnormalities of neuronal migration. Mol Psychiatry. 2002;7:564-570.
27. Cotter D, Landau S, Beasley C, et al. The density and spatial distribution of GABAergic neurons, labelled using calcium binding proteins, in the anterior cingulate cortex in major depressive disorder, bipolar disorder, and schizophrenia. Biol Psychiatry. 2002;51:377-386.
28. Tooney PA, Chahl LA. Neurons expressing calcium-binding proteins in the prefrontal cortex in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2004;28:273-278.
29. Lewis DA, González-Burgos G. Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology. 2008;33:141-165.
30. Weinberger DR. From neuropathology to neurodevelopment. Lancet. 1995;346:552-557.
31. Beneyto M, Lewis DA. Insights into the neurodevelopmental origin of schizophrenia from postmortem studies of prefrontal cortical circuitry. Int J Dev Neurosci. 2011;29:295-304.
32. Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA. Maturation of cognitive processes from late childhood to adulthood. Child Dev. 2004;75:1357-1372.
33. Reichenberg A, Caspi A, Harrington H, et al. Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: a 30-year study. Am J Psychiatry. 2010;167:160-169.
34. Hoftman GD, Lewis DA. Postnatal developmental trajectories of neural circuits in the primate prefrontal cortex: identifying sensitive periods for vulnerability to schizophrenia. Schizophr Bull. 2011;37:493-503.
35. Catts VS, Fung SJ, Long LE, et al. Rethinking schizophrenia in the context of normal neurodevelopment. Front Cell Neurosci. 2013;7:60.
36. Webster MJ, Elashoff M, Weickert CS. Molecular evidence that cortical synaptic growth predominates during the first decade of life in humans. Int J Dev Neurosci. 2011;29:225-236.
37. Erickson SL, Lewis DA. Postnatal development of parvalbumin-and GABA transporter-immunoreactive axon terminals in monkey prefrontal cortex. J Comp Neurol. 2002;448:186-202.
38. Hashimoto T, Bazmi HH, Mirnics K, Wu Q, Sampson AR, Lewis DA. Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia. Am J Psychiatry. 2008;165:479-489.
39. Volk DW, Radchenkova PV, Walker EM, Sengupta EJ, Lewis DA. Cortical opioid markers in schizophrenia and across postnatal development. Cereb Cortex. 2012;22:1215-1223.
40. Bourgeois JP, Goldman-Rakic PS, Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex. 1994;4:78-96.
41. Huttenlocher PR. Synaptic density in human frontal cortex-developmental changes and effects of aging. Brain Res. 1979;163:195-205.
42. Petanjek Z, Judaš M, Šimic G, et al. Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci USA. 2011;108:13281-13286.
43. Anderson SA, Classey JD, Condé F, Lund JS, Lewis DA. Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex. Neuroscience. 1995;67:7-22.
44. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature. 2010;468:203-212.
45. Hensch TK. Critical period plasticity in local cortical circuits. Nat Rev Neurosci. 2005;6:877-888.
46. Lewandowski KE, Cohen BM, Ongur D. Evolution of neuropsychological dysfunction during the course of schizophrenia and bipolar disorder. Psychol Med. 2011;41:225-241.
47. Zipursky RB, Reilly TJ, Murray RM. The myth of schizophrenia as a progressive brain disease. Schizophr Bull. 2013;39:1363-1372.
48. Huang HS, Matevossian A, Whittle C, et al. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. J Neurosci. 2007;27:11254-11262.
49. Colantuoni C, Lipska BK, Ye T, et al. Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature. 2011;478:519-523.
50. Hashimoto T, Nguyen QL, Rotaru D, et al. Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry. 2009;65:1015-1023.
51. Maldonado-Avilés JG, Curley AA, Hashimoto T, et al. Altered markers of tonic inhibition in the dorsolateral prefrontal cortex of subjects with schizophrenia. Am J Psychiatry. 2009;166:450-459.
52. Drake CT, Milner TA. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res. 1999;849:203-215.
53. Drake CT, Milner TA. Mu opioid receptors are in discrete hippocampal interneuron subpopulations. Hippocampus. 2002;12:119-136.
54. Stumm RK, Zhou C, Schulz S, Höllt V. Neuronal types expressing mu-and delta-opioid receptor mRNA in the rat hippocampal formation. J Comp Neurol. 2004;469:107-118.
55. Drasbek KR, Hoestgaard-Jensen K, Jensen K. Modulation of extrasynaptic THIP conductances by GABAA-receptor modulators in mouse neocortex. J Neurophysiol. 2007;97:2293-2300.
56. Drasbek KR, Jensen K. THIP, a hypnotic and antinociceptive drug, enhances an extrasynaptic GABAA receptormediated conductance in mouse neocortex. Cereb Cortex. 2006;16:1134-1141.
57. Sibille E, Morris HM, Kota RS, Lewis DA. GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol. 2011;14:721-734.
58. Lewis DA, Levitt P. Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci. 2002;25:409-432.
59. Moore TH, Zammit S, Lingford-Hughes A, et al. Cannabis use and risk of psychotic or affective mental health outcomes: a systematic review. Lancet. 2007;370:319-328.
60. Le Magueresse C, Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron. 2013;77:388-405.
61. Fagiolini M, Fritschy JM, Löw K, Möhler H, Rudolph U, Hensch TK. Specific GABAA circuits for visual cortical plasticity. Science. 2004;303:1681-1683.
62. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P. Differential synaptic localization of two major gammaaminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA. 1996;93:11939-11944.
63. Fung SJ, Sivagnanasundaram S, Weickert CS. Lack of change in markers of presynaptic terminal abundance alongside subtle reductions in markers of presynaptic terminal plasticity in prefrontal cortex of schizophrenia patients. Biol Psychiatry. 2011;69:71-79.