Immune system disturbances in schizophrenia

Biological Psychiatry

Volumn 75, Issue 4, 2014, Pages 316-323

  Horváth, Szatmár ^a,c   Mirnics, Károly ^a,b,c  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF SZEGED   (Hungary)

Author keywords

blood vessels; Blood brain barrier; CD14; CHI3L1; IFITM; IFITM3; immune; meninges; pia mater; postmortem; schizophrenia; SERPINA3

Indexed keywords

ANTIINFLAMMATORY AGENT; BIOLOGICAL MARKER; INTERFERON INDUCIBLE TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN; SERINE PROTEINASE INHIBITOR; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; BLOOD VESSEL; BRAIN DEVELOPMENT; CLADISTICS; ENDOTHELIUM CELL; GENE EXPRESSION; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOPATHOLOGY; INTERNEURON; MENINX; MULTIGENE FAMILY; NONHUMAN; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA;

BLOOD VESSELS; BLOOD-BRAIN BARRIER; CD14; CHI3L1; IFITM; IFITM3; IMMUNE; MENINGES; PIA MATER; POSTMORTEM; SCHIZOPHRENIA; SERPINA3;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BRAIN; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MATERNAL EXPOSURE; MEMBRANE PROTEINS; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; RNA-BINDING PROTEINS; SCHIZOPHRENIA; SERPINS; TRANSCRIPTOME;

EID: 84892572641     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.06.010     Document Type: Review

References (95)

1. M. Michel, M.J. Schmidt, and K. Mirnics Immune system gene dysregulation in autism and schizophrenia Dev Neurobiol 72 2012 1277 1287
2. A.S. Brown The environment and susceptibility to schizophrenia Prog Neurobiol 93 2010 23 58
3. A.S. Brown, and E.J. Derkits Prenatal infection and schizophrenia: A review of epidemiologic and translational studies Am J Psychiatry 167 2010 261 280
4. N. Muller COX-2 inhibitors as antidepressants and antipsychotics: Clinical evidence Curr Opin Investig Drugs 11 2010 31 42
5. N. Muller, A.M. Myint, and M.J. Schwarz Immunological treatment options for schizophrenia Curr Pharm Biotechnol 13 2012 1606 1613
6. H. Stefansson, R.A. Ophoff, S. Steinberg, O.A. Andreassen, S. Cichon, and D. Rujescu et al. Common variants conferring risk of schizophrenia Nature 460 2009 744 747
7. M. Bamne, J. Wood, K. Chowdari, A.M. Watson, C. Celik, and H. Mansour et al. Evaluation of HLA polymorphisms in relation to schizophrenia risk and infectious exposure Schizophr Bull 38 2012 1149 1154
8. I. Agartz, A.A. Brown, L.M. Rimol, C.B. Hartberg, A.M. Dale, and I. Melle et al. Common sequence variants in the major histocompatibility complex region associate with cerebral ventricular size in schizophrenia Biol Psychiatry 70 2011 696 698
9. Consortium SPG-WAS Genome-wide association study identifies five new schizophrenia loci Nat Genet 43 2011 969 976
10. P. Jia, L. Wang, A.H. Fanous, X. Chen, K.S. Kendler, and Z. Zhao A bias-reducing pathway enrichment analysis of genome-wide association data confirmed association of the MHC region with schizophrenia J Med Genet 49 2011 96 103
11. T. Li, J. Underhill, X.H. Liu, P.C. Sham, P. Donaldson, and R.M. Murray et al. Transmission disequilibrium analysis of HLA class II DRB1, DQA1, DQB1 and DPB1 polymorphisms in schizophrenia using family trios from a Han Chinese population Schizophr Res 49 2001 73 78
12. D. Arion, T. Unger, D.A. Lewis, P. Levitt, and K. Mirnics Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia Biol Psychiatry 62 2007 711 721
13. D. Arion, S. Horvath, D.A. Lewis, and K. Mirnics Infragranular gene expression disturbances in the prefrontal cortex in schizophrenia: Signature of altered neural development? Neurobiol Dis 37 2009 738 746
14. P. Saetre, L. Emilsson, E. Axelsson, J. Kreuger, E. Lindholm, and E. Jazin Inflammation-related genes up-regulated in schizophrenia brains BMC Psychiatry 7 2007 46
15. S.G. Fillman, N. Cloonan, V.S. Catts, L.C. Miller, J. Wong, and T. McCrossin et al. Increased inflammatory markers identified in the dorsolateral prefrontal cortex of individuals with schizophrenia Mol Psychiatry 18 2012 206 214
16. B.J. Miller, P. Buckley, W. Seabolt, A. Mellor, and B. Kirkpatrick Meta-analysis of cytokine alterations in schizophrenia: Clinical status and antipsychotic effects Biol Psychiatry 70 2011 663 671
17. S.M. Kurian, H. Le-Niculescu, S.D. Patel, D. Bertram, J. Davis, and C. Dike et al. Identification of blood biomarkers for psychosis using convergent functional genomics Mol Psychiatry 16 2009 37 58
18. R.C. Drexhage, E.M. Knijff, R.C. Padmos, L. Heul-Nieuwenhuijzen, W. Beumer, and M.A. Versnel et al. The mononuclear phagocyte system and its cytokine inflammatory networks in schizophrenia and bipolar disorder Expert Rev Neurother 10 2009 59 76
19. X.Q. Song, L.X. Lv, W.Q. Li, Y.H. Hao, and J.P. Zhao The interaction of nuclear factor-kappa B and cytokines is associated with schizophrenia Biol Psychiatry 65 2009 481 488
20. J. Steiner, M. Walter, W. Glanz, Z. Sarnyai, H.G. Bernstein, and S. Vielhaber et al. Increased prevalence of diverse N-methyl-D-aspartate glutamate receptor antibodies in patients with an initial diagnosis of schizophrenia: Specific relevance of IgG NR1a antibodies for distinction from N-methyl-D-aspartate glutamate receptor encephalitis JAMA Psychiatry 70 2013 271 278
21. M. Berk, O. Dean, H. Drexhage, J.J. McNeil, S. Moylan, and A. Oneil et al. Aspirin: A review of its neurobiological properties and therapeutic potential for mental illness BMC Med 11 2013 74
22. N. Muller, D. Krause, S. Dehning, R. Musil, R. Schennach-Wolff, and M. Obermeier et al. Celecoxib treatment in an early stage of schizophrenia: Results of a randomized, double-blind, placebo-controlled trial of celecoxib augmentation of amisulpride treatment Schizophr Res 121 2010 118 124
23. H. Sugino, T. Futamura, Y. Mitsumoto, K. Maeda, and Y. Marunaka Atypical antipsychotics suppress production of proinflammatory cytokines and up-regulate interleukin-10 in lipopolysaccharide-treated mice Prog Neuropsychopharmacol Biol Psychiatry 33 2009 303 307
24. B. Dean Understanding the role of inflammatory-related pathways in the pathophysiology and treatment of psychiatric disorders: Evidence from human peripheral studies and CNS studies Int J Neuropsychopharmacol 14 2010 997 1012
25. L. Shi, S.H. Fatemi, R.W. Sidwell, and P.H. Patterson Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring J Neurosci 23 2003 297 302
26. H. Nawa, and N. Takei Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines Neurosci Res 56 2006 2 13
27. H. Nawa, and K. Yamada Experimental schizophrenia models in rodents established with inflammatory agents and cytokines Methods Mol Biol 829 2012 445 451
28. A.S. Brown, C.A. Schaefer, C.P. Quesenberry Jr, L. Liu, V.P. Babulas, and E.S. Susser Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring Am J Psychiatry 162 2005 767 773
29. S.E. Smith, J. Li, K. Garbett, K. Mirnics, and P.H. Patterson Maternal immune activation alters fetal brain development through interleukin-6 J Neurosci 27 2007 10695 10702
30. P. Boksa Effects of prenatal infection on brain development and behavior: A review of findings from animal models Brain Behav Immun 24 2010 881 897
31. J.L. Moreno, M. Kurita, T. Holloway, J. Lopez, R. Cadagan, and L. Martinez-Sobrido et al. Maternal influenza viral infection causes schizophrenia-like alterations of 5-HT(2)A and mGlu(2) receptors in the adult offspring J Neurosci 31 2010 1863 1872
32. S. Giovanoli, H. Engler, A. Engler, J. Richetto, M. Voget, and R. Willi et al. Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice Science 339 2013 1095 1099
33. T.V. Lipina, C. Zai, D. Hlousek, J.C. Roder, and A.H. Wong Maternal immune activation during gestation interacts with Disc1 point mutation to exacerbate schizophrenia-related behaviors in mice J Neurosci 33 2013 7654 7666
34. S. Horvath, Z. Janka, and K. Mirnics Analyzing schizophrenia by DNA microarrays Biol Psychiatry 69 2010 157 162
35. K. Mirnics, P. Levitt, and D.A. Lewis Critical appraisal of DNA microarrays in psychiatric genomics Biol Psychiatry 60 2006 163 176
36. S. Horvath, and K. Mirnics Breaking the gene barrier in schizophrenia Nat Med 15 2009 488 490
37. 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
38. 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
39. G. Faludi, and K. Mirnics Synaptic changes in the brain of subjects with schizophrenia Int J Dev Neurosci 29 2011 305 309
40. T. Hashimoto, H.H. Bazmi, K. Mirnics, Q. Wu, A.R. Sampson, and D.A. Lewis Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia Am J Psychiatry 165 2008 479 489
41. T. Hashimoto, D. Arion, T. Unger, J.G. Maldonado-Aviles, H.M. Morris, and D.W. Volk et al. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia Mol Psychiatry 13 2008 147 161
42. F.A. Middleton, K. Mirnics, J.N. Pierri, D.A. Lewis, and P. Levitt Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia J Neurosci 22 2002 2718 2729
43. L. Shao, M.V. Martin, S.J. Watson, A. Schatzberg, H. Akil, and R.M. Myers et al. Mitochondrial involvement in psychiatric disorders Ann Med 40 2008 281 295
44. K. Iwamoto, M. Bundo, and T. Kato 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 14 2005 241 253
45. H. Le-Niculescu, Y. Balaraman, S. Patel, J. Tan, K. Sidhu, and R.E. Jerome et al. Towards understanding the schizophrenia code: An expanded convergent functional genomics approach Am J Med Genet B Neuropsychiatr Genet 144B 2007 129 158
46. Y. Hakak, J.R. Walker, C. Li, W.H. Wong, K.L. Davis, and J.D. Buxbaum et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia Proc Natl Acad Sci U S A 98 2001 4746 4751
47. P. Roussos, P. Katsel, K.L. Davis, L.J. Siever, and V. Haroutunian A system-level transcriptomic analysis of schizophrenia using postmortem brain tissue samples Arch Gen Psychiatry 69 2012 1205 1213
48. J. Li, S.L. Mathieu, R. Harris, J. Ji, D.J. Anderson, and J. Malysz et al. Role of alpha7 nicotinic acetylcholine receptors in regulating tumor necrosis factor-alpha (TNF-alpha) as revealed by subtype selective agonists J Neuroimmunol 239 2011 37 43
49. M. Lee Neurotransmitters and microglial-mediated neuroinflammation Curr Protein Pept Sci 14 2013 21 32
50. D.B. McGavern, and S.S. Kang Illuminating viral infections in the nervous system Nat Rev Immunol 11 2011 318 329
51. P. Katsel, K.L. Davis, J.M. Gorman, and V. Haroutunian Variations in differential gene expression patterns across multiple brain regions in schizophrenia Schizophr Res 77 2005 241 252
52. C. Baker, O. Belbin, N. Kalsheker, and K. Morgan SERPINA3 (aka alpha-1-antichymotrypsin) Front Biosci 12 2007 2821 2835
53. N.A. Twine, C. Janitz, M.R. Wilkins, and M. Janitz Sequencing of hippocampal and cerebellar transcriptomes provides new insights into the complexity of gene regulation in the human brain Neurosci Lett 541 2013 263 268
54. S.M. Gopalan, K.M. Wilczynska, B.S. Konik, L. Bryan, and T. Kordula Nuclear factor-1-X regulates astrocyte-specific expression of the alpha1-antichymotrypsin and glial fibrillary acidic protein genes J Biol Chem 281 2006 13126 13133
55. S.M. Gopalan, K.M. Wilczynska, B.S. Konik, L. Bryan, and T. Kordula Astrocyte-specific expression of the alpha1-antichymotrypsin and glial fibrillary acidic protein genes requires activator protein-1 J Biol Chem 281 2006 1956 1963
56. A.J. Horvath, J.A. Irving, J. Rossjohn, R.H. Law, S.P. Bottomley, and N.S. Quinsey et al. The murine orthologue of human antichymotrypsin: A structural paradigm for clade A3 serpins J Biol Chem 280 2005 43168 43178
57. S.T. Chelbi, M.L. Wilson, A.C. Veillard, S.A. Ingles, J. Zhang, and F. Mondon et al. Genetic and epigenetic mechanisms collaborate to control SERPINA3 expression and its association with placental diseases Hum Mol Genet 21 2013 1968 1978
58. S.T. Chelbi, F. Mondon, H. Jammes, C. Buffat, T.M. Mignot, and J. Tost et al. Expressional and epigenetic alterations of placental serine protease inhibitors: SERPINA3 is a potential marker of preeclampsia Hypertension 49 2007 76 83
59. K.E. Taylor, and K.L. Mossman Recent advances in understanding viral evasion of type I interferon Immunology 138 2013 190 197
60. M.S. Diamond, and M. Farzan The broad-spectrum antiviral functions of IFIT and IFITM proteins Nat Rev Immunol 13 2013 46 57
61. E.M. Feeley, J.S. Sims, S.P. John, C.R. Chin, T. Pertel, and L.M. Chen et al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry PLoS Pathog 7 2011 e1002337
62. A.L. Brass, I.C. Huang, Y. Benita, S.P. John, M.N. Krishnan, and E.M. Feeley et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus Cell 139 2009 1243 1254
63. C.C. Bailey, I.C. Huang, C. Kam, and M. Farzan Ifitm3 limits the severity of acute influenza in mice PLoS Pathog 8 2012 e1002909
64. D.W. Volk, B.I. Siegel, E.J. Sengupta, J.R. Edelson, and D.A. Lewis Elevated transcript levels for viral restriction factors in cortical endothelial cells in schizophrenia Neuropsychopharmacology 38 2012 T32
65. K. Ohi, R. Hashimoto, Y. Yasuda, T. Yoshida, H. Takahashi, and N. Iike et al. The chitinase 3-like 1 gene and schizophrenia: Evidence from a multi-center case-control study and meta-analysis Schizophr Res 116 2010 126 132
66. M.S. Yang, D.W. Morris, G. Donohoe, E. Kenny, C.T. O'Dushalaine, and S. Schwaiger et al. Chitinase-3-like 1 (CHI3L1) gene and schizophrenia: Genetic association and a potential functional mechanism Biol Psychiatry 64 2008 98 103
67. H. Yamamori, R. Hashimoto, K. Ohi, Y. Yasuda, M. Fukumoto, and E. Kasahara et al. A promoter variant in the chitinase 3-like 1 gene is associated with serum YKL-40 level and personality trait Neurosci Lett 513 2012 204 208
68. R.J. Medina, C.L. O'Neill, M. Sweeney, J. Guduric-Fuchs, T.A. Gardiner, and D.A. Simpson et al. Molecular analysis of endothelial progenitor cell (EPC) subtypes reveals two distinct cell populations with different identities BMC Med Genomics 3 2010 18
69. J.G. Bode, C. Ehlting, and D. Haussinger The macrophage response towards LPS and its control through the p38(MAPK)-STAT3 axis Cell Signal 24 2012 1185 1194
70. M. Ringsholt, E.V. Hogdall, J.S. Johansen, P.A. Price, and L.H. Christensen YKL-40 protein expression in normal adult human tissues - an immunohistochemical study J Mol Histol 38 2007 33 43
71. N. Junker, J.S. Johansen, L.T. Hansen, E.L. Lund, and P.E. Kristjansen Regulation of YKL-40 expression during genotoxic or microenvironmental stress in human glioblastoma cells Cancer Sci 96 2005 183 190
72. J.M. Pasternack, C.R. Abraham, B.J. Van Dyke, H. Potter, and S.G. Younkin Astrocytes in Alzheimer's disease gray matter express alpha 1-antichymotrypsin mRNA Am J Pathol 135 1989 827 834
73. P.H. Patterson Immune involvement in schizophrenia and autism: Etiology, pathology and animal models Behav Brain Res 204 2009 313 321
74. E.Y. Hsiao, and P.H. Patterson Placental regulation of maternal-fetal interactions and brain development Dev Neurobiol 72 2012 1317 1326
75. R. Daneman The blood-brain barrier in health and disease Ann Neurol 72 2013 648 672
76. K.A. Garbett, E.Y. Hsiao, S. Kalman, P.H. Patterson, and K. Mirnics Effects of maternal immune activation on gene expression patterns in the fetal brain Transl Psychiatry 2 2012 e98
77. D. Martins-de-Souza, G. Maccarrone, T. Wobrock, I. Zerr, P. Gormanns, and S. Reckow et al. Proteome analysis of the thalamus and cerebrospinal fluid reveals glycolysis dysfunction and potential biomarkers candidates for schizophrenia J Psychiatr Res 44 2010 1176 1189
78. D. Martins-de-Souza, A. Schmitt, R. Roder, M. Lebar, T. Schneider-Axmann, and P. Falkai et al. Sex-specific proteome differences in the anterior cingulate cortex of schizophrenia J Psychiatr Res 44 2010 989 991
79. B. Abazyan, J. Nomura, G. Kannan, K. Ishizuka, K.L. Tamashiro, and F. Nucifora et al. Prenatal interaction of mutant DISC1 and immune activation produces adult psychopathology Biol Psychiatry 68 2010 1172 1181
80. V. Borrell, and O. Marin Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling Nat Neurosci 9 2006 1284 1293
81. F. Impagnatiello, A.R. Guidotti, C. Pesold, Y. Dwivedi, H. Caruncho, and M.G. Pisu et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia Proc Natl Acad Sci U S A 95 1998 15718 15723
82. S.H. Fatemi, E.S. Emamian, D. Kist, R.W. Sidwell, K. Nakajima, and P. Akhter et al. Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice Mol Psychiatry 4 1999 145 154
83. K. Zarbalis, Y. Choe, J.A. Siegenthaler, L.A. Orosco, and S.J. Pleasure Meningeal defects alter the tangential migration of cortical interneurons in Foxc1hith/hith mice Neural Dev 7 2012 2
84. E.E. McCandless, M. Budde, J.R. Lees, D. Dorsey, E. Lyng, and R.S. Klein IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis J Immunol 183 2009 613 620
85. J. Steiner, B. Bogerts, Z. Sarnyai, M. Walter, T. Gos, and H.G. Bernstein et al. Bridging the gap between the immune and glutamate hypotheses of schizophrenia and major depression: Potential role of glial NMDA receptor modulators and impaired blood-brain barrier integrity World J Biol Psychiatry 13 2011 482 492
86. Y. Watanabe, T. Someya, and H. Nawa Cytokine hypothesis of schizophrenia pathogenesis: Evidence from human studies and animal models Psychiatry Clin Neurosci 64 2010 217 230
87. D. Ibi, T. Nagai, A. Nakajima, H. Mizoguchi, T. Kawase, and D. Tsuboi et al. Astroglial IFITM3 mediates neuronal impairments following neonatal immune challenge in mice Glia 61 2013 679 693
88. G. Rajkowska, L.D. Selemon, and P.S. Goldman-Rakic Neuronal and glial somal size in the prefrontal cortex: A postmortem morphometric study of schizophrenia and Huntington disease Arch Gen Psychiatry 55 1998 215 224
89. M. Beneyto, and J.H. Meador-Woodruff Lamina-specific abnormalities of AMPA receptor trafficking and signaling molecule transcripts in the prefrontal cortex in schizophrenia Synapse 60 2006 585 598
90. W.B. Ruzicka, A. Zhubi, M. Veldic, D.R. Grayson, E. Costa, and A. Guidotti Selective epigenetic alteration of layer I GABAergic neurons isolated from prefrontal cortex of schizophrenia patients using laser-assisted microdissection Mol Psychiatry 12 2007 385 397
91. S. Akbarian, J.J. Kim, S.G. Potkin, J.O. Hagman, A. Tafazzoli, and W.E. Bunney Jr et al. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics Arch Gen Psychiatry 52 1995 258 266
92. C.L. Beasley, Z.J. Zhang, I. Patten, and 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
93. J.R. Glausier, and D.A. Lewis Selective pyramidal cell reduction of GABA(A) receptor alpha1 subunit messenger RNA expression in schizophrenia Neuropsychopharmacology 36 2011 2103 2110
94. Wu JQ, Wang X, Beveridge NJ, Tooney PA, Scott RJ, Carr VJ, et al. (2012): Transcriptome sequencing revealed significant alteration of cortical promoter usage and splicing in schizophrenia. PLoS One 7:e36351.
95. K. Garbett, P.J. Ebert, A. Mitchell, C. Lintas, B. Manzi, and K. Mirnics et al. Immune transcriptome alterations in the temporal cortex of subjects with autism Neurobiol Dis 30 2008 303 311