Lack of change in markers of presynaptic terminal abundance alongside subtle reductions in markers of presynaptic terminal plasticity in prefrontal cortex of schizophrenia patients

Biological Psychiatry

Volumn 69, Issue 1, 2011, Pages 71-79

  Fung, Samantha J ^a   Sivagnanasundaram, Sinthuja ^a   Weickert, Cynthia Shannon ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Complexin; Dorsolateral prefrontal cortex; GAP43; Neuronal navigator; Schizophrenia; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID CARRIER; COMPLEXIN 1; COMPLEXIN 2; DYSBINDIN; MESSENGER RNA; NERVE PROTEIN; NEUROMODULIN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER;

AMNESIA; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOSKELETON; GENERAL PATHOLOGY; GENETIC POLYMORPHISM; HUMAN; HUMAN TISSUE; HYPOTHESIS; MENTAL PATIENT; NERVE CELL PLASTICITY; NERVE ENDING; NERVE FIBER GROWTH; NEUROPATHOLOGY; PREFRONTAL CORTEX; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHIZOPHRENIA; SYMPTOM; WORKING MEMORY;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; BIOLOGICAL MARKERS; CARRIER PROTEINS; GAP-43 PROTEIN; GENE EXPRESSION; HUMANS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; POLYMORPHISM, SINGLE NUCLEOTIDE; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; SCHIZOPHRENIA; VESICLE-ASSOCIATED MEMBRANE PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 78649990335     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2010.09.036     Document Type: Article

References (72)

1. P.J. Harrison, and D.R. Weinberger Schizophrenia genes, gene expression, and neuropathology: On the matter of their convergence Mol Psychiatry 10 2005 40 68
2. T.H. McGlashan, and R.E. Hoffman Schizophrenia as a disorder of developmentally reduced synaptic connectivity Arch Gen Psychiatry 57 2000 637 648
3. K. Mirnics, F.A. Middleton, D.A. Lewis, and P. Levitt Analysis of complex brain disorders with gene expression microarrays: Schizophrenia as a disease of the synapse Trends Neurosci 24 2001 479 486
4. K. Mirnics, F.A. Middleton, A. Marquez, D.A. Lewis, and P. Levitt Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex Neuron 28 2000 53 67
5. J.M. Goldstein, J.M. Goodman, L.J. Seidman, D.N. Kennedy, N. Makris, and H. Lee Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging Arch Gen Psychiatry 56 1999 537 547
6. M. Sanfilipo, T. Lafargue, H. Rusinek, L. Arena, C. Loneragan, and A. Lautin Volumetric measure of the frontal and temporal lobe regions in schizophrenia: Relationship to negative symptoms Arch Gen Psychiatry 57 2000 471 480
7. L.D. Selemon, G. Rajkowska, and P.S. Goldman-Rakic Abnormally high neuronal density in the schizophrenic cortex A morphometric analysis of prefrontal area 9 and occipital area. 17 Arch Gen Psychiatry 52 1995 805 818 discussion 819820
8. L.D. Selemon, G. Rajkowska, and P.S. Goldman-Rakic Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: Application of a three-dimensional, stereologic counting method J Comp Neurol 392 1998 402 412
9. L.D. Selemon, and P.S. Goldman-Rakic The reduced neuropil hypothesis: A circuit based model of schizophrenia Biol Psychiatry 45 1999 17 25
10. E. Masliah, R.D. Terry, M. Alford, and R. DeTeresa Quantitative immunohistochemistry of synaptophysin in human neocortex: An alternative method to estimate density of presynaptic terminals in paraffin sections J Histochem Cytochem 38 1990 837 844
11. S.L. Eastwood, P.W. Burnet, B. McDonald, J. Clinton, and P.J. Harrison Synaptophysin gene expression in human brain: A quantitative in situ hybridization and immunocytochemical study Neuroscience 59 1994 881 892
12. S.L. Eastwood, P.W. Burnet, and P.J. Harrison Altered synaptophysin expression as a marker of synaptic pathology in schizophrenia Neuroscience 66 1995 309 319
13. S.L. Eastwood, N.J. Cairns, and P.J. Harrison Synaptophysin gene expression in schizophrenia Investigation of synaptic pathology in the cerebral cortex Br J Psychiatry 176 2000 236 242
14. L.A. Glantz, M.C. Austin, and D.A. Lewis Normal cellular levels of synaptophysin mRNA expression in the prefrontal cortex of subjects with schizophrenia Biol Psychiatry 48 2000 389 397
15. L.J. Gray, B. Dean, H.C. Kronsbein, P.J. Robinson, and E. Scarr Region and diagnosis-specific changes in synaptic proteins in schizophrenia and bipolar I disorder Psychiatry Res 178 2010 374 380
16. N.D. Halim, C.S. Weickert, B.W. McClintock, T.M. Hyde, D.R. Weinberger, J.E. Kleinman, and B.K. Lipska Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development Mol Psychiatry 8 2003 797 810
17. W.G. Honer, P. Falkai, C. Chen, V. Arango, J.J. Mann, and A.J. Dwork Synaptic and plasticity-associated proteins in anterior frontal cortex in severe mental illness Neuroscience 91 1999 1247 1255
18. C.N. Karson, R.E. Mrak, K.O. Schluterman, W.Q. Sturner, J.G. Sheng, and W.S. Griffin Alterations in synaptic proteins and their encoding mRNAs in prefrontal cortex in schizophrenia: A possible neurochemical basis for "hypofrontality" Mol Psychiatry 4 1999 39 45
19. E. Scarr, L. Gray, D. Keriakous, P.J. Robinson, and B. Dean Increased levels of SNAP-25 and synaptophysin in the dorsolateral prefrontal cortex in bipolar I disorder Bipolar Disord 8 2006 133 143
20. C.S. Weickert, R.E. Straub, B.W. McClintock, M. Matsumoto, R. Hashimoto, and T.M. Hyde Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain Arch Gen Psychiatry 61 2004 544 555
21. L.A. Glantz, and D.A. Lewis Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia Regional and diagnostic specificity Arch Gen Psychiatry 54 1997 943 952
22. N.I. Perrone-Bizzozero, A.C. Sower, E.D. Bird, L.I. Benowitz, K.J. Ivins, and R.L. Neve Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia Proc Natl Acad Sci U S A 93 1996 14182 14187
23. C. Duncan, M. Webster, D. Rothmond, S. Bahn, M. Elashoff, and C. Shannon Weickert Prefrontal GABA(A) receptor alpha subunit expression in normal postnatal human development and schizophrenia J Psychiatr Res 44 2010 673 681
24. T. Hashimoto, D.W. Volk, S.M. Eggan, K. Mirnics, J.N. Pierri, and Z. Sun Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia J Neurosci 23 2003 6315 6326
25. D.A. Lewis, D.A. Cruz, D.S. Melchitzky, and J.N. Pierri Lamina-specific deficits in parvalbumin-immunoreactive varicosities in the prefrontal cortex of subjects with schizophrenia: Evidence for fewer projections from the thalamus Am J Psychiatry 158 2001 1411 1422
26. J.N. Pierri, A.S. Chaudry, T.U. Woo, and D.A. Lewis Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects Am J Psychiatry 156 1999 1709 1719
27. D. Volk, M. Austin, J. Pierri, A. Sampson, and D. Lewis GABA transporter-1 mRNA in the prefrontal cortex in schizophrenia: Decreased expression in a subset of neurons Am J Psychiatry 158 2001 256 265
28. D.W. Volk, M.C. Austin, J.N. Pierri, A.R. Sampson, and D.A. Lewis 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 2000 237 245
29. Fung S, Webster M, Sivagnanasundaram S, Duncan C, Elashoff M, Shannon Weickert C (in press): Expression of interneuron markers in the dorsolateral prefrontal cortex of the developing human and in schizophrenia. Am J Psychiatry.
30. K. Sawada, C.E. Young, A.M. Barr, K. Longworth, S. Takahashi, and V. Arango Altered immunoreactivity of complexin protein in prefrontal cortex in severe mental illness Mol Psychiatry 7 2002 484 492
31. S.L. Eastwood, and P.J. Harrison Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: Further evidence for a synaptic pathology affecting glutamate neurons Schizophr Res 73 2005 159 172
32. L.A. Glantz, and D.A. Lewis Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia Arch Gen Psychiatry 57 2000 65 73
33. L.J. Garey, W.Y. Ong, T.S. Patel, M. Kanani, A. Davis, and A.M. Mortimer Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia J Neurol Neurosurg Psychiatry 65 1998 446 453
34. C.S. Weickert, M.J. Webster, T.M. Hyde, M.M. Herman, S.E. Bachus, and G. Bali Reduced GAP-43 mRNA in dorsolateral prefrontal cortex of patients with schizophrenia Cereb Cortex 11 2001 136 147
35. J.S. Chambers, D. Thomas, L. Saland, R.L. Neve, and N.I. Perrone-Bizzozero Growth-associated protein 43 (GAP-43) and synaptophysin alterations in the dentate gyrus of patients with schizophrenia Prog Neuropsychopharmacol Biol Psychiatry 29 2005 283 290
36. S.L. Eastwood, and P.J. Harrison Hippocampal and cortical growth-associated protein-43 messenger RNA in schizophrenia Neuroscience 86 1998 437 448
37. S.Y. Tian, J.F. Wang, Y.B. Bezchlibnyk, and L.T. Young Immunoreactivity of 43 kDa growth-associated protein is decreased in post mortem hippocampus of bipolar disorder and schizophrenia Neurosci Lett 411 2007 123 127
38. M.J. Webster, C. Shannon Weickert, M.M. Herman, T.M. Hyde, and J.E. Kleinman Synaptophysin and GAP-43 mRNA levels in the hippocampus of subjects with schizophrenia Schizophr Res 49 2001 89 98
39. K. Blennow, N. Bogdanovic, C.G. Gottfries, and P. Davidsson The growth-associated protein GAP-43 is increased in the hippocampus and in the gyrus cinguli in schizophrenia J Mol Neurosci 13 1999 101 109
40. A.C. Sower, E.D. Bird, and N.I. Perrone-Bizzozero Increased levels of GAP-43 protein in schizophrenic brain tissues demonstrated by a novel immunodetection method Mol Chem Neuropathol 24 1995 1 11
41. C.S. Weickert, D. Sheedy, D.A. Rothmond, I. Dedova, S. Fung, and T. Garrick Selection of reference gene expression in a schizophrenia brain cohort Aust N Z J Psychiatry 44 2010 59 70
42. A.Y. Guo, J. Sun, B.P. Riley, D.L. Thiselton, K.S. Kendler, and Z. Zhao The dystrobrevin-binding protein 1 gene: Features and networks Mol Psychiatry 14 2009 18 29
43. C.S. Weickert, D.A. Rothmond, T.M. Hyde, J.E. Kleinman, and R.E. Straub Reduced DTNBP1 (dysbindin-1) mRNA in the hippocampal formation of schizophrenia patients Schizophr Res 98 2008 105 110
44. N.J. Bray, A. Preece, N.M. Williams, V. Moskvina, P.R. Buckland, M.J. Owen, and M.C. O'Donovan Haplotypes at the dystrobrevin binding protein 1 (DTNBP1) gene locus mediate risk for schizophrenia through reduced DTNBP1 expression Hum Mol Genet 14 2005 1947 1954
45. K. Talbot, W.L. Eidem, C.L. Tinsley, M.A. Benson, E.W. Thompson, and R.J. Smith Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia J Clin Invest 113 2004 1353 1363
46. G. Rajkowska, and P.S. Goldman-Rakic Cytoarchitectonic definition of prefrontal areas in the normal human cortex I. Remapping of areas 9 and 46 using quantitative criteria Cereb Cortex 5 1995 307 322
47. Y. Yang, S. Fung, A. Rothwell, S. Tianmei, and C. Shannon Weickert Increased interstitial white matter neuron density in the DLPFC of people with schizophrenia [published online ahead of print October 23] Biol Psychiatry 2010
48. F.E. McGuigan, and S.H. Ralston Single nucleotide polymorphism detection: Allelic discrimination using TaqMan Psychiatr Genet 12 2002 133 136
49. L. Bragina, S. Giovedi, P. Barbaresi, F. Benfenati, and F. Conti Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex: Analysis of synaptogyrin, vesicle-associated membrane protein, and syntaxin Neuroscience 165 2010 934 943
50. M.R. Bennett Synapse formation and regression in the cortex during adolescence and in schizophrenia Med J Aust 190 2009 S14 S16
51. A. Hayashi-Takagi, and A. Sawa Disturbed synaptic connectivity in schizophrenia: Convergence of genetic risk factors during neurodevelopment Brain Res Bull 83 2010 140 146
52. M.S. Keshavan, S. Anderson, and J.W. Pettegrew Is schizophrenia due to excessive synaptic pruning in the prefrontal cortex? The Feinberg hypothesis revisited J Psychiatr Res 28 1994 239 265
53. I. Feinberg Schizophrenia: Caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17 1982 319 334
54. N. Brose Altered complexin expression in psychiatric and neurological disorders: Cause or consequence? Mol Cells 25 2008 7 19
55. S.L. Eastwood, P.W. Burnet, and P.J. Harrison Expression of complexin I and II mRNAs and their regulation by antipsychotic drugs in the rat forebrain Synapse 36 2000 167 177
56. P.J. Harrison, and S.L. Eastwood Preferential involvement of excitatory neurons in medial temporal lobe in schizophrenia Lancet 352 1998 1669 1673
57. S. Takahashi, H. Yamamoto, Z. Matsuda, M. Ogawa, K. Yagyu, and T. Taniguchi Identification of two highly homologous presynaptic proteins distinctly localized at the dendritic and somatic synapses FEBS Lett 368 1995 455 460
58. S.L. Eastwood, and P.J. Harrison Hippocampal synaptic pathology in schizophrenia, bipolar disorder and major depression: A study of complexin mRNAs Mol Psychiatry 5 2000 425 432
59. S.L. Eastwood, and P.J. Harrison 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 complexions Brain Res Bull 55 2001 569 578
60. K. Reim, M. Mansour, F. Varoqueaux, H.T. McMahon, T.C. Sudhof, and N. Brose Complexions regulate a late step in Ca2+-dependent neurotransmitter release Cell 104 2001 71 81
61. K. Sawada, A.M. Barr, M. Nakamura, K. Arima, C.E. Young, and A.J. Dwork Hippocampal complexin proteins and cognitive dysfunction in schizophrenia Arch Gen Psychiatry 62 2005 263 272
62. K.L. Schmidt, N. Marcus-Gueret, A. Adeleye, J. Webber, D. Baillie, and E.G. Stringham The cell migration molecule UNC-53/NAV2 is linked to the ARP2/3 complex by ABI-1 Development 136 2009 563 574
63. B. Dean, D. Keriakous, E. Scarr, and E.A. Thomas Gene expression profiling in Brodmann's area 46 from subjects with schizophrenia Aust N Z J Psychiatry 41 2007 308 320
64. M. Gronborg, N.J. Pavlos, I. Brunk, J.J. Chua, A. Munster-Wandowski, and D. Riedel Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein J Neurosci 30 2010 2 12
65. J.B. Denny Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43 Curr Neuropharmacol 4 2006 293 304
66. M.J. Martinez-Lopez, S. Alcantara, C. Mascaro, F. Perez-Branguli, P. Ruiz-Lozano, and T. Maes Mouse neuron navigator 1, a novel microtubule- associated protein involved in neuronal migration Mol Cell Neurosci 28 2005 599 612
67. T. Maes, A. Barcelo, and C. Buesa Neuron navigator: A human gene family with homology to unc-53, a cell guidance gene from Caenorhabditis elegans Genomics 80 2002 21 30
68. J. van Haren, K. Draegestein, N. Keijzer, J.P. Abrahams, F. Grosveld, and P.J. Peeters Mammalian navigators are microtubule plus-end tracking proteins that can reorganize the cytoskeleton to induce neurite-like extensions Cell Motil Cytoskeleton 66 2009 824 838
69. P.D. Muley, E.M. McNeill, M.A. Marzinke, K.M. Knobel, M.M. Barr, and M. Clagett-Dame The atRA-responsive gene neuron navigator 2 functions in neurite outgrowth and axonal elongation Dev Neurobiol 68 2008 1441 1453
70. R.A. Merrill, L.A. Plum, M.E. Kaiser, and M. Clagett-Dame A mammalian homolog of unc-53 is regulated by all-trans retinoic acid in neuroblastoma cells and embryos Proc Natl Acad Sci U S A 99 2002 3422 3427
71. D.K. Dickman, and G.W. Davis The schizophrenia susceptibility gene dysbindin controls synaptic homeostasis Science 326 2009 1127 1130
72. T.T. Tang, F. Yang, B.S. Chen, Y. Lu, Y. Ji, K.W. Roche, and B. Lu Dysbindin regulates hippocampal LTP by controlling NMDA receptor surface expression Proc Natl Acad Sci U S A 106 2009 21395 21400