Social isolation exacerbates schizophrenia-like phenotypes via oxidative stress in cortical interneurons

Biological Psychiatry

Volumn 73, Issue 10, 2013, Pages 1024-1034

  Jiang, Zhihong ^a   Rompala, Gregory R ^a   Zhang, Shuqin ^a   Cowell, Rita M ^b   Nakazawa, Kazu ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Interneuron; NMDA receptor hypofunction; oxidative stress; parvalbumin; PGC 1 ; schizophrenia; social isolation; transgenic mice

Indexed keywords

4 AMINOBUTYRIC ACID; APOCYNIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PARVALBUMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DISEASE EXACERBATION; FEMALE; INTERNEURON; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; SCHIZOPHRENIA; SOCIAL ISOLATION;

ACETOPHENONES; ANIMALS; ANTIOXIDANTS; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; HUMANS; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OXIDATIVE STRESS; PARVALBUMINS; PHENOTYPE; PROTEINS; REACTIVE OXYGEN SPECIES; RECEPTORS, AMPA; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SOCIAL ISOLATION; SUPEROXIDE DISMUTASE;

EID: 84876900043     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.12.004     Document Type: Article

References (56)

1. D.W. Fulker A biometrical genetic approach to intelligence and schizophrenia Soc Biol 20 1973 266 275
2. A.G. Cardno, and I.I. Gottesman Twin studies of schizophrenia: From bow-and-arrow concordances to star wars Mx and functional genomics Am J Med Genet 97 2000 12 17
3. W. Veling, and E. Susser Migration and psychotic disorders Expert Rev Neurother 11 2011 65 76
4. S. Schiavone, S. Sorce, M. Dubois-Dauphin, V. Jaquet, M. Colaianna, and M. Zotti Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats Biol Psychiatry 66 2009 384 392
5. M. Möller, J.L. Du Preez, R. Emsley, and B.H. Harvey Isolation rearing-induced deficits in sensorimotor gating and social interaction in rats are related to cortico-striatal oxidative stress, and reversed by sub-chronic clozapine administration Eur Neuropsychopharmacol 21 2011 471 483
6. K.Q. Do, J.-H. Cabungcal, A. Frank, P. Steullet, and M. Cuenod Redox dysregulation, neurodevelopment, and schizophrenia Curr Opin Neurobiol 19 2009 220 230
7. J.K. Yao, and M.S. Keshavan Antioxidants, redox signaling, and pathophysiology in schizophrenia: An integrative view Antioxid Redox Signal 15 2011 2011 2035
8. R. Reddy, M.P. Sahebarao, S. Mukherjee, and J.N. Murthy Enzymes of the antioxidant defense system in chronic schizophrenic patients Biol Psychiatry 30 1991 409 412
9. S. Mukerjee, S.P. Mahadik, R. Scheffer, E.E. Correnti, and H. Kelkar Impaired antioxidant defense at the onset of psychosis Schizophr Res 19 1996 19 26
10. J.M. Coughlin, K. Ishizuka, S.I. Kano, J.A. Edwards, F.T. Seifuddin, and M.A. Shimano Marked reduction of soluble superoxide dismutase-1 (SOD1) in cerebrospinal fluid of patients with recent-onset schizophrenia Mol Psychiatry 18 2013 10 11
11. S.B. Powell, T.J. Sejnowski, and M.M. Behrens Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin- interneuron maturation in rodent models of schizophrenia Neuropharmacology 62 2012 1322 1331
12. N.V. Radonjić, I.D. Knezević, U. Vilimanovich, T. Kravić-Stevović, L.V. Marina, and T. Nikolić Decreased glutathione levels and altered antioxidant defense in an animal model of schizophrenia: Long-term effects of perinatal phencyclidine administration Neuropharmacology 58 2010 739 745
13. M.M. Behrens, S.S. Ali, D.N. Dao, J. Lucero, G. Shekhtman, and K.L. Quick Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase Science 318 2007 1645 1647
14. Y. Zhang, M.M. Behrens, and J.E. Lisman Prolonged exposure to NMDAR antagonist suppresses inhibitory synaptic transmission in prefrontal cortex J Neurophysiol 100 2008 959 965
15. J.E. Belforte, V. Zsiros, E.R. Sklar, Z. Jiang, G. Yu, and Y. Li Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes Nat Neurosci 13 2010 76 83
16. M.T. Dang, F. Yokoi, H.H. Yin, D.M. Lovinger, Y. Wang, and Y. Li Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum Proc Natl Acad Sci U S A 103 2006 15254 15259
17. M.M. Harraz, J.J. Marden, W. Zhou, Y. Zhang, A. Williams, and V.S. Sharov SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model J Clin Invest 118 2008 659 670
18. S. Heumüller, S. Wind, E. Barbosa-Sicard, H.H. Schmidt, R. Busse, and K. Schröder Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 51 2008 211 217
19. J.M. Simons, B.A. Hart, T.R. Ip Vai Ching, D.H. Van, and R.P. Labadie Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils Free Radic Biol Med 8 1990 251 258
20. C. Tanahira, S. Higo, K. Watanabe, R. Tomioka, S. Ebihara, and T. Kaneko Parvalbumin neurons in the forebrain as revealed by parvalbumin-Cre transgenic mice Neurosci Res 63 2009 213 223
21. L. Benov, L. Sztejnberg, and I. Fridovich Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical Free Radic Biol Med 25 1998 826 831
22. J. Lin, C. Handschin, and B.M. Spiegelman Metabolic control through the PGC-1 family of transcription coactivators Cell Metab 1 2005 361 370
23. J. St-Pierre, S. Drori, M. Uldry, J.M. Silvaggi, J. Rhee, and S. Jäger Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 127 2006 397 408
24. E.K. Lucas, S.J. Markwardt, S. Gupta, J.H. Meador-Woodruff, J.D. Lin, and L. Overstreet-Wadiche Parvalbumin deficiency and GABAergic dysfunction in mice lacking PGC-1α J Neurosci 30 2010 7227 7235
25. I. Soltesz, and M. Deschênes Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia J Neurophysiol 70 1993 97 116
26. T. Klausberger, P.J. Magill, L.F. Márton, J.D. Roberts, P.M. Cobden, and G. Buzsáki Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo Nature 421 2003 844 848
27. N. Hajos, J. Palhalmi, E.O. Mann, B. Nemeth, O. Paulsen, and T.F. Freund Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro J Neurosci 24 2004 9127 9137
28. M.O. Cunningham, J. Hunt, S. Middleton, F.E. LeBeau, M.J. Gillies, and C.H. Davies Region-specific reduction in entorhinal gamma oscillations and parvalbumin-immunoreactive neurons in animal models of psychiatric illness J Neurosci 26 2006 2767 2776
29. A.I. Gulyás, G. Buzsáki, T.F. Freund, and H. Hirase Populations of hippocampal inhibitory neurons express different levels of cytochrome c Eur J Neurosci 23 2006 2581 2594
30. B. Czeh, M. Simon, M.G. van der Hart, B. Schmelting, M.B. Hesselink, and E. Fuchs Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: prevention by treatment with a substance P receptor (NK1) antagonist Neuropsychopharmacology 30 2005 67 79
31. W. Hu, M. Zhang, B. Czéh, G. Flügge, and W. Zhang Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin- expressing neuronal network Neuropsychopharmacology 35 2010 1693 1707
32. R.M. Cowell, K.R. Blake, and J.W. Russell Localization of the transcriptional coactivator PGC-1α to GABAergic neurons during maturation of the rat brain J Comp Neurol 502 2007 1 18
33. H. Meng, H.L. Liang, and M. Wong-Riley Quantitative immuno-electron microscopic analysis of depolarization-induced expression of PGC-1α in cultured rat visual cortical neurons Brain Res 1175 2007 10 16
34. Y. Luo, W. Zhu, J. Jia, C. Zhang, and Y. Xu NMDA receptor dependent PGC-1α up-regulation protects the cortical neuron against oxygen-glucose deprivation/reperfusion injury J Mol Neurosci 39 2009 262 268
35. H.L. Liang, S.S. Dhar, and M.T. Wong-Riley p38 mitogen-activated protein kinase and calcium channels mediate signaling in depolarization-induced activation of peroxisome proliferator-activated receptor gamma coactivator-1α in neurons J Neurosci Res 88 2010 640 649
36. H.L. Liang, and M.T. Wong-Riley Activity-dependent regulation of nuclear respiratory factor-1, nuclear respiratory factor-2, and peroxisome proliferatoractivated receptor gamma coactivator-1 in neurons Neuroreport 17 2006 401 405
37. P.H. Patterson Immune involvement in schizophrenia and autism: Etiology, pathology and animal models Behav Brain Res 204 2009 313 321
38. U. Meyer Developmental neuroinflammation and schizophrenia [published online ahead of print November 15] Prog Neuropsychopharmacol Biol Psychiatry. 2011 doi: 10.1016/j.pnpbp.2011.11.003
39. T.A. Bayer, R. Buslei, L. Havas, and P. Falkai Evidence for activation of microglia in patients with psychiatric illnesses Neurosci Lett 271 1999 126 128
40. K. Radewicz, L.J. Garey, S.M. Gentleman, and R. Reynolds Increase in HLA-DR immunoreactive microglia in frontal and temporal cortex of chronic schizophrenics J Neuropathol Exp Neurol 59 2000 137 150
41. J. Steiner, C. Mawrin, A. Ziegeler, H. Bielau, O. Ullrich, and H.G. Bernstein Distribution of HLA-DR-positive microglia in schizophrenia reflects impaired cerebral lateralization Acta Neuropathol 112 2006 305 316
42. J. Steiner, H. Bielau, R. Brisch, P. Danos, O. Ullrich, and C. Mawrin Immunological aspects in the neurobiology of suicide: Elevated microglial density in schizophrenia and depression is associated with suicide J Psychiatr Res 42 2008 151 157
43. 11C]PK11195 positron emission tomography study Biol Psychiatry 64 2008 820 822
44. M.M. Behrens, S.S. Ali, and L.L. Dugan Interleukin-6 mediates the increase in NADPH-oxidase in the ketamine model of schizophrenia J Neurosci 28 2008 13957 13966
45. S. Sorce, S. Schiavone, P. Tucci, M. Colaianna, V. Jaquet, and V. Cuomo The NADPH oxidase NOX2 controls glutamate release: A novel mechanism involved in psychosis-like ketamine responses J Neurosci 30 2010 11317 11325
46. I. Takac, K. Schröder, L. Zhang, B. Lardy, N. Anilkumar, and J.D. Lambeth The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4 J Biol Chem 286 2011 13304 13313
47. C.C. Winterbourn Reconciling the chemistry and biology of reactive oxygen species Nat Chem Biol 4 2008 278 286
48. A.S. Brown The environment and susceptibility to schizophrenia Prog Neurobiol 93 2011 23 58
49. D.H. Blackwood, L. He, S.W. Morris, A. McLean, C. Whitton, and M. Thomson A locus for bipolar affective disorder on chromosome 4p Nat Genet 12 1996 427 430
50. A. Christoforou, S.L. Hellard, P.A. Thomson, S.W. Morris, A. Tenesa, and B.S. Pickard Association analysis of the chromosome 4p15-p16 candidate region for bipolar and schizophrenia Mol Psychiatry 12 2007 1011 1025
51. A. Christoforou, K.A. McGhee, S.W. Morris, P.A. Thomson, S. Anderson, and A. McLean Convergence of linkage, association and GWAS findings for a candidate region for bipolar disorder and schizophrenia on chromosome 4p Mol Psychiatry 16 2010 240 242
52. Y.H. Hsiao, P.S. Chen, S.H. Chen, and P.W. Gean The involvement of Cdk5 activator p35 in social isolation-triggered onset of early Alzheimer's disease-related cognitive deficit in the transgenic mice Neuropsychopharmacology 36 2011 1848 1858
53. G. Hermes, N. Li, C. Duman, and R. Duman Post-weaning chronic social isolation produces profound behavioral dysregulation with decreases in prefrontal cortex synaptic-associated protein expression in female rats Physiol Behav 104 2011 354 359
54. K.C.F. Fone, and M.V. Porkess Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders Neurosci Biobehav Rev 32 2008 1087 1102
55. K.H. Nuechterlein, and M.E. Dawson A heuristic vulnerability/stress model of schizophrenic episodes Schizophr Bull 10 1984 300 312
56. T.A. Bayer, P. Falkai, and W. Maier Genetic and non-genetic vulnerability factors in schizophrenia: The basis of the two hit hypothesis J Psychiatr Res 33 1999 543 548