Prominent synaptic and metabolic abnormalities revealed by proteomic analysis of the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder (original) (raw)

• Frith C, Dolan R . The role of the prefrontal cortex in higher cognitive functions. Brain Res Cogn Brain Res 1996; 5: 175–181.
  Article CAS PubMed Google Scholar
• Goldman-Rakic PS, Selemon LD . Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophr Bull 1997; 23: 437–458.
  Article CAS PubMed Google Scholar
• Goldstein JM, Goodman JM, Seidman LJ, Kennedy DN, Makris N, Lee H et al. Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging. Arch Gen Psychiatry 1999; 56: 537–547.
  Article CAS PubMed Google Scholar
• Sanfilipo M, Lafargue T, Rusinek H, Arena L, Loneragan C, Lautin A et al. Volumetric measure of the frontal and temporal lobe regions in schizophrenia: relationship to negative symptoms. Arch Gen Psychiatry 2000; 57: 471–480.
  Article CAS PubMed Google Scholar
• Pantelis C, Velakoulis D, McGorry PD, Wood SJ, Suckling J, Phillips LJ et al. Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 2003; 361: 281–288.
  Article PubMed Google Scholar
• Drevets WC, Price JL, Simpson Jr JR, Todd RD, Reich T, Vannier M et al. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997; 386: 824–827.
  Article CAS PubMed Google Scholar
• Strakowski SM, Adler CM, DelBello MP . Volumetric MRI studies of mood disorders: do they distinguish unipolar and bipolar disorder? Bipolar Disord 2002; 4: 80–88.
  Article PubMed Google Scholar
• Sheline YI . Neuroimaging studies of mood disorder effects on the brain. Biol Psychiatry 2003; 54: 338–352.
  Article PubMed Google Scholar
• Selemon LD, Rajkowska G, Goldman-Rakic PS . Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three-dimensional, stereologic counting method. J Comp Neurol 1998; 392: 402–412.
  Article CAS PubMed Google Scholar
• Pierri JN, Volk CL, Auh S, Sampson A, Lewis DA . Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia. Arch Gen Psychiatry 2001; 58: 466–473.
  Article CAS PubMed Google Scholar
• Rajkowska G, Selemon LD, Goldman-Rakic PS . Neuronal and glial somal size in the prefrontal cortex: a postmortem morphometric study of schizophrenia and Huntington disease. Arch Gen Psychiatry 1998; 55: 215–224.
  Article CAS PubMed Google Scholar
• Broadbelt K, Byne W, Jones LB . Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex. Schizophr Res 2002; 58: 75–81.
  Article PubMed Google Scholar
• Black JE, Kodish IM, Grossman AW, Klintsova AY, Orlovskaya D, Vostrikov V et al. Pathology of layer V pyramidal neurons in the prefrontal cortex of patients with schizophrenia. Am J Psychiatry 2004; 161: 742–744.
  Article PubMed Google Scholar
• Rosoklija G, Toomayan G, Ellis SP, Keilp J, Mann JJ, Latov N et al. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 2000; 57: 349–356.
  Article CAS PubMed Google Scholar
• Kolluri N, Sun Z, Sampson AR, Lewis DA . Lamina-specific reductions in dendritic spine density in the prefrontal cortex of subjects with schizophrenia. Am J Psychiatry 2005; 162: 1200–1202.
  Article PubMed Google Scholar
• Cotter D, Mackay D, Chana G, Beasley C, Landau S, Everall IP . Reduced neuronal size and glial cell density in area 9 of the dorsolateral prefrontal cortex in subjects with major depressive disorder. Cereb Cortex 2002; 12: 386–394.
  Article PubMed Google Scholar
• Knable MB, Torrey EF, Webster MJ, Bartko JJ . Multivariate analysis of prefrontal cortical data from the Stanley Foundation Neuropathology Consortium. Brain Res Bull 2001; 55: 651–659.
  Article CAS PubMed Google Scholar
• Torrey EF, Barci BM, Webster MJ, Bartko JJ, Meador-Woodruff JH, Knable MB . Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol Psychiatry 2005; 57: 252–260.
  Article CAS PubMed Google Scholar
• Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci USA 2001; 98: 4746–4751.
  Article CAS PubMed PubMed Central Google Scholar
• Vawter MP, Crook JM, Hyde TM, Kleinman JE, Weinberger DR, Becker KG et al. Microarray analysis of gene expression in the prefrontal cortex in schizophrenia: a preliminary study. Schizophr Res 2002; 58: 11–20.
  Article PubMed Google Scholar
• Glatt SJ, Everall IP, Kremen WS, Corbeil J, Sasik R, Khanlou N et al. Comparative gene expression analysis of blood and brain provides concurrent validation of SELENBP1 up-regulation in schizophrenia. Proc Natl Acad Sci USA 2005; 102: 15533–15538.
  Article CAS PubMed PubMed Central Google Scholar
• Vawter MP, Barrett T, Cheadle C, Sokolov BP, Wood III WH, Donovan DM et al. Application of cDNA microarrays to examine gene expression differences in schizophrenia. Brain Res Bull 2001; 55: 641–650.
  Article CAS PubMed Google Scholar
• Mirnics K, Middleton FA, Marquez A, Lewis DA, Levitt P . Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 2000; 28: 53–67.
  Article CAS PubMed Google Scholar
• Eastwood SL, Burnet PW, Harrison PJ . Decreased hippocampal expression of the susceptibility gene PPP3CC and other calcineurin subunits in schizophrenia. Biol Psychiatry 2005; 57: 702–710.
  Article CAS PubMed Google Scholar
• Sawada K, Barr AM, Nakamura M, Arima K, Young CE, Dwork AJ et al. Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch Gen Psychiatry 2005; 62: 263–272.
  Article CAS PubMed Google Scholar
• Owen MJ, O’Donovan MC, Harrison PJ . Schizophrenia: a genetic disorder of the synapse? BMJ 2005; 330: 158–159.
  Article PubMed PubMed Central Google Scholar
• Frankle WG, Lerma J, Laruelle M . The synaptic hypothesis of schizophrenia. Neuron 2003; 39: 205–216.
  Article CAS PubMed Google Scholar
• Anderson L, Seilhamer J . A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 1997; 18: 533–537.
  Article CAS PubMed Google Scholar
• Gygi SP, Rochon Y, Franza BR, Aebersold R . Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999; 19: 1720–1730.
  Article CAS PubMed PubMed Central Google Scholar
• Johnston-Wilson NL, Sims CD, Hofmann JP, Anderson L, Shore AD, Torrey EF et al. Disease-specific alterations in frontal cortex brain proteins in schizophrenia, bipolar disorder, and major depressive disorder. The Stanley Neuropathology Consortium. Mol Psychiatry 2000; 5: 142–149.
  Article CAS PubMed Google Scholar
• Prabakaran S, Swatton JE, Ryan MM, Huffaker SJ, Huang JT, Griffin JL et al. Mitochondrial dysfunction in schizophrenia: evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 2004; 9: 684–697, 643.
  Article CAS PubMed Google Scholar
• Clark D, Dedova I, Cordwell S, Matsumoto I . A proteome analysis of the anterior cingulate cortex gray matter in schizophrenia. Mol Psychiatry 2006; 11: 459–470, 423.
  Article CAS PubMed Google Scholar
• Beasley CL, Pennington K, Behan A, Wait R, Dunn MJ, Cotter D . Proteomic analysis of the anterior cingulate cortex in the major psychiatric disorders: evidence for disease-associated changes. Proteomics 2006; 6: 3414–3425.
  Article CAS PubMed Google Scholar
• Vawter MP, Tomita H, Meng F, Bolstad B, Li J, Evans S et al. Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders. Mol Psychiatry 2006; 11: 615, 663–679.
  Article CAS PubMed PubMed Central Google Scholar
• Li JZ, Vawter MP, Walsh DM, Tomita H, Evans SJ, Choudary PV et al. Systematic changes in gene expression in postmortem human brains associated with tissue pH and terminal medical conditions. Hum Mol Genet 2004; 13: 609–616.
  Article CAS PubMed Google Scholar
• Fountoulakis M, Hardmeier R, Hoger H, Lubec G . Postmortem changes in the level of brain proteins. Exp Neurol 2001; 167: 86–94.
  Article CAS PubMed Google Scholar
• Franzen B, Yang Y, Sunnemark D, Wickman M, Ottervald J, Oppermann M et al. Dihydropyrimidinase related protein-2 as a biomarker for temperature and time dependent post mortem changes in the mouse brain proteome. Proteomics 2003; 3: 1920–1929.
  Article CAS PubMed Google Scholar
• O’Farrell PH . High resolution two-dimensional electrophoresis of proteins. J Biol Chem 1975; 250: 4007–4021.
  PubMed Google Scholar
• Rabilloud T, Valette C, Lawrence JJ . Sample application by in-gel rehydration improves the resolution of two-dimensional electrophoresis with immobilized pH gradients in the first dimension. Electrophoresis 1994; 15: 1552–1558.
  Article CAS PubMed Google Scholar
• Sanchez JC, Rouge V, Pisteur M, Ravier F, Tonella L, Moosmayer M et al. Improved and simplified in-gel sample application using reswelling of dry immobilized pH gradients. Electrophoresis 1997; 18: 324–327.
  Article CAS PubMed Google Scholar
• Gorg A, Postel W, Gunther S, Weser J, Strahler JR, Hanash SM et al. Approach to stationary two-dimensional pattern: influence of focusing time and immobiline/carrier ampholytes concentrations. Electrophoresis 1988; 9: 37–46.
  Article CAS PubMed Google Scholar
• Yan JX, Wait R, Berkelman T, Harry RA, Westbrook JA, Wheeler CH et al. A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 2000; 21: 3666–3672.
  Article CAS PubMed Google Scholar
• Eastwood SL, Burnet PW, Harrison PJ . Decreased hippocampal expression of the susceptibility gene PPP3CC and other calcineurin subunits in schizophrenia. Biol Psychiatry 2005; 57: 702–710.
  Article CAS PubMed Google Scholar
• Sawada K, Barr AM, Nakamura M, Arima K, Young CE, Dwork AJ et al. Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch Gen Psychiatry 2005; 62: 263–272.
  Article CAS PubMed Google Scholar
• Owen MJ, O’Donovan MC, Harrison PJ . Schizophrenia: a genetic disorder of the synapse? BMJ 2005; 330: 158–159.
  Article PubMed PubMed Central Google Scholar
• Frankle WG, Lerma J, Laruelle M . The synaptic hypothesis of schizophrenia. Neuron 2003; 39: 205–216.
  Article CAS PubMed Google Scholar
• Harrison PJ, Weinberger DR . Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005; 10: 40–68.
  Article CAS PubMed Google Scholar
• Eastwood SL, Harrison PJ . Hippocampal synaptic pathology in schizophrenia, bipolar disorder and major depression: a study of complexin mRNAs. Mol Psychiatry 2000; 5: 425–432.
  Article CAS PubMed Google Scholar
• Eastwood SL, Harrison PJ . Synaptic pathology in the anterior cingulate cortex in schizophrenia and mood disorders. A review and a Western blot study of synaptophysin, GAP-43 and the complexins. Brain Res Bull 2001; 55: 569–578.
  Article CAS PubMed Google Scholar
• Saito T, Guan F, Papolos DF, Lau S, Klein M, Fann CS et al. Mutation analysis of SYNJ1: a possible candidate gene for chromosome 21q22-linked bipolar disorder. Mol Psychiatry 2001; 6: 387–395.
  Article CAS PubMed Google Scholar
• Beasley CL, Honer WG, Bergmann K, Falkai P, Lutjohann D, Bayer TA . Reductions in cholesterol and synaptic markers in association cortex in mood disorders. Bipolar Disord 2005; 7: 449–455.
  Article CAS PubMed Google Scholar
• Byk T, Dobransky T, Cifuentes-Diaz C, Sobel A . Identification and molecular characterization of Unc-33-like phosphoprotein (Ulip), a putative mammalian homolog of the axonal guidance-associated unc-33 gene product. J Neurosci 1996; 16: 688–701.
  Article CAS PubMed PubMed Central Google Scholar
• Horiuchi M, Loebrich S, Brandstaetter JH, Kneussel M, Betz H . Cellular localization and subcellular distribution of Unc-33-like protein 6, a brain-specific protein of the collapsin response mediator protein family that interacts with the neuronal glycine transporter 2. J Neurochem 2005; 94: 307–315.
  Article CAS PubMed Google Scholar
• Kowara R, Chen Q, Milliken M, Chakravarthy B . Calpain-mediated truncation of dihydropyrimidinase-like 3 protein (DPYSL3) in response to NMDA and H2O2 toxicity. J Neurochem 2005; 95: 466–474.
  Article CAS PubMed Google Scholar
• Modregger J, Ritter B, Witter B, Paulsson M, Plomann M . All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 2000; 113(Part 24): 4511–4521.
  CAS PubMed Google Scholar
• Praefcke GJ, McMahon HT . The dynamin superfamily: universal membrane tubulation and fission molecules? Nat Rev Mol Cell Biol 2004; 5: 133–147.
  Article CAS PubMed Google Scholar
• Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG . Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat Neurosci 2000; 3: 661–669.
  Article CAS PubMed Google Scholar
• Predescu SA, Predescu DN, Timblin BK, Stan RV, Malik AB . Intersectin regulates fission and internalization of caveolae in endothelial cells. Mol Biol Cell 2003; 14: 4997–5010.
  Article CAS PubMed PubMed Central Google Scholar
• Fatemi SH, Earle JA, Stary JM, Lee S, Sedgewick J . Altered levels of the synaptosomal associated protein SNAP-25 in hippocampus of subjects with mood disorders and schizophrenia. NeuroReport 2001; 12: 3257–3262.
  Article CAS PubMed Google Scholar
• Thompson PM, Egbufoama S, Vawter MP . SNAP-25 reduction in the hippocampus of patients with schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2003; 27: 411–417.
  Article CAS PubMed Google Scholar
• Sokolov BP . Expression of NMDAR1, GluR1, GluR7, and KA1 glutamate receptor mRNAs is decreased in frontal cortex of “neuroleptic-free” schizophrenics: evidence on reversible up-regulation by typical neuroleptics. J Neurochem 1998; 71: 2454–2464.
  Article CAS PubMed Google Scholar
• Le Corre S, Harper CG, Lopez P, Ward P, Catts S . Increased levels of expression of an NMDARI splice variant in the superior temporal gyrus in schizophrenia. NeuroReport 2000; 11: 983–986.
  Article CAS PubMed Google Scholar
• Robinson PJ, Sontag JM, Liu JP, Fykse EM, Slaughter C, McMahon H et al. Dynamin GTPase regulated by protein kinase C phosphorylation in nerve terminals. Nature 1993; 365: 163–166.
  Article CAS PubMed Google Scholar
• Sontag JM, Fykse EM, Ushkaryov Y, Liu JP, Robinson PJ, Sudhof TC . Differential expression and regulation of multiple dynamins. J Biol Chem 1994; 269: 4547–4554.
  CAS PubMed Google Scholar
• Kristiansen LV, Beneyto M, Haroutunian V, Meador-Woodruff JH . Changes in NMDA receptor subunits and interacting PSD proteins in dorsolateral prefrontal and anterior cingulate cortex indicate abnormal regional expression in schizophrenia. Mol Psychiatry 2006; 11: 737–747, 705.
  Article CAS PubMed Google Scholar
• Toyooka K, Muratake T, Tanaka T, Igarashi S, Watanabe H, Takeuchi H et al. 14-3-3 protein eta chain gene (YWHAH) polymorphism and its genetic association with schizophrenia. Am J Med Genet 1999; 88: 164–167.
  Article CAS PubMed Google Scholar
• Middleton FA, Peng L, Lewis DA, Levitt P, Mirnics K . Altered expression of 14-3-3 genes in the prefrontal cortex of subjects with schizophrenia. Neuropsychopharmacology 2005; 30: 974–983.
  Article CAS PubMed Google Scholar
• Hennah W, Tuulio-Henriksson A, Paunio T, Ekelund J, Varilo T, Partonen T et al. A haplotype within the DISC1 gene is associated with visual memory functions in families with a high density of schizophrenia. Mol Psychiatry 2005; 10: 1097–1103.
  Article CAS PubMed Google Scholar
• Thomson PA, Wray NR, Millar JK, Evans KL, Hellard SL, Condie A et al. Association between the TRAX/DISC locus and both bipolar disorder and schizophrenia in the Scottish population. Mol Psychiatry 2005; 10: 657–668, 616.
  Article CAS PubMed Google Scholar
• Goff DC, Coyle JT . The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am J Psychiatry 2001; 158: 1367–1377.
  Article CAS PubMed Google Scholar
• Collier DA, Li T . The genetics of schizophrenia: glutamate not dopamine? Eur J Pharmacol 2003; 480: 177–184.
  Article CAS PubMed Google Scholar
• Zarate Jr CA, Singh J, Manji HK . Cellular plasticity cascades: targets for the development of novel therapeutics for bipolar disorder. Biol Psychiatry 2006; 59: 1006–1020.
  Article CAS PubMed Google Scholar
• Toro C, Deakin JF . NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophr Res 2005; 80: 323–330.
  Article PubMed Google Scholar
• Hall PA, Jung K, Hillan KJ, Russell SE . Expression profiling the human septin gene family. J Pathol 2005; 206: 269–278.
  Article CAS PubMed Google Scholar
• Murphy KC, Jones LA, Owen MJ . High rates of schizophrenia in adults with velo–cardio–facial syndrome. Arch Gen Psychiatry 1999; 56: 940–945.
  Article CAS PubMed Google Scholar
• Weksberg R, Stachon AC, Squire JA, Moldovan L, Bayani J, Meyri S et al. Molecular characterization of deletion breakpoints in adults with 22q11 deletion syndrome. Hum Genet 2007; 120: 837–845.
  Article CAS PubMed Google Scholar
• Tunbridge EM, Weinberger DR, Harrison PJ . A novel protein isoform of catechol _O_-methyltransferase (COMT): brain expression analysis in schizophrenia and bipolar disorder and effect of Val158Met genotype. Mol Psychiatry 2006; 11: 116–117.
  Article CAS PubMed Google Scholar
• Kremer BE, Haystead T, Macara IG . Mammalian septins regulate microtubule stability through interaction with the microtubule-binding protein MAP4. Mol Biol Cell 2005; 16: 4648–4659.
  Article CAS PubMed PubMed Central Google Scholar
• Beites CL, Xie H, Bowser R, Trimble WS . The septin CDCrel-1 binds syntaxin and inhibits exocytosis. Nat Neurosci 1999; 2: 434–439.
  Article CAS PubMed Google Scholar
• Beites CL, Campbell KA, Trimble WS . The septin Sept5/CDCrel-1 competes with alpha-SNAP for binding to the SNARE complex. Biochem J 2005; 385: 347–353.
  Article CAS PubMed PubMed Central Google Scholar
• Kinoshita A, Noda M, Kinoshita M . Differential localization of septins in the mouse brain. J Comp Neurol 2000; 428: 223–239.
  Article CAS PubMed Google Scholar
• Caltagarone J, Rhodes J, Honer WG, Bowser R . Localization of a novel septin protein, hCDCrel-1, in neurons of human brain. NeuroReport 1998; 9: 2907–2912.
  Article CAS PubMed Google Scholar
• Kinoshita A, Kinoshita M, Akiyama H, Tomimoto H, Akiguchi I, Kumar S et al. Identification of septins in neurofibrillary tangles in Alzheimer's disease. Am J Pathol 1998; 153: 1551–1560.
  Article CAS PubMed PubMed Central Google Scholar
• Choi P, Snyder H, Petrucelli L, Theisler C, Chong M, Zhang Y et al. SEPT5_v2 is a parkin-binding protein. Brain Res Mol Brain Res 2003; 117: 179–189.
  Article CAS PubMed Google Scholar
• Whatley SA, Curti D, Das GF, Ferrier IN, Jones S, Taylor C et al. Superoxide, neuroleptics and the ubiquinone and cytochrome b5 reductases in brain and lymphocytes from normals and schizophrenic patients. Mol Psychiatry 1998; 3: 227–237.
  Article CAS PubMed Google Scholar
• Prince JA, Blennow K, Gottfries CG, Karlsson I, Oreland L . Mitochondrial function is differentially altered in the basal ganglia of chronic schizophrenics. Neuropsychopharmacology 1999; 21: 372–379.
  Article CAS PubMed Google Scholar
• Maurer I, Zierz S, Moller H . Evidence for a mitochondrial oxidative phosphorylation defect in brains from patients with schizophrenia. Schizophr Res 2001; 48: 125–136.
  Article CAS PubMed Google Scholar
• Marchbanks RM, Ryan M, Day IN, Owen M, McGuffin P, Whatley SA . A mitochondrial DNA sequence variant associated with schizophrenia and oxidative stress. Schizophr Res 2003; 65: 33–38.
  Article CAS PubMed Google Scholar
• Kato T, Kato N . Mitochondrial dysfunction in bipolar disorder. Bipolar Disord 2000; 2: 180–190.
  Article CAS PubMed Google Scholar
• Mah L, Zarate Jr CA, Singh J, Duan YF, Luckenbaugh DA, Manji HK et al. Regional cerebral glucose metabolic abnormalities in bipolar II depression. Biol Psychiatry 2007; 61: 765–775.
  Article CAS PubMed Google Scholar
• Sun X, Wang JF, Tseng M, Young LT . Downregulation in components of the mitochondrial electron transport chain in the postmortem frontal cortex of subjects with bipolar disorder. J Psychiatry Neurosci 2006; 31: 189–196.
  PubMed PubMed Central Google Scholar
• Bezchlibnyk YB, Wang JF, McQueen GM, Young LT . Gene expression differences in bipolar disorder revealed by cDNA array analysis of post-mortem frontal cortex. J Neurochem 2001; 79: 826–834.
  Article CAS PubMed Google Scholar
• Iwamoto K, Bundo M, Kato T . Altered expression of mitochondria-related genes in postmortem brains of patients with bipolar disorder or schizophrenia, as revealed by large-scale DNA microarray analysis. Hum Mol Genet 2005; 14: 241–253.
  Article CAS PubMed Google Scholar
• Ryan MM, Lockstone HE, Huffaker SJ, Wayland MT, Webster MJ, Bahn S . Gene expression analysis of bipolar disorder reveals downregulation of the ubiquitin cycle and alterations in synaptic genes. Mol Psychiatry 2006; 11: 965–978.
  Article CAS PubMed Google Scholar
• Higgs BW, Elashoff M, Richman S, Barci B . An online database for brain disease research. BMC Genomics 2006; 7: 70.
  Article PubMed PubMed Central CAS Google Scholar
• Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, Yolken RH . Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun 2001; 15: 388–400.
  Article CAS PubMed Google Scholar
• Toro CT, Hallak JE, Dunham JS, Deakin JF . Glial fibrillary acidic protein and glutamine synthetase in subregions of prefrontal cortex in schizophrenia and mood disorder. Neurosci Lett 2006; 404: 276–281.
  Article CAS PubMed Google Scholar
• Inagaki M, Gonda Y, Nishizawa K, Kitamura S, Sato C, Ando S et al. Phosphorylation sites linked to glial filament disassembly in vitro locate in a non-alpha-helical head domain. J Biol Chem 1990; 265: 4722–4729.
  CAS PubMed Google Scholar