Glutamate Decarboxylase 67 Deficiency in a Subset of GABAergic Neurons Induces Schizophrenia-Related Phenotypes

Neuropsychopharmacology

Volumn 40, Issue 10, 2015, Pages 2475-2486

  Fujihara, Kazuyuki ^a,b   Miwa, Hideki ^a,b   Kakizaki, Toshikazu ^a,b   Kaneko, Ryosuke ^a,b   Mikuni, Masahiko ^a   Tanahira, Chiyoko ^c   Tamamaki, Nobuaki ^c   Yanagawa, Yuchio ^a,b  

^a GUNMA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; DIZOCILPINE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; 2-AMINO-5-PHOSPHOPENTANOIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ACTIN; AMINO ACID RECEPTOR BLOCKING AGENT; GLUTAMATE DECARBOXYLASE 1; SOMATOSTATIN; VALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR CHANGE; BEHAVIOR DISORDER; BRAIN ELECTROPHYSIOLOGY; CLINICAL FEATURE; CONTROLLED STUDY; DENDRITIC SPINE; DISEASE ASSOCIATION; GLUTAMATERGIC SYNAPSE; HAPLOINSUFFICIENCY; HETEROZYGOTE; HIPPOCAMPAL CA1 REGION; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; MEMORY; MOUSE; MUTANT MOUSE STRAIN; NERVE CELL; NONHUMAN; PATHOGENESIS; PHENOTYPIC VARIATION; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SCHIZOPHRENIA; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SOCIAL ASPECT; SPINE MOBILITY; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; DEFICIENCY; DENDRITE; DISEASE MODEL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; GENETICS; HIPPOCAMPUS; MAZE TEST; METABOLISM; PATHOLOGY; PHENOTYPE; PHYSIOLOGY; STARTLE REFLEX; TRANSGENIC MOUSE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTINS; ACTION POTENTIALS; ANIMALS; DENDRITES; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID ANTAGONISTS; EXPLORATORY BEHAVIOR; GABAERGIC NEURONS; GLUTAMATE DECARBOXYLASE; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; PARVALBUMINS; PHENOTYPE; REFLEX, STARTLE; SCHIZOPHRENIA; SOMATOSTATIN; VALINE;

EID: 84939263362     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.117     Document Type: Article

References (50)

1. Beasley CL, Reynolds GP (1997). Parvalbumin-immunoreactive neurons are reduced in the prefrontal cortex of schizophrenics. Schizophr Res 24: 349-355.
2. Behrens MM, Ali SS, Dao DN, Lucero J, Shekhtman G, Quick KL et al (2007). Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase. Science 318: 1645-1647.
3. Belforte JE, Zsiros V, Sklar ER, Jiang Z, Yu G, Li Y et al (2010). Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 13: 76-83.
4. Ben-Ari Y, Khalilov I, Represa A, Gozlan H (2004). Interneurons set the tune of developing networks. Trends Neurosci 27: 422-427.
5. Blaha CD, Yang CR, Floresco SB, Barr AM, Phillips AG (1997). Stimulation of the ventral subiculum of the hippocampus evokes glutamate receptor-mediated changes in dopamine efflux in the rat nucleus accumbens. Eur J Neurosci 9: 902-911.
6. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology (Berl) 156: 234-258.
7. Brown JA, Ramikie TS, Schmidt MJ, Báldi R, Garbett K, Everheart MG et al (2015). Inhibition of parvalbumin-expressing interneurons results in complex behavioral changes. Mol Psychiatry; e-pub ahead of print 27 January 2015; doi:10.1038/mp.2014.192.
8. Bubeníková-Valesová V, Horácek J, Vrajová M, Höschl C (2008). Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 32: 1014-1023.
9. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, Fu Y et al (2007). GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54: 889-903.
10. Couture SM, Penn DL, Roberts DL (2006). The functional significance of social cognition in schizophrenia: a review. Schizophr Bull 32(Suppl 1): S44-S63.
11. Ducharme G, Lowe GC, Goutagny R, Williams S (2012). Early alterations in hippocampal circuitry and theta rhythm generation in a mouse model of prenatal infection: implications for schizophrenia. PLoS One 7: e29754.
12. Esclapez M, Houser CR (1999). Up-regulation of GAD65 and GAD67 in remaining hippocampal GABA neurons in a model of temporal lobe epilepsy. J Comp Neurol 412: 488-505.
13. Glantz LA, Lewis DA (2000). Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57: 65-73.
14. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR et al (2000). Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: a postmortem brain study. Arch Gen Psychiatry 57: 1061-1069.
15. Hashimoto T, Arion D, Unger T, Maldonado-Avilés JG, Morris HM, Volk DW et al (2008). Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Mol Psychiatry 13: 147-161.
16. Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z et al (2003). Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 23: 6315-6326.
17. Hikida T, Jaaro-Peled H, Seshadri S, Oishi K, Hookway C, Kong S et al (2007). Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci USA 104: 14501-14506.
18. Hunt DL, Castillo PE (2012). Synaptic plasticity of NMDA receptors: mechanisms and functional implications. Curr Opin Neurobiol 22: 496-508.
19. Huttenlocher PR, Dabholkar AS (1997). Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387: 167-178.
20. Hwang I, Kim D-W, Yoo K-Y, Kang T-C, Kim Y, Kwon D et al (2007). Parvalbumin immunoreactivity and protein content alter in the hippocampus after adrenalectomy in seizure sensitive gerbils. Neurol Res 29: 441-448.
21. Insel TR (2010). Rethinking schizophrenia. Nature 468: 187-193.
22. Kägi U, Berchtold MW, Heizmann CW (1987). Ca2+-binding parvalbumin in rat testis. Characterization, localization, and expression during development. J Biol Chem 262: 7314-7320.
23. Kirson ED, Schirra C, Konnerth A, Yaari Y (1999). Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells. J Physiol 521(Pt 1): 99-111.
24. Kobayashi Y, Hensch TK (2013). Germline recombination by conditional gene targeting with Parvalbumin-Cre lines. Front Neural Circuits 7: 168.
25. Kosaka T, Heizmann CW (1989). Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res 483: 158-163.
26. Lahti AC, Koffel B, LaPorte D, Tamminga CA (1995). Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 13: 9-19.
27. Laruelle M, Abi-Dargham A (1999). Dopamine as the wind of the psychotic fire: new evidence from brain imaging studies. J Psychopharmacol 13: 358-371.
28. Lazarus MS, Krishnan K, Huang ZJ (2013). GAD67 deficiency in parvalbumin interneurons produces deficits in inhibitory transmission and network disinhibition in mouse prefrontal cortex. Cereb Cortex 25: 1290-1296.
29. Lee FHF, Zai CC, Cordes SP, Roder JC, Wong AHC (2013). Abnormal interneuron development in disrupted-in-schizophrenia- 1 L100P mutant mice. Mol Brain 6: 20.
30. Legault M, Wise RA (1999). Injections of N-methyl-D-aspartate into the ventral hippocampus increase extracellular dopamine in the ventral tegmental area and nucleus accumbens. Synapse 31: 241-249.
31. Liu WS, Pesold C, Rodriguez MA, Carboni G, Auta J, Lacor P et al (2001). Down-regulation of dendritic spine and glutamic acid decarboxylase 67 expressions in the reelin haploinsufficient heterozygous reeler mouse. Proc Natl Acad Sci USA 98: 3477-3482.
32. Lodge DJ, Behrens MM, Grace AA (2009). A loss of parvalbumincontaining interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci 29: 2344-2354.
33. Mauney SA, Athanas KM, Pantazopoulos H, Shaskan N, Passeri E, Berretta S et al (2013). Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia. Biol Psychiatry 74: 427-435.
34. Miwa H, Fukaya M, Watabe AM, Watanabe M, Manabe T (2008). Functional contributions of synaptically localized NR2B subunits of the NMDA receptor to synaptic transmission and long-term potentiation in the adult mouse CNS. J Physiol 586: 2539-2550.
35. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A et al (2004). Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 3: 303-314.
36. Obata K, Hirono M, Kume N, Kawaguchi Y, Itohara S, Yanagawa Y (2008). GABA and synaptic inhibition of mouse cerebellum lacking glutamate decarboxylase 67. Biochem Biophys Res Commun 370: 429-433.
37. Paul C-M, Magda G, Abel S (2009). Spatial memory: theoretical basis and comparative review on experimental methods in rodents. Behav Brain Res 203: 151-164.
38. Peleg-Raibstein D, Knuesel I, Feldon J (2008). Amphetamine sensitization in rats as an animal model of schizophrenia. Behav Brain Res 191: 190-201.
39. Piskulic D, Olver JS, Norman TR, Maruff P (2007). Behavioural studies of spatial working memory dysfunction in schizophrenia: a quantitative literature review. Psychiatry Res 150: 111-121.
40. Pohl V, Pattyn G, Berchtold M (1995). Parvalbumin expression during developmental differentiation of the rat ovary. Differentiation 59: 235-242.
41. Schiller J, Schiller Y (2001). NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr Opin Neurobiol 11: 343-348.
42. Schobel SA, Lewandowski NM, Corcoran CM, Moore H, Brown T, Malaspina D et al (2009). Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Arch Gen Psychiatry 66: 938-946.
43. Takao K, Kobayashi K, Hagihara H, Ohira K, Shoji H, Hattori S et al (2013). Deficiency of schnurri-2, an MHC enhancer binding protein, induces mild chronic inflammation in the brain and confers molecular, neuronal, and behavioral phenotypes related to schizophrenia. Neuropsychopharmacology 38: 1409-1425.
44. Tanahira C, Higo S, Watanabe K, Tomioka R, Ebihara S, Kaneko T et al (2009). Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice. Neurosci Res 63: 213-223.
45. Todtenkopf MS, Benes FM (1998). Distribution of glutamate decarboxylase65 immunoreactive puncta on pyramidal and nonpyramidal neurons in hippocampus of schizophrenic brain. Synapse 29: 323-332.
46. Torrey EF, Barci BM, Webster MJ, Bartko JJ, Meador-Woodruff JH, Knable MB (2005). Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol Psychiatry 57: 252-260.
47. Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA (2000). Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry 57: 237-245.
48. Wen L, Lu Y-S, Zhu X-H, Li X-M, Woo R-S, Chen Y-J et al (2010). Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci USA 107: 1211-1216.
49. Woo TU, Miller JL, Lewis DA (1997). Schizophrenia and the parvalbumin-containing class of cortical local circuit neurons. Am J Psychiatry 154: 1013-1015.
50. Zhang ZJ, Reynolds GP (2002). A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr Res 55: 1-10.