Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts

Biological Psychiatry

Volumn 58, Issue 2, 2005, Pages 85-96

  Altar, C Anthony ^a   Jurata, Linda W ^a   Charles, Vin ^a   Lemire, Andrew ^a   Liu, Peng ^a   Bukhman, Yury ^a   Young, Theresa A ^a   Bullard, Jeff ^a   Yokoe, Hiroko ^a   Webster, Maree J ^b   Knable, Michael B ^c   Brockman, Jeffrey A ^a  

^a Psychiatric Genomics Inc   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c Stanley Medical Research Institute   (United States)

Author keywords

Bipolar disease; Dentate gyrus; Laser capture microdissection; Major depression; Microarray; Schizophrenia

Indexed keywords

COMPLEMENTARY DNA; CYTOCHROME C OXIDASE; CYTOSKELETON PROTEIN; ISOCITRIC ACID; LACTIC ACID; MALIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEASOME; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SUCCINATE DEHYDROGENASE; UBIQUITIN;

AEROBIC METABOLISM; ANAMNESIS; ARTICLE; AUTOPSY; BIPOLAR DISORDER; BODY WEIGHT; BRAIN; BRAIN NERVE CELL; BRAIN WEIGHT; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DNA MICROARRAY; ENERGY METABOLISM; FRONTAL CORTEX; GENE; GENE CLUSTER; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; LASER CAPTURE MICRODISSECTION; MAJOR DEPRESSION; MENTAL PATIENT; MITOCHONDRIAL GENETICS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NERVE CELL; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUROIMAGING; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHIZOPHRENIA; SEX; UNINDEXED SEQUENCE;

ANALYSIS OF VARIANCE; BIPOLAR DISORDER; CASE-CONTROL STUDIES; DENTATE GYRUS; DEPRESSIVE DISORDER, MAJOR; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; GENE EXPRESSION PROFILING; HUMANS; HYDROGEN-ION CONCENTRATION; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; SCHIZOPHRENIA; SEVERITY OF ILLNESS INDEX; UBIQUITIN;

EID: 22444441576     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2005.03.031     Document Type: Article

References (80)

1. S.E. Arnold, J.Q. Trojanowski Recent advances in defining the neuropathology of schizophrenia Acta Neuropathol (Berl) 92 1996 217 231
2. S. Bahn, S.J. Augood, M. Ryan, D.G. Standaert, M. Starkey, P.C. Emson Gene expression profiling in the post-mortem human brain-no cause for dismay J Chem Neuroanat 22 2001 79 94
3. C.L. Beasley, Z.J. Zhang, I. Patten, G.P. Reynolds Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins Biol Psychiatry 52 2002 708 715
4. F.M. Benes, S. Berreta Amygdalo-entorhinal inputs to the hippocampal formation in relation to schizophrenia Ann N Y Acad Sci 911 2000 283 304
5. D. Ben-Shachar Mitochondrial dysfunction in schizophrenia A possible linkage to dopamine J Neurochem 83 2002 1241 1251
6. A. Bertolino, J.H. Callicott, V.S. Mattay, K.M. Weidenhammer, R. Rakow, M.F. Egan The effect of treatment with antipsychotic drugs on brain N-acetylaspartate measures in patients with schizophrenia Biol Psychiatry 49 2001 39 46
7. A. Bertolino, S. Nawroz, V.S. Mattay, A.S. Barnett, J.H. Duyn, C.T. Moonen Regionally specific pattern of neurochemical pathology in schizophrenia as assessed by multislice proton magnetic resonance spectroscopic imaging Am J Psychiatry 153 1996 1554 1563
8. E. Bleuler Dementia Praecox or the Group of Schizophrenias 1950 International Universities Press New York
9. M.S. Buchsbaum, K.H. Nuechterlein, R.J. Haier, J. Wu, N. Sicotte, E. Hazlett Glucose metabolic rate in normals and schizophrenics during the Continuous Performance Test assessed by positron emission tomography Br J Psychiatry 156 1990 216 227
10. M.S. Buchsbaum, L. Shihabuddin, E.A. Hazlett, J. Schroder, M.M. Haznedar, P. Powchik Kraepelinian and non-Kraepelinian schizophrenia subgroup differences in cerebral metabolic rate Schizophr Res 55 2002 25 40
11. W. Byne, M.S. Buchsbaum, L.A. Mattiace, E.A. Hazlett, E. Kemether, S.L. Elhakem Postmortem assessment of thalamic nuclear volumes in subjects with schizophrenia Am J Psychiatry 159 2002 59 65
12. L. Cavelier, E.E. Jazin, I. Eriksson, J. Prince, U. Bave, L. Oreland Decreased cytochrome-c oxidase activity and lack of age-related accumulation of mitochondrial DNA deletions in the brains of schizophrenics Genomics 29 1995 217 224
13. M.L. Chen, C.H. Chen Microarray analysis of differentially expressed genes in rat frontal cortex under chronic risperidone treatment Neuropsychopharmacology 30 2004 1 10
14. J.M. Crook, E. Tomaskovic-Crook, D.L. Copolov, B. Dean Decreased muscarinic receptor binding in subjects with schizophrenia A study of the human hippocampal formation Biol Psychiatry 48 2000 381 388
15. K.L. Davis, D.G. Stewart, J.I. Friedman, M. Buchsbaum, P.D. Harvey, P.R. Hof White matter changes in schizophrenia Evidence for myelin-related dysfunction Arch Gen Psychiatry 60 2003 443 456
16. M. Desco, J.D. Gispert, S. Reig, J. Sanz, J. Pascau, F. Sarramea Cerebral metabolic patterns in chronic and recent-onset schizophrenia Psychiatry Res 122 2003 125 135
17. C.C. Dickey, R.W. McCarley, M.E. Shenton The brain in schizotypal personality disorder A review of structural MRI and CT findings Harv Rev Psychiatry 10 2002 1 15
18. D. Dwyer, X. Lu, A. Freeman Neuronal glucose metabolism and schizophrenia Therapeutic prospects? Expert Rev Neurother 3 2003 89 100
19. S.L. Eastwood, B. McDonald, P.W. Burnet, J.P. Beckwith, R.W. Kerwin, P.J. Harrison Decreased expression of mRNAs encoding non-NMDA glutamate receptors GluR1 and GluR2 in medial temporal lobe neurons in schizophrenia Brain Res Mol Brain Res 29 1995 211 223
20. J. Eberwine Amplification of mRNA populations using aRNA generated from immobilized oligo(dT)-T7 primed cDNA Biotechniques 20 1996 584 591
21. M.D. Ehlers Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system Nat Neurosci 6 2003 231 242
22. D. Fannon, A. Simmons, L. Tennakoon, S. O'Ceallaigh, A. Sumich, V. Doku Selective deficit of hippocampal N-acetylaspartate in antipsychotic-naive patients with schizophrenia Biol Psychiatry 54 2003 587 598
23. R. Freedman, C.E. Adams, S. Leonard The alpha7-nicotinic acetylcholine receptor and the pathology of hippocampal interneurons in schizophrenia J Chem Neuroanat 20 2000 299 306
24. Y. Hakak, J.R. Walker, C. Li, W.H. Wong, K.L. Davis, J.D. Buxbaum Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia Proc Natl Acad Sci U S A 98 2001 4746 4751
25. P.J. Harrison The neuropathology of schizophrenia. A critical review of the data and their interpretation Brain 122 1999 593 624
26. P.J. Harrison The hippocampus in schizophrenia A review of the neuropathological evidence and its pathophysiological implications Psychopharmacology (Berl) 174 2004 151 162
27. P.J. Harrison, P.R. Heath, S.L. Eastwood, P.W. Burnet, B. McDonald, R.C. Pearson The relative importance of premortem acidosis and postmortem interval for human brain gene expression studies Selective mRNA vulnerability and comparison with their encoded proteins Neurosci Lett 200 1995 151 154
28. A.N. Hegde, A. DiAntonio Ubiquitin and the synapse Nat Rev Neurosci 3 2002 854 861
29. S.E. Hemby, S.D. Ginsberg, B. Brunk, S.E. Arnold, J.Q. Trojanowski, J.H. Eberwine Gene expression profile for schizophrenia Discrete neuron transcription patterns in the entorhinal cortex Arch Gen Psychiatry 59 2002 631 640
30. G.U. Hoglinger, G. Carrard, P.P. Michel, F. Medja, A. Lombes, M. Ruberg Dysfunction of mitochondrial complex I and the proteasome Interactions between two biochemical deficits in a cellular model of Parkinson's disease J Neurochem 86 2003 1297 1307
31. H.H. Holcomb, N.G. Cascella, G.K. Thaker, D.R. Medoff, R.F. Dannals, C.A. Tamminga Functional sites of neuroleptic drug action in the human brain PET/FDG studies with and without haloperidol Am J Psychiatry 153 1996 41 49
32. D.A. Hosack, G. Dennis Jr, B.T. Sherman, H.C. Lane, R.A. Lempicki Identifying biological themes within lists of genes with EASE Genome Biol 4 2003 R70
33. F. Jessen, L. Scheef, L. Germeshausen, Y. Tawo, M. Kockler, K.U. Kuhn Reduced hippocampal activation during encoding and recognition of words in schizophrenia patients Am J Psychiatry 160 2003 1305 1312
34. N.L. Johnston, J. Cervenak, A.D. Shore, E.F. Torrey, R.H. Yolken, J. Cerevnak Multivariate analysis of RNA levels from postmortem human brains as measured by three different methods of RT-PCR. Stanley Neuropathology Consortium J Neurosci Methods 77 1997 83 92
35. L. Jurata, Y.V. Bukhman, V.D. Charles, F. Capriglione, J. Bullard, A. Lemire Comparison of mRNA profiling technologies for identification of psychiatric disease and drug signatures J Neurosci Methods 138 1-2 2004 173 188
36. A.E. Kingsbury, O.J. Foster, A.P. Nisbet, N. Cairns, L. Bray, D.J. Eve Tissue pH as an indicator of mRNA preservation in human post-mortem brain Brain Res Mol Brain Res 28 1995 311 318
37. H. Kishimoto, K. Yamada, E. Iseki, K. Kosaka, T. Okoshi Brain imaging of affective disorders and schizophrenia Psychiatry Clin Neurosci 52 suppl 1998 S212 S214
38. M.B. Knable, B.M. Barci, M.J. Webster, J. Meador-Woodruff, E.F. Torrey Molecular abnormalities of the hippocampus in severe psychiatric illness Postmortem findings from the Stanley Neuropathology Consortium Mol Psychiatry 9 6 2004 609 620 544
39. M.B. Knable, E.F. Torrey, M.J. Webster, J.J. Bartko Multivariate analysis of prefrontal cortical data from the Stanley Foundation Neuropathology Consortium Brain Res Bull 55 2001 651 659
40. C. Konradi, M. Eaton, M.L. MacDonald, J. Walsh, F.M. Benes, S. Heckers Molecular evidence for mitochondrial dysfunction in bipolar disorder Arch Gen Psychiatry 61 2004 300 308
41. E. Kraeplin, R.M. Barclay Dementia Praecox and Paraphrenia 1971 Krieger RE New York
42. L. Kung, R.C. Roberts Mitochondrial pathology in human schizophrenic striatum A postmortem ultrastructural study Synapse 31 1999 67 75
43. M. Lauer, H. Beckmann, D. Senitz Increased frequency of dentate granule cells with basal dendrites in the hippocampal formation of schizophrenics Psychiatry Res 122 2003 89 97
44. A.J. Law, J.F. Deakin Asymmetrical reductions of hippocampal NMDAR1 glutamate receptor mRNA in the psychoses Neuroreport 12 2001 2971 2974
45. E. Lehrmann, T.M. Hyde, M.P. Vawter, K.G. Becker, J.E. Kleinman, W.J. Freed The use of microarrays to characterize neuropsychiatric disorders Postmortem studies of substance abuse and schizophrenia Curr Mol Med 3 2003 437 446
46. J.Z. Li, M.P. Vawter, D.M. Walsh, H. Tomita, S.J. Evans, P.V. Choudary Systematic changes in gene expression in postmortem human brains associated with tissue pH and terminal medical conditions Hum Mol Genet 13 2004 609 616
47. L. Luo, R.C. Salunga, H. Guo, A. Bittner, K.C. Joy, J.E. Galindo Gene expression profiles of laser-captured adjacent neuronal subtypes Nat Med 5 1999 117 122
48. X.J. Ma, R. Salunga, J.T. Tuggle, J. Gaudet, E. Enright, P. McQuary Gene expression profiles of human breast cancer progression Proc Natl Acad Sci U S A 100 2003 5974 5979
49. R.M. Marchbanks, J. Mulcrone, S.A. Whatley Aspects of oxidative metabolism in schizophrenia Br J Psychiatry 167 1995 293 298
50. I. Maurer, S. Zierz, H. Moller Evidence for a mitochondrial oxidative phosphorylation defect in brains from patients with schizophrenia Schizophr Res 48 2001 125 136
51. R.W. McCarley, C.G. Wible, M. Frumin, Y. Hirayasu, J.J. Levitt, I.A. Fischer MRI anatomy of schizophrenia Biol Psychiatry 45 1999 1099 1119
52. F.A. Middleton, K. Mirnics, J.N. Pierri, D.A. Lewis, P. Levitt Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia J Neurosci 22 2002 2718 2729
53. K. Mirnics, F.A. Middleton, A. Marquez, D.A. Lewis, P. Levitt Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex Neuron 28 2000 53 67
54. R.K. Murphey, T.A. Godenschwege New roles for ubiquitin in the assembly and function of neuronal circuits Neuron 36 2002 5 8
55. S. Nudmamud, L.M. Reynolds, G.P. Reynolds N-acetylaspartate and N-acetylaspartylglutamate deficits in superior temporal cortex in schizophrenia and bipolar disorder A postmortem study Biol Psychiatry 53 2003 1138 1141
56. D.T. Pak, M. Sheng Targeted protein degradation and synapse remodeling by an inducible protein kinase Science 302 2003 1368 1373
57. W.M. Perlstein, N.K. Dixit, C.S. Carter, D.C. Noll, J.D. Cohen Prefrontal cortex dysfunction mediates deficits in working memory and prepotent responding in schizophrenia Biol Psychiatry 53 2003 25 38
58. S. Prabakaran, J.E. Swatton, M.M. Ryan, S.J. Huffaker, J.J. Huang, J.L. Griffin Mitochondrial dysfunction in schizophrenia Evidence for compromised brain metabolism and oxidative stress Mol Psychiatry 9 7 2004 684 697 643
59. J.A. Prince, J. Harro, K. Blennow, C.G. Gottfries, L. Oreland Putamen mitochondrial energy metabolism is highly correlated to emotional and intellectual impairment in schizophrenics Neuropsychopharmacology 22 2000 284 292
60. J.A. Prince, L. Oreland Mitochondrial activity in the mapping of functional brain changes in schizophrenia Restor Neurol Neurosci 12 1998 185 193
61. J.A. Prince, M.S. Yassin, L. Oreland Neuroleptic-induced mitochondrial enzyme alterations in the rat brain J Pharmacol Exp Ther 280 1997 261 267
62. J.A. Prince, M.S. Yassin, L. Oreland Normalization of cytochrome-c oxidase activity in the rat brain by neuroleptics after chronic treatment with PCP or methamphetamine Neuropharmacology 36 1997 1665 1678
63. J.A. Prince, M.S. Yassin, L. Oreland A histochemical demonstration of altered cytochrome oxidase activity in the rat brain by neuroleptics Eur Neuropsychopharmacol 8 1998 1 6
64. J. Quackenbush Microarray data normalization and transformation Nat Genet 32 suppl 2002 496 501
65. D.K. Slonim From patterns to pathways Gene expression data analysis comes of age Nat Genet 32 suppl 2002 502 508
66. B.P. Sokolov, L. Jiang, N.S. Trivedi, C. Aston Transcription profiling reveals mitochondrial, ubiquitin and signaling systems abnormalities in postmortem brains from subjects with a history of alcohol abuse or dependence J Neurosci Res 72 2003 756 767
67. S.D. Speese, N. Trotta, C.K. Rodesch, B. Aravamudan, K. Broadie The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy Curr Biol 13 2003 899 910
68. W.S. Stone, L.J. Seidman, J.D. Wojcik, A.I. Green Glucose effects on cognition in schizophrenia Schizophr Res 62 2003 93 103
69. Y. Takahashi, T. Kumanishi, S. Hayashi Using a DNA microarray method to examine gene expression in brain from clozapine-injected mice Ann NY Acad Sci 1025 2004 561 569
70. C.A. Tamminga, G.K. Thaker, R. Buchanan, B. Kirkpatrick, L.D. Alphs, T.N. Chase Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome Arch Gen Psychiatry 49 1992 522 530
71. D. Tkachev, M.L. Mimmack, M.M. Ryan, M. Wayland, T. Freeman, P.B. Jones Oligodendrocyte dysfunction in schizophrenia and bipolar disorder Lancet 362 2003 798 805
72. E.F. Torrey, M. Webster, M. Knable, N. Johnston, R.H. Yolken The stanley foundation brain collection and neuropathology consortium Schizophr Res 44 2000 151 155
73. G. Tsai, L.A. Passani, B.S. Slusher, R. Carter, L. Baer, J.E. Kleinman Abnormal excitatory neurotransmitter metabolism in schizophrenic brains Arch Gen Psychiatry 52 1995 829 836
74. N. Uranova, D. Orlovskaya, O. Vikhreva, I. Zimina, N. Kolomeets, V. Vostrikov Electron microscopy of oligodendroglia in severe mental illness Brain Res Bull 55 2001 597 610
75. R.N. Van Gelder, M.E. von Zastrow, A. Yool, W.C. Dement, J.D. Barchas, J.H. Eberwine Amplified RNA synthesized from limited quantities of heterogeneous cDNA Proc Natl Acad Sci U S A 87 1990 1663 1667
76. M.P. Vawter, T. Barrett, C. Cheadle, B.P. Sokolov, W.H. Wood 3rd, D.M. Donovan Application of cDNA microarrays to examine gene expression differences in schizophrenia Brain Res Bull 55 2001 641 650
77. D. Velakoulis, G.W. Stuart, S.J. Wood, D.J. Smith, W.J. Brewer, P. Desmond Selective bilateral hippocampal volume loss in chronic schizophrenia Biol Psychiatry 50 2001 531 539
78. W.N. Venables, B.D. Ripley Modern Applied Statistics with S 4th ed. 2002 Springer
79. D.R. Weinberger Cell biology of the hippocampal formation in schizophrenia Biol Psychiatry 45 1999 395 402
80. S.A. Whatley, D. Curtis, R.M. Marchbanks Mitochondrial involvement in schizophrenia and other functional psychoses Neurochem Res 21 1996 995 1004