Enhanced interaction among ErbB4, PSD-95 and NMDAR by chronic MK-801 treatment is associated with behavioral abnormalities

Pharmacology Biochemistry and Behavior

Volumn 108, Issue , 2013, Pages 44-53

  Li, Ji Tao ^a   Feng, Yu ^a   Su, Yun Ai ^a   Wang, Xiao Dong ^a   Si, Tian Mei ^a  

^a PEKING UNIVERSITY SIXTH HOSPITAL   (China)

Author keywords

ErbB4; Immunoprecipitation; NMDA receptor; NRG1; Schizophrenia

Indexed keywords

DIZOCILPINE; EPIDERMAL GROWTH FACTOR RECEPTOR 4; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOPRECIPITATION; LOCOMOTION; MALE; MEMORY; MOLECULAR INTERACTION; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PREPULSE INHIBITION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RECOGNITION; SPATIAL MEMORY; STARTLE REFLEX; WESTERN BLOTTING;

ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; DIZOCILPINE MALEATE; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LOCOMOTION; MALE; MEMBRANE PROTEINS; MEMORY; PROTEIN BINDING; RATS; RATS, WISTAR; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, N-METHYL-D-ASPARTATE;

RATTUS; RATTUS NORVEGICUS;

EID: 84877616370     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2013.04.008     Document Type: Article

References (61)

1. Z. Abdul-Monim, J.C. Neill, and G.P. Reynolds Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat J Psychopharmacol 21 2007 198 205 (Pubitemid 46280471)
2. A.M. Achim, M. Maziade, E. Raymond, D. Olivier, C. Merette, and M.A. Roy How prevalent are anxiety disorders in schizophrenia? A meta-analysis and critical review on a significant association Schizophr Bull 37 2011 811 821
3. N. Amitai, R. Kuczenski, M.M. Behrens, and A. Markou Repeated phencyclidine administration alters glutamate release and decreases GABA markers in the prefrontal cortex of rats Neuropharmacology 62 2012 1422 1431
4. M.C. Audet, S. Goulet, and F.Y. Dore Enhanced anxiety follows withdrawal from subchronic exposure to phencyclidine in rats Behav Brain Res 176 2007 358 361 (Pubitemid 44880095)
5. P.C. Baier, A. Blume, J. Koch, A. Marx, G. Fritzer, and J.B. Aldenhoff Early postnatal depletion of NMDA receptor development affects behaviour and NMDA receptor expression until later adulthood in rats - a possible model for schizophrenia Behav Brain Res 205 2009 96 101
6. I. Balderas, C.J. Rodriguez-Ortiz, P. Salgado-Tonda, J. Chavez-Hurtado, J.L. McGaugh, and F. Bermudez-Rattoni The consolidation of object and context recognition memory involve different regions of the temporal lobe Learn Mem 15 2008 618 624
7. A. Banerjee, M.L. Macdonald, K.E. Borgmann-Winter, and C.G. Hahn Neuregulin 1-erbB4 pathway in schizophrenia: from genes to an interactome Brain Res Bull 83 2010 132 139
8. A. Barbon, F. Fumagalli, L. La Via, L. Caracciolo, G. Racagni, and M.A. Riva Chronic phencyclidine administration reduces the expression and editing of specific glutamate receptors in rat prefrontal cortex Exp Neurol 208 2007 54 62 (Pubitemid 47600147)
9. R.J. Beninger, J.K. Forsyth, M. Van Adel, J.N. Reynolds, R.J. Boegman, and K. Jhamandas Subchronic MK-801 behavioural deficits in rats: partial reversal by the novel nitrate GT 1061 Pharmacol Biochem Behav 91 2009 495 502
10. S. Beraki, R. Diaz-Heijtz, F. Tai, and S.O. Ogren Effects of repeated treatment of phencyclidine on cognition and gene expression in C57BL/6 mice Int J Neuropsychopharmacol 12 2009 243 255
11. R.A. Bevins, and J. Besheer Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory' Nat Protoc 1 2006 1306 1311
12. M. Bjarnadottir, D.L. Misner, S. Haverfield-Gross, S. Bruun, V.G. Helgason, and H. Stefansson Neuregulin1 (NRG1) signaling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1 ± knock-outs compared with wild-type mice J Neurosci 27 2007 4519 4529 (Pubitemid 46663586)
13. D.L. Braff, R. Freedman, N.J. Schork, and I.I. Gottesman Deconstructing schizophrenia: an overview of the use of endophenotypes in order to understand a complex disorder Schizophr Bull 33 2007 21 32 (Pubitemid 46026257)
14. A. Buonanno The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits Brain Res Bull 83 2010 122 131
15. A. Buonanno, and G.D. Fischbach Neuregulin and ErbB receptor signaling pathways in the nervous system Curr Opin Neurobiol 11 2001 287 296 (Pubitemid 32524093)
16. Y.J. Chen, M.A. Johnson, M.D. Lieberman, R.E. Goodchild, S. Schobel, and N. Lewandowski Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components J Neurosci 28 2008 6872 6883
17. V.Z. Chong, M. Thompson, S. Beltaifa, M.J. Webster, A.J. Law, and C.S. Weickert Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients Schizophr Res 100 2008 270 280
18. J.T. Coyle, G. Tsai, and D. Goff Converging evidence of NMDA receptor hypofunction in the pathophysiology of schizophrenia Ann N Y Acad Sci 1003 2003 318 327 (Pubitemid 38083065)
19. R. Dall'Olio, O. Gandolfi, and N. Montanaro Effect of chronic treatment with dizocilpine (MK-801) on the behavioral response to dopamine receptor agonists in the rat Psychopharmacology (Berl) 107 1992 591 594
20. B. Dean, T. Karl, G. Pavey, S. Boer, L. Duffy, and E. Scarr Increased levels of serotonin 2A receptors and serotonin transporter in the CNS of neuregulin 1 hypomorphic/mutant mice Schizophr Res 99 2008 341 349 (Pubitemid 351249119)
21. S.L. Dix, and J.P. Aggleton Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition Behav Brain Res 99 1999 191 200 (Pubitemid 29083445)
22. T.M. du Bois, K.A. Newell, and X.F. Huang Perinatal phencyclidine treatment alters neuregulin 1/erbB4 expression and activation in later life Eur Neuropsychopharmacol 22 2012 356 363
23. T. Enomoto, and S.B. Floresco Disruptions in spatial working memory, but not short-term memory, induced by repeated ketamine exposure Prog Neuropsychopharmacol Biol Psychiatry 33 2009 668 675
24. D.L. Falls Neuregulins: functions, forms, and signaling strategies Exp Cell Res 284 2003 14 30 (Pubitemid 36335807)
25. Y. Feng, X.D. Wang, C.M. Guo, Y. Yang, J.T. Li, and Y.A. Su Expressions of neuregulin 1beta and ErbB4 in prefrontal cortex and hippocampus of a rat schizophrenia model induced by chronic MK-801 administration J Biomed Biotechnol 2010 2010 859516
26. R.A. Garcia, K. Vasudevan, and A. Buonanno The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses Proc Natl Acad Sci USA 97 2000 3596 3601 (Pubitemid 30183348)
27. D.A. Gearhart, M.L. Middlemore, and A.V. Terry ELISA methods to measure cholinergic markers and nerve growth factor receptors in cortex, hippocampus, prefrontal cortex, and basal forebrain from rat brain J Neurosci Methods 150 2006 159 173 (Pubitemid 43144453)
28. M.A. Geyer Assessing prepulse inhibition of startle in wild-type and knockout mice Psychopharmacology (Berl) 147 1999 11 13 (Pubitemid 30010012)
29. Z. Gu, Q. Jiang, A.K. Fu, N.Y. Ip, and Z. Yan Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex J Neurosci 25 2005 4974 4984 (Pubitemid 40712840)
30. C.G. Hahn, H.Y. Wang, D.S. Cho, K. Talbot, R.E. Gur, and W.H. Berrettini Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia Nat Med 12 2006 824 828 (Pubitemid 44050073)
31. P.J. Harrison, and A.J. Law Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology Biol Psychiatry 60 2006 132 140
32. K. Hashimoto, and Y. Fujita Phencyclidine-induced cognitive deficits in mice are improved by subsequent subchronic administration of clozapine, but not haloperidol Eur J Pharmacol 519 2005 114 117 (Pubitemid 43181173)
33. T. Hori, S. Subramaniam, L.K. Srivastava, and R. Quirion Behavioral and neurochemical alterations following repeated phencyclidine administration in rats with neonatal ventral hippocampal lesions Neuropharmacology 39 2000 2478 2491 (Pubitemid 30642791)
34. Y.Z. Huang, S. Won, D.W. Ali, Q. Wang, M. Tanowitz, and Q.S. Du Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses Neuron 26 2000 443 455
35. J.D. Jentsch, and R.H. Roth The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia Neuropsychopharmacology 20 1999 201 225 (Pubitemid 29067401)
36. K. Kawabe, and E. Miyamoto Effects of neonatal repeated MK-801 treatment on delayed nonmatching-to-position responses in rats Neuroreport 19 2008 969 973
37. K. Kawabe, T. Iwasaki, and Y. Ichitani Repeated treatment with N-methyl-d-aspartate antagonists in neonatal, but not adult, rats causes long-term deficits of radial-arm maze learning Brain Res 1169 2007 77 86 (Pubitemid 47374093)
38. H.C. Kornau, L.T. Schenker, M.B. Kennedy, and P.H. Seeburg Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95 Science 269 1995 1737 1740
39. O.B. Kwon, M. Longart, D. Vullhorst, D.A. Hoffman, and A. Buonanno Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses J Neurosci 25 2005 9378 9383 (Pubitemid 41464750)
40. J.T. Li, Y.A. Su, C.M. Guo, Y. Feng, Y. Yang, and R.H. Huang Persisting cognitive deficits induced by low-dose, subchronic treatment with MK-801 in adolescent rats Eur J Pharmacol 652 2011 65 72
41. L.E. Long, D.T. Malone, and D.A. Taylor Cannabidiol reverses MK-801-induced disruption of prepulse inhibition in mice Neuropsychopharmacology 31 2006 795 803
42. S. Mandillo, A. Rinaldi, A. Oliverio, and A. Mele Repeated administration of phencyclidine, amphetamine and MK-801 selectively impairs spatial learning in mice: a possible model of psychotomimetic drug-induced cognitive deficits Behav Pharmacol 14 2003 533 544 (Pubitemid 38293514)
43. L. Mei, and W.C. Xiong Neuregulin 1 in neural development, synaptic plasticity and schizophrenia Nat Rev Neurosci 9 2008 437 452 (Pubitemid 351704944)
44. A. Mele, C. Castellano, and A. Oliverio Chronic treatment with MK-801 affects the behavioral response to both D1 and D2 dopamine agonist in the one-trial inhibitory avoidance Psychopharmacology (Berl) 121 1995 401 405
45. B. Moghaddam Bringing order to the glutamate chaos in schizophrenia Neuron 40 2003 881 884 (Pubitemid 37522046)
46. S. Nakamura, N. Murayama, T. Noshita, R. Katsuragi, and T. Ohno Cognitive dysfunction induced by sequential injection of amyloid-beta and ibotenate into the bilateral hippocampus; protection by memantine and MK-801 Eur J Pharmacol 548 2006 115 122 (Pubitemid 44404130)
47. J. O'Donnell, J. Stemmelin, and A. Nitta Gene expression profiling following chronic NMDA receptor blockade-induced learning deficits in rats Synapse 50 2003 171 180 (Pubitemid 37315347)
48. T.A. Paine, and W.A. Carlezon Jr. Effects of antipsychotic drugs on MK-801-induced attentional and motivational deficits in rats Neuropharmacology 56 2009 788 797
49. G.M. Pitcher, L.V. Kalia, D. Ng, N.M. Goodfellow, K.T. Yee, and E.K. Lambe Schizophrenia susceptibility pathway neuregulin 1-ErbB4 suppresses Src upregulation of NMDA receptors Nat Med 17 2011 470 478
50. J.P. Redrobe, L. Elster, K. Frederiksen, C. Bundgaard, I.E. de Jong, and G.P. Smith Negative modulation of GABA(A) alpha5 receptors by RO4938581 attenuates discrete sub-chronic and early postnatal phencyclidine (PCP)-induced cognitive deficits in rats Psychopharmacology (Berl) 221 2012 451 468
51. D. Rujescu, A. Bender, and M. Keck Pharmacological model for psychosis based on N-methyl-d-aspartate receptor hypofunction: molecular, cellular, functional and behavioral abnormalities Biol Psychiatry 59 2006 721 729
52. K. Schwabe, J. Brosda, N. Wegener, and M. Koch Clozapine enhances disruption of prepulse inhibition after sub-chronic dizocilpine- or phencyclidine-treatment in Wistar rats Pharmacol Biochem Behav 80 2005 213 219 (Pubitemid 40170419)
53. A. Seillier, and A. Giuffrida Evaluation of NMDA receptor models of schizophrenia: divergences in the behavioral effects of sub-chronic PCP and MK-801 Behav Brain Res 204 2009 410 415
54. M.S. Seo, S.H. Kim, Y.M. Ahn, Y. Kim, W.J. Jeon, and S.C. Yoon The effects of repeated administrations of MK-801 on ERK and GSK-3beta signalling pathways in the rat frontal cortex Int J Neuropsychopharmacol 10 2007 359 368 (Pubitemid 46701004)
55. S.M. Simpson, J.L. Menard, J.N. Reynolds, and R.J. Beninger Post-weaning social isolation increases activity in a novel environment but decreases defensive burying and subchronic MK-801 enhances the activity but not the burying effect in rats Pharmacol Biochem Behav 95 2010 72 79
56. C.W. Smith, S. Park, and B. Cornblatt Spatial working memory deficits in adolescents at clinical high risk for schizophrenia Schizophr Res 81 2006 211 215 (Pubitemid 43107695)
57. M.R. Stefani, and B. Moghaddam Transient N-methyl-d-aspartate receptor blockade in early development causes lasting cognitive deficits relevant to schizophrenia Biol Psychiatry 57 2005 433 436 (Pubitemid 40215775)
58. Y.A. Su, X.D. Wang, J.T. Li, C.M. Guo, Y. Feng, and Y. Yang Age-specific effects of early MK-801 treatment on working memory in female rats Neuroreport 22 2011 402 406
59. C.V. Vorhees, and M.T. Williams Morris water maze: procedures for assessing spatial and related forms of learning and memory Nat Protoc 1 2006 848 858
60. L. Wen, Y.S. Lu, X.H. Zhu, X.M. Li, R.S. Woo, and Y.J. Chen Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons Proc Natl Acad Sci USA 107 2010 1211 1216
61. B. Yu, C. Wang, J. Liu, K.M. Johnson, and J.P. Gallagher Adaptation to chronic PCP results in hyperfunctional NMDA and hypofunctional GABA(A) synaptic receptors Neuroscience 113 2002 1 10 (Pubitemid 34786006)