Proteomic analysis of membrane microdomain-associated proteins in the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder reveals alterations in LAMP, STXBP1 and BASP1 protein expression - Molecular Psychiatry (original) (raw)

• Guidotti A, Auta J, Davis JM, Dong E, Grayson DR, Veldic M et al. GABAergic dysfunction in schizophrenia: new treatment strategies on the horizon. Psychopharmacology (Berl) 2005; 180: 191–205.
  Article CAS Google Scholar
• Beneyto M, Kristiansen LV, Oni-Orisan A, McCullumsmith RE, Meador-Woodruff JH . Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 2007; 32: 1888–1902.
  Article CAS PubMed Google Scholar
• Beneyto M, Meador-Woodruff JH . Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia. Synapse 2006; 60: 585–598.
  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
• 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
• Harrison PJ, Weinberger DR . Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005; 10: 40–68; image 5.
  Article CAS PubMed Google Scholar
• Brambilla P, Glahn DC, Balestrieri M, Soares JC . Magnetic resonance findings in bipolar disorder. Psychiatr Clin North Am 2005; 28: 443–467.
  Article PubMed Google Scholar
• Rajkowska G, Halaris A, Selemon LD . Reductions in neuronal and glial density characterize the dorsolateral prefrontal cortex in bipolar disorder. Biol Psychiatry 2001; 49: 741–752.
  Article CAS PubMed Google Scholar
• Rajkowska G, Miguel-Hidalgo JJ, Makkos Z, Meltzer H, Overholser J, Stockmeier C . Layer-specific reductions in GFAP-reactive astroglia in the dorsolateral prefrontal cortex in schizophrenia. Schizophr Res 2002; 57: 127–138.
  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
• 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
• Lewis DA, Hashimoto T . Deciphering the disease process of schizophrenia: the contribution of cortical gaba neurons. Int Rev Neurobiol 2007; 78: 109–131.
  Article CAS PubMed Google Scholar
• Lewis DA, Moghaddam B . Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 2006; 63: 1372–1376.
  Article 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
• Clark D, Dedova I, Cordwell S, Matsumoto I . A proteome analysis of the anterior cingulate cortex gray matter in schizophrenia. Mol Psychiatry 2006; 11: 423, 459–470.
  Article 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: 643, 684–697.
  Article Google Scholar
• Pennington K, Beasley CL, Dicker P, Fagan A, English J, Pariante CM et al. Prominent synaptic and metabolic abnormalities revealed by proteomic analysis of the dorsolateral prefrontal cortex in schizophrenia and bipolar disorder. Mol Psychiatry 2007; Oct 16 e-pub ahead of print.
• Dean B, Opeskin K, Pavey G, Hill C, Keks N . Changes in protein kinase C and adenylate cyclase in the temporal lobe from subjects with schizophrenia. J Neural Transm 1997; 104: 1371–1381.
  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
• Opeskin K, Dean B, Pavey G, Hill C, Keks N, Copolov D . Neither protein kinase C nor adenylate cyclase are altered in the striatum from subjects with schizophrenia. Schizophr Res 1996; 22: 159–164.
  Article CAS PubMed Google Scholar
• Pennington K, Cotter D, Dunn MJ . The role of proteomics in investigating psychiatric disorders. Br J Psychiatry 2005; 187: 4–6.
  Article CAS PubMed Google Scholar
• Allen JA, Halverson-Tamboli RA, Rasenick MM . Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 2007; 8: 128–140.
  Article CAS PubMed Google Scholar
• Gil C, Soler-Jover A, Blasi J, Aguilera J . Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes. Biochem Biophys Res Commun 2005; 329: 117–124.
  Article CAS PubMed Google Scholar
• Li N, Mak A, Richards DP, Naber C, Keller BO, Li L et al. Monocyte lipid rafts contain proteins implicated in vesicular trafficking and phagosome formation. Proteomics 2003; 3: 536–548.
  Article CAS PubMed Google Scholar
• Bini L, Pacini S, Liberatori S, Valensin S, Pellegrini M, Raggiaschi R et al. Extensive temporally regulated reorganization of the lipid raft proteome following T-cell antigen receptor triggering. Biochem J 2003; 369: 301–309.
  Article CAS PubMed PubMed Central Google Scholar
• Foster LJ, De Hoog CL, Mann M . Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci USA 2003; 100: 5813–5818.
  Article CAS PubMed PubMed Central Google Scholar
• Nebl T, Pestonjamasp KN, Leszyk JD, Crowley JL, Oh SW, Luna EJ . Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes. J Biol Chem 2002; 277: 43399–43409.
  Article CAS PubMed Google Scholar
• Blonder J, Hale ML, Lucas DA, Schaefer CF, Yu LR, Conrads TP et al. Proteomic analysis of detergent-resistant membrane rafts. Electrophoresis 2004; 25: 1307–1318.
  Article CAS PubMed Google Scholar
• Jia J, Lamer S, Schüemann M, Schmidt M, Krause E, Haucke V . Quantitative proteomic analysis of detergent-resistant membranes from chemical synapses: evidence for cholesterol as spatial organizer of synaptic vesicle cycling. Mol Cell Proteomics 2006; 5: 2060–2071.
  Article CAS PubMed Google Scholar
• Martosella J, Zolotarjova N, Liu H, Moyer SC, Perkins PD, Boyes BE . High recovery HPLC separation of lipid rafts for membrane proteome analysis. J Proteome Res 2006; 5: 1301–1312.
  Article CAS PubMed Google Scholar
• Parkin ET, Hussain I, Karran EH, Turner AJ, Hooper NM . Characterization of detergent-insoluble complexes containing the familial Alzheimer's disease-associated presenilins. J Neurochem 1999; 72: 1534–1543.
  Article CAS PubMed Google Scholar
• Jiang L, He L, Fountoulakis M . Comparison of protein precipitation methods for sample preparation prior to proteomic analysis. J Chromatogr A 2004; 1023: 317–320.
  Article CAS PubMed Google Scholar
• Maguire PB, Wynne KJ, Harney DF, O’Donoghue NM, Stephens G, Fitzgerald DJ . Identification of the phosphotyrosine proteome from thrombin activated platelets. Proteomics 2002; 2: 642–648.
  Article CAS PubMed Google Scholar
• Behan A, Doyle S, Farrell M . Adaptive responses to mitochondrial dysfunction in the rho degrees Namalwa cell. Mitochondrion 2005; 5: 173–193.
  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
• Focking M, Boersema PJ, O’Donoghue N, Lubec G, Pennington SR, Cotter DR et al. 2-D DIGE as a quantitative tool for investigating the HUPO Brain Proteome Project mouse series. Proteomics 2006; 6: 4914–4931.
  Article CAS PubMed Google Scholar
• Beasley CL, Honer WG, Bergmann K, Falkai P, Lütjohann 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
• 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
• Shevchenko A, Wilm M, Vorm O, Mann M . Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996; 68: 850–858.
  Article CAS PubMed Google Scholar
• Coppinger JA, Cagney G, Toomey S, Kislinger T, Belton O, McRedmond JP et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood 2004; 103: 2096–2104.
  Article CAS PubMed Google Scholar
• Nesvizhskii AI, Keller A, Kolker E, Aebersold R . A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003; 75: 4646–4658.
  Article CAS PubMed Google Scholar
• Kokubo H, Helms JB, Ohno-Iwashita Y, Shimada Y, Horikoshi Y, Yamaguchi H . Ultrastructural localization of flotillin-1 to cholesterol-rich membrane microdomains, rafts, in rat brain tissue. Brain Res 2003; 965: 83–90.
  Article CAS PubMed Google Scholar
• Slaughter N, Laux I, Tu X, Whitelegge J, Zhu X, Effros R et al. The flotillins are integral membrane proteins in lipid rafts that contain TCR-associated signaling components: implications for T-cell activation. Clin Immunol 2003; 108: 138–151.
  Article CAS PubMed Google Scholar
• Harder T, Scheiffele P, Verkade P, Simons K . Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 1998; 141: 929–942.
  Article CAS PubMed PubMed Central Google Scholar
• Khan TK, Yang B, Thompson NL, Maekawa S, Epand RM, Jacobson K . Binding of NAP-22, a calmodulin-binding neuronal protein, to raft-like domains in model membranes. Biochemistry 2003; 42: 4780–4786.
  Article CAS PubMed Google Scholar
• Gil C, Cubi R, Blasi J, Aguilera J . Synaptic proteins associate with a sub-set of lipid rafts when isolated from nerve endings at physiological temperature. Biochem Biophys Res Commun 2006; 348: 1334–1342.
  Article CAS PubMed Google Scholar
• Funatsu N, Miyata S, Kumanogoh H, Shigeta M, Hamada K, Endo Y et al. Characterization of a novel rat brain glycosylphosphatidylinositol-anchored protein (Kilon), a member of the IgLON cell adhesion molecule family. J Biol Chem 1999; 274: 8224–8230.
  Article CAS PubMed Google Scholar
• Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M . Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 2002; 157: 521–532.
  Article CAS PubMed PubMed Central Google Scholar
• Kim KB, Lee JW, Lee CS, Kim BW, Choo HJ, Jung SY et al. Oxidation–reduction respiratory chains and ATP synthase complex are localized in detergent-resistant lipid rafts. Proteomics 2006; 6: 2444–2453.
  Article CAS PubMed Google Scholar
• Raimondo F, Ceppi P, Guidi K, Masserini M, Foletti C, Pitto M . Proteomics of plasma membrane microdomains. Expert Rev Proteomics 2005; 2: 793–807.
  Article CAS PubMed Google Scholar
• Behan ÁT, Wynne M, Clarke K, Sullivan MM, Cotter DM, Maguire PM . Analysis of membrane microdomain-associated proteins in the insular cortex of post-mortem human brain. Proteomics Clin Appl 2007; 1: 1324–1331.
  Article CAS PubMed Google Scholar
• Quinton TM, Kim S, Jin J, Kunapuli SP . Lipid rafts are required in Galpha(i) signaling downstream of the P2Y12 receptor during ADP-mediated platelet activation. J Thromb Haemost 2005; 3: 1036–1041.
  Article CAS PubMed Google Scholar
• Yang B, Steegmaier M, Gonzalez Jr LC, Scheller RH . nSec1 binds a closed conformation of syntaxin1A. J Cell Biol 2000; 148: 247–252.
  Article CAS PubMed PubMed Central Google Scholar
• Mitchell SJ, Ryan TA . Munc18-dependent regulation of synaptic vesicle exocytosis by syntaxin-1A in hippocampal neurons. Neuropharmacology 2005; 48: 372–380.
  Article CAS PubMed Google Scholar
• Rickman C, Medine CN, Bergmann A, Duncan RR . Functionally and spatially distinct modes of munc18-syntaxin 1 interaction. J Biol Chem 2007; 282: 12097–12103.
  Article CAS PubMed Google Scholar
• Sokolov BP, Tcherepanov AA, Haroutunian V, Davis KL . Levels of mRNAs encoding synaptic vesicle and synaptic plasma membrane proteins in the temporal cortex of elderly schizophrenic patients. Biol Psychiatry 2000; 48: 184–196.
  Article CAS PubMed Google Scholar
• Gabriel SM, Haroutunian V, Powchik P, Honer WG, Davidson M, Davies P et al. Increased concentrations of presynaptic proteins in the cingulate cortex of subjects with schizophrenia. Arch Gen Psychiatry 1997; 54: 559–566.
  Article CAS PubMed Google Scholar
• Honer WG, Falkai P, Young C, Wang T, Xie J, Bonner J et al. Cingulate cortex synaptic terminal proteins and neural cell adhesion molecule in schizophrenia. Neuroscience 1997; 78: 99–110.
  Article CAS PubMed Google Scholar
• Halim ND, Weickert CS, McClintock BW, Hyde TM, Weinberger DR, Kleinman JE et al. Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development. Mol Psychiatry 2003; 8: 797–810.
  Article CAS PubMed Google Scholar
• Honer WG, Falkai P, Bayer TA, Xie J, Hu L, Li HY et al. Abnormalities of SNARE mechanism proteins in anterior frontal cortex in severe mental illness. Cereb Cortex 2002; 12: 349–356.
  Article PubMed Google Scholar
• Mukaetova-Ladinska EB, Hurt J, Honer WG, Harrington CR, Wischik CM . Loss of synaptic but not cytoskeletal proteins in the cerebellum of chronic schizophrenics. Neurosci Lett 2002; 317: 161–165.
  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
• Maekawa S, Iino S, Miyata S . Molecular characterization of the detergent-insoluble cholesterol-rich membrane microdomain (raft) of the central nervous system. Biochim Biophys Acta 2003; 1610: 261–270.
  Article CAS PubMed Google Scholar
• Frey D, Laux T, Xu L, Schneider C, Caroni P . Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J Cell Biol 2000; 149: 1443–1454.
  Article CAS PubMed PubMed Central 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
• Weickert CS, Webster MJ, Hyde TM, Herman MM, Bachus SE, Bali G et al. Reduced GAP-43 mRNA in dorsolateral prefrontal cortex of patients with schizophrenia. Cereb Cortex 2001; 11: 136–147.
  Article CAS PubMed Google Scholar
• Eastwood SL, Harrison PJ . Hippocampal and cortical growth-associated protein-43 messenger RNA in schizophrenia. Neuroscience 1998; 86: 437–448.
  Article CAS PubMed Google Scholar
• Horton HL, Levitt P . A unique membrane protein is expressed on early developing limbic system axons and cortical targets. J Neurosci 1988; 8: 4653–4661.
  Article CAS PubMed PubMed Central Google Scholar
• Zacco A, Cooper V, Chantler PD, Fisher-Hyland S, Horton HL, Levitt P . Isolation, biochemical characterization and ultrastructural analysis of the limbic system-associated membrane protein (LAMP), a protein expressed by neurons comprising functional neural circuits. J Neurosci 1990; 10: 73–90.
  Article CAS PubMed PubMed Central Google Scholar
• Pimenta AF, Levitt P . Characterization of the genomic structure of the mouse limbic system-associated membrane protein (Lsamp) gene. Genomics 2004; 83: 790–801.
  Article CAS PubMed Google Scholar
• Harrison PJ . The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999; 122 (Part 4): 593–624.
  Article 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
• Steiner P, Sarria JC, Huni B, Marsault R, Catsicas S, Hirling H . Overexpression of neuronal Sec1 enhances axonal branching in hippocampal neurons. Neuroscience 2002; 113: 893–905.
  Article CAS PubMed Google Scholar
• Bellon A . New genes associated with schizophrenia in neurite formation: a review of cell culture experiments. Mol Psychiatry 2007; 12: 620–629.
  Article CAS PubMed Google Scholar
• Shirasu M, Kimura K, Kataoka M, Takahashi M, Okajima S, Kawaguchi S et al. VAMP-2 promotes neurite elongation and SNAP-25A increases neurite sprouting in PC12 cells. Neurosci Res 2000; 37: 265–275.
  Article CAS PubMed Google Scholar
• Knable MB, Barci BM, Bartko JJ, Webster MJ, Torrey EF . Molecular abnormalities in the major psychiatric illnesses: classification and regression tree (CRT) analysis of post-mortem prefrontal markers. Mol Psychiatry 2002; 7: 392–404.
  Article CAS PubMed Google Scholar
• McCullumsmith RE, Kristiansen LV, Beneyto M, Scarr E, Dean B, Meador-Woodruff JH . Decreased NR1, NR2A, and SAP102 transcript expression in the hippocampus in bipolar disorder. Brain Res 2007; 1127: 108–118.
  Article CAS PubMed Google Scholar
• Blennow K, Bogdanovic N, Gottfries CG, Davidsson P . The growth-associated protein GAP-43 is increased in the hippocampus and in the gyrus cinguli in schizophrenia. J Mol Neurosci 1999; 13: 101–109.
  Article CAS PubMed Google Scholar
• Perrone-Bizzozero NI et al. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci USA 1996; 93: 14182–14187.
  Article CAS PubMed PubMed Central Google Scholar
• Sower AC, Bird ED, Perrone-Bizzozero NI . Increased levels of GAP-43 protein in schizophrenic brain tissues demonstrated by a novel immunodetection method. Mol Chem Neuropathol 1995; 24: 1–11.
  Article CAS PubMed Google Scholar
• Scarr E, Gray L, Keriakous D, Robinson PJ, Dean B . Increased levels of SNAP-25 and synaptophysin in the dorsolateral prefrontal cortex in bipolar I disorder. Bipolar Disord 2006; 8: 133–143.
  Article CAS PubMed Google Scholar
• Chambers JS, Thomas D, Saland L, Neve RL, Perrone-Bizzozero NI . Growth-associated protein 43 (GAP-43) and synaptophysin alterations in the dentate gyrus of patients with schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 283–290.
  Article CAS PubMed Google Scholar
• Vawter MP . Dysregulation of the neural cell adhesion molecule and neuropsychiatric disorders. Eur J Pharmacol 2000; 405: 385–395.
  Article CAS PubMed Google Scholar
• Barr AM, Young CE, Phillips AG, Honer WG . Selective effects of typical antipsychotic drugs on SNAP-25 and synaptophysin in the hippocampal trisynaptic pathway. Int J Neuropsychopharmacol 2006; 9: 457–463.
  Article CAS PubMed Google Scholar
• Eastwood SL, Heffernan J, Harrison PJ . Chronic haloperidol treatment differentially affects the expression of synaptic and neuronal plasticity-associated genes. Mol Psychiatry 1997; 2: 322–329.
  Article CAS PubMed Google Scholar