Presynaptic proteins in the prefrontal cortex of patients with schizophrenia and rats with abnormal prefrontal development

Molecular Psychiatry

Volumn 8, Issue 9, 2003, Pages 797-810

  Halim, N D ^a   Weickert, C S ^a   McClintock, B W ^a   Hyde, T M ^a   Weinberger, D R ^a   Kleinman, J E ^a   Lipska, B K ^a,b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b Bldg 10 ^*  (United States)

Author keywords

Animal model; GAP 43; Hippocampus; SNAP 25; Synaptobrevin; Synaptophysin; Syntaxin; VAMP

Indexed keywords

BRAIN PROTEIN; NEUROMODULIN; SYNAPTOBREVIN; SYNAPTOPHYSIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

ADULT; AGED; ANALYSIS OF VARIANCE; ANIMAL TISSUE; ARTICLE; AUTOPSY; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOREACTIVITY; MALE; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; PREFRONTAL CORTEX; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; RAT; SCHIZOPHRENIA; TISSUE DISTRIBUTION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BIOLOGICAL MARKERS; CARRIER PROTEINS; CASE-CONTROL STUDIES; DISEASE MODELS, ANIMAL; FEMALE; GAP-43 PROTEIN; HIPPOCAMPUS; HUMANS; MALE; MATCHED-PAIR ANALYSIS; MEMBRANE PROTEINS; MIDDLE AGED; NERVE NET; NERVE TISSUE PROTEINS; PREFRONTAL CORTEX; PRESYNAPTIC TERMINALS; QA-SNARE PROTEINS; R-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; SNARE PROTEINS; SYNAPTOPHYSIN; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; VESICULAR TRANSPORT PROTEINS;

EID: 0042831054     PISSN: 13594184     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.mp.4001319     Document Type: Article

References (76)

1. Gold JM, Rehkemper G, Binks III SW, Carpenter CJ, Fleming K, Goldberg TE et al. Learning and forgetting in schizophrenia. J Abnorm Psychol 2000; 109: 534-538.
2. Goldberg TE, Weinberger DR. Probing prefrontal function in schizophrenia with neuropsychological paradigms. Schizophr Bull 1988; 14: 179-183.
3. Goldman-Rakic PS, Selemon LD. Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophr Bull 1997; 23: 437-458.
4. Weickert TW, Goldberg TE, Gold JM, Bigelow LB, Egan MF, Weinberger DR. Cognitive impairments in patients with schizophrenia displaying preserved and compromised intellect. Arch Gen Psychiatry 2000; 57: 907-913.
5. Weinberger DR, Egan MF, Bertolino A, Callicott JH, Mattay VS, Lipska BK et al. Prefrontal neurons and the genetics of schizophrenia. Biol Psychiatry 2001; 50: 825-844.
6. Lewis DA, Cruz DA, Melchitzky DS, Pierri JN. 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 2001; 158: 1411-1422.
7. Meyer-Lindenberg A, Poline JB, Kohn PD, Holt JL, Egan MF, Weinberger DR et al. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am J Psychiatry 2001; 158: 1809-1817.
8. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. Biol Psychiatry 1999; 45: 17-25.
9. Selemon LD, Rajkowska G, Goldman-Rakic PS. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995; 52: 805-818.
10. Benes FM, Davidson J, Bird ED. Quantitative cytoarchitectural studies of the cerebral cortex of schizophrenics. Arch Gen Psychiatry 1986; 43: 31-35.
11. Breier A, Buchanan RW, Elkashef A, Munson RC, Kirkpatrick B, Gellad F. Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex, and caudate structures. Arch Gen Psychiatry 1992; 49: 921-926.
12. Buchanan RW, Vladar K, Barta PE, Pearlson GD. Structural evaluation of the prefrontal cortex in schizophrenia. Am J Psychiatry 1998; 155: 1049-1055.
13. Pakkenberg B. Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry 1993; 34: 768-772.
14. 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.
15. Thune JJ, Uylings HB, Pakkenberg B. No deficit in total number of neurons in the prefrontal cortex in schizophrenics. J Psychiatr Res 2001; 35: 15-21.
16. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000; 57: 65-73.
17. Garey LJ, Ong WY, Patel TS, Kanani M, Davis A, Mortimer AM et al. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry 1998; 65: 446-453.
18. Akil M, Pierri JN, Whitehead RE, Edgar CL, Mohila C, Sampson AR et al. Lamina-specific alterations in the dopamine innervation of the prefront schizophrenic subjects. Am J Psychiatry 1999; 156: 1580-1589.
19. 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.
20. Honer WG, Falkai P, Chen C, Arango V, Mann JJ, Dwork AJ. Synaptic and plasticity-associated proteins in anterior frontal cortex in severe mental illness. Neuroscience 1999; 91: 1247-1255.
21. 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.
22. Ohnuma T, Kato H, Arai H, Faull RL, McKenna PJ, Emson PC. Gene expression of PSD95 in prefrontal cortex and hippocampus in schizophrenia. Neuroreport 2000; 11: 3133-3137.
23. 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.
24. Betrolino A, Esposito G, Callicott JH, Mattay VS, Van Horn JD, Frank JA et al. Specific relationship between prefrontal neuronal N-acetylaspartate and activation of the working memory cortical network in schizophrenia. Am J Psychiatry 2000; 157: 26-33.
25. Middleton FA, Mirnics K, Pierri JN, Lewis DA, Levitt P. Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia. J Neurosci 2002; 22: 2718-2729.
26. Karson CN, Mrak RE, Schluterman KO, Sturner WQ, Sheng JG, Griffin WS. Alterations in synaptic proteins and their encoding mRNAs in prefrontal cortex in schizophrenia: a possible neurochemical basis for 'hypofrontality'. Mol Psychiatry 1999; 4: 39-45.
27. Eastwood SL, Cairns NJ, Harrison PJ. Synaptophysin gene expression in schizophrenia. Investigation of synaptic pathology in the cerebral cortex. Br J Psychiatry 2000; 176: 236-242.
28. 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.
29. Perrone-Bizzozero NI, Sower AC, Bird ED, Benowitz LI, Ivins KJ, Neve RL. 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.
30. Eastwood SL, Burnet PW, McDonald B, Clinton J, Harrison PJ. Synaptophysin gene expression in human brain: a quantitative in situ hybridization and immunocytochemical study. Neuroscience 1994; 59: 881-892.
31. Lewis DA. The human brain revisited: opportunities and challenges in postmortem studies of psychiatric disorders. Neuropsychopharmacology 2002; 26: 143-154.
32. Eastwood SL, McDonald B, Burnet PW, Beckwith JP, Kerwin RW, Harrison PJ. Decreased expression of mRNAs encoding non-NMDA glutamate receptors GluR1 and GluR2 in medial temporal lobe neurons in schizophrenia. Brain Res Mol Brain Res 1995; 29: 211-223.
33. Falkai P, Bogerts B. Cell loss in the hippocampus of schizophrenics. Eur Arch Psychiatry Neurol Sci 1986; 236: 154-161.
34. Harrison PJ. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 1999; 122: 593-624.
35. Suddath RL, Christisin GW, Torrey EF, Casanova M, Weinberger DR. Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. N Engl J Med 1990; 322: 789-794.
36. Weinberger DR. Cell biology of the hippocampal formation in schizophrenia. Biol Psychiatry 1999; 45: 395-402.
37. Lipska BK, Weinberger DR. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000; 23: 223-239.
38. Carr DB, Sesack SR. Hippocampal afferents to the rat prefrontal cortex: synaptic targets and relation to dopaminergic terminals. J Comp Neurol 1996; 369: 1-15.
39. Jay TM, Glowinski J, Thierry A-M. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 1989; 505: 337-340.
40. Lipska BK, Aultman JM, Verma A, Weinberger DR, Moghaddam B. Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 2002; 27: 47-54.
41. Lipska BK, Jaskiw GE, Weinberger DR. Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal hippocampal damage: a potential animal model of schizophrenia. Neuropsychopharmacology 1993; 9: 67-75.
42. Lipska BK, Al-Amin HA, Weinberger DR. Excitotoxic lesions of the rat medial prefrontal cortex: effects on abnormal behaviors associated with neonatal hippocampal damage. Neuropsychopharmacology 1998; 19: 451-464.
43. O'Donnell P, Lewis BL, Lerman D, Weinberger DR, Lipska BK. Neonatal hippocampal damage alters electrophysiological properties of prefrontal cortical neurons. Cereb Cortex 2002; 12: 975-982.
44. Bertolino A, Roffman JL, Lipska BK, Van Gelderen P, Olson A, Weinberger DR. Postpubertal emergence of prefrontal neuronal deficits and altered dopaminergic behaviors in rats with neonatal hippocampal lesions. Cereb Cortex 2002; 12: 983-990.
45. Gorny G, Kolb B, Weinberger DR, Sheridan R, Lipska BK. Synaptic pathology in the prefrontal cortex and nucleus accumbens of rats with neonatal damage of the ventral hippocampus. Soc Neurosci Abstract 2001; 27: 876.16.
46. Kleinman JE, Hyde TM, Herman MM. Methodological issues in the neuropathology of mental illness. In: Bloom FE, Kupfer DJ (eds). Psychopharmacology: the Fourth Generation of Progress. Raven Press: New York, 1995, pp 859-864.
47. Zalcman S, Endicott J, Clayton P, Winokur G. Diagnostic Evaluation After Death (DEAD). National Institute of Mental Health: Rockville, MD, 1983.
48. Keks NA, Hill C, Opeskin K, Copolov D, Dean B. Psychiatric diagnosis after death: the problems of accurate diagnosis from case history review and relative interviews. In: Dean B, Kleinman JE (eds). Using CNS Tissue in Psychiatric Research: A Practical Guide. Overseas Publishers Association: Amsterdam, 1999, pp. 19-37.
49. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC, 1994.
50. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, compact 3rd edn. Academic Press: San Diego, CA, 1997.
51. Romanczyk TB, Shannon Weickert C, Webster MJ, Herman MM, Akil M, Kleinman JE. Alterations in trkB mRNA in the human prefrontal cortex throughout the lifespan. Eur J Neurosci 2002; 15: 269-280.
52. 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.
53. Masliah E, Terry RD, Alford M, DeTeresa R. Quantitative immunohistochemistry of synaptophysin in human neocortex: an alternative method to estimate density of presynaptic terminals in paraffin sections. J Histochem Cytochem 1990; 38: 837-844.
54. Masliah E, Terry RD. The role of synaptic proteins in the pathogenesis of disorders of the central nervous system. Brain Pathol 1993; 3: 77-86.
55. Masliah E, Miller A, Terry RD. The synaptic organization of the neocortex in Alzheimer's disease. Med Hypotheses 1993; 41: 334-340.
56. 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. Schiz Res 2002; 58: 11-20.
57. Glantz LA, Lewis DA. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia. Regional and diagnostic specificity. Arch Gen Psychiatry 1997; 54: 943-952.
58. Glantz LA, Austin MC, Lewis DA. Normal cellular levels of synaptophysin mRNA expression in the prefrontal cortex of subjects with schizophrenia. Biol Psych 2000; 48: 389-397.
59. Thompson PM, Sower AC, Perrone-Bizzozero NI. Altered levels of the synaptosomal associated protein SNAP-25 in schizophrenia. Biol Psychiatry 1998; 43: 239-243.
60. Eastwood SL, Harrison PJ. Hippocampal and cortical growth-associated protein-43 messenger RNA in schizophrenia. Neuroscience 1998; 86: 437-448.
61. Honer WG, Falkai P, Li H-Y, Knable MB, Buslei R, Bayer TA. Abnormalities of prefrontal cortex SNARE complex proteins in bipolar disorder. Bipolar Disord 2002; 4(Suppl 1): 50.
62. Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC et al. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001; 294: 1117-1122.
63. Trimble WS, Gray TS, Elferink LA, Wilson MC, Scheller RH. Distinct patterns of expression of two VAMP genes within the rat brain. J Neurosci 1990; 10: 1380-1387.
64. Hu K, Carroll J, Fedorovich S, Rickman C, Sukhodub A, Davletov B. Vesicular restriction of synaptobrevin suggests a role for calcium in membrane fusion. Nature 2002; 415: 646-650.
65. Lipska BK, Caruso A, Lund I, Weinberger DR. Evaluation of projections to the medial prefrontal cortex in rats with neonatal ventral hippocampal lesion: a retrograde labeling study. Soc Neurosci Abstract 2000; 26: 1039.
66. Owe-Larsson B, Berglund M, Kristensson K, Garoff H, Larhammar D, Brodin L et al. Perturbation of the synaptic release machinery in hippocampal neurons by overexpression of SNAP-25 with the Semliki Forest virus vector. Eur J Neurosci 1999; 11: 1981-1987.
67. Bittner MA, Bennett MK, Holz RW. Evidence that syntaxin 1A is involved in storage in the secretory pathway. J Biol Chem 1996; 271: 11214-11221.
68. Lipska BK, Halim ND, Segal PN, Weinberger DR. Effects of reversible inactivation of the neonatal ventral hippocampus on behavior in the adult rat. J Neurosci 2002; 22: 2835-2842.
69. Nakahara T, Nakamura K, Tsutsumi T, Hashimoto K, Hondo H, Hisatomi S et al. Effect of chronic haloperidol treatment on synaptic protein mRNAs in the rat brain. Brain Res Mol Brain Res 1998; 61: 238-242.
70. Masliah E, Mallory M, Hansen L, DeTeresa R, Terry RD. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 1993; 43: 192-197.
71. Shimohama S, Fujimoto S, Sumida Y, Akagawa K, Shirao T, Matsuoka Y et al. Differential expression of rat brain synaptic proteins in development and aging. Biochem Biophys Res Comm 1998; 251: 394-398.
72. Harrison PJ. The neuropathological effects of antipsychotic drugs. Schizophr Res 1999; 40: 87-99.
73. Lidow MS, Song ZM, Castner SA, Allen PB, Greengard P, Goldman-Rakic PS. Antipsychotic treatment induces alterations in dendrite- and spine-associated proteins in dopamine-rich areas of the primate cerebral cortex. Biol Psychiatry 2001; 49: 1-12.
74. 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.
75. Fog R, Pakkenberg H, Juul P, Back E, Jorgensen OS, Andersen J. High-dose treatment of rats with perphenazine enanthate. Psychopharmacology 1976; 50: 305-307.
76. Sawada K, Young CE, Barr AM, Longworth K, Takahashi S, Arango V et al. Altered immunoreactivity of complexin protein in prefrontal cortex in severe mental illness. Mol Psychiatry 2002; 7: 484-492.