Abstract
Neuregulin-1 (NRG1) and its ErbB2/B4 receptors are encoded by candidate susceptibility genes for schizophrenia, yet the essential functions of NRG1 signaling in the CNS are still unclear. Using CRE/LOX technology, we have inactivated ErbB2/B4-mediated NRG1 signaling specifically in the CNS. In contrast to expectations, cell layers in the cerebral cortex, hippocampus, and cerebellum develop normally in the mutant mice. Instead, loss of ErbB2/B4 impairs dendritic spine maturation and perturbs interactions of postsynaptic scaffold proteins with glutamate receptors. Conversely, increased NRG1 levels promote spine maturation. ErbB2/B4-deficient mice show increased aggression and reduced prepulse inhibition. Treatment with the antipsychotic drug clozapine reverses the behavioral and spine defects. We conclude that ErbB2/B4-mediated NRG1 signaling modulates dendritic spine maturation, and that defects at glutamatergic synapses likely contribute to the behavioral abnormalities in ErbB2/B4-deficient mice.
MeSH Terms
Adaptor Proteins, Signal Transducing
Animals
Antipsychotic Agents/pharmacology
Central Nervous System
Cerebral Cortex/cytology
Clozapine/pharmacology
Dendritic Spines/pathology
Mice
Mice, Knockout
Nerve Tissue Proteins/deficiency,physiology
Neuregulin-1
Oncogene Proteins v-erbB/deficiency,physiology
Receptor, ErbB-2/physiology
Receptors, Glutamate
Signal Transduction
Chemicals
Adaptor Proteins, Signal Transducing
Antipsychotic Agents
Nerve Tissue Proteins
Neuregulin-1
Nrg1 protein, mouse
Oncogene Proteins v-erbB
Receptors, Glutamate
Receptor, ErbB-2
Clozapine
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Barros Claudia S
Department of Cell Biology, Institute of Childhood and Neglected Disease, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
Calabrese Barbara
Chamero Pablo
Roberts Amanda J
Korzus Ed
Lloyd Kent
Stowers Lisa
Mayford Mark
Halpain Shelley
Müller Ulrich
References (32)
32 references, click to expand
-
Erbb2 regulates neuromuscular synapse formation and is essential for muscle spindle development.
Development. 2003 Jun;130(11):2291-301
PMID: 12702645
-
Erbin is a protein concentrated at postsynaptic membranes that interacts with PSD-95.
J Biol Chem. 2001 Jun 1;276(22):19318-26
PMID: 11279080
-
Schizophrenia.
Curr Biol. 2005 Dec 20;15(24):R980-4
PMID: 16360673
-
CBP histone acetyltransferase activity is a critical component of memory consolidation.
Neuron. 2004 Jun 24;42(6):961-72
PMID: 15207240
-
A forward genetics screen in mice identifies recessive deafness traits and reveals that pejvakin is essential for outer hair cell function.
J Neurosci. 2007 Feb 28;27(9):2163-75
PMID: 17329413
-
Requirement for neuregulin receptor erbB2 in neural and cardiac development.
Nature. 1995 Nov 23;378(6555):394-8
PMID: 7477377
-
Multiple essential functions of neuregulin in development.
Nature. 1995 Nov 23;378(6555):386-90
PMID: 7477375
-
Promiscuous interactions between AMPA-Rs and MAGUKs.
Neuron. 2006 Oct 19;52(2):222-4
PMID: 17046684
-
Atypical antipsychotic agents in the treatment of violent patients with schizophrenia and schizoaffective disorder.
Arch Gen Psychiatry. 2006 Jun;63(6):622-9
PMID: 16754835
-
Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage.
J Neurosci. 2002 Aug 1;22(15):6309-14
PMID: 12151506
-
Interactions among genes in the ErbB-Neuregulin signalling network are associated with increased susceptibility to schizophrenia.
Behav Brain Funct. 2007 Jun 28;3:31
PMID: 17598910
-
Neuregulin 1 in neural development, synaptic plasticity and schizophrenia.
Nat Rev Neurosci. 2008 Jun;9(6):437-52
PMID: 18478032
-
Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses.
Neuron. 2000 May;26(2):443-55
PMID: 10839362
-
Sex differences in prepulse inhibition deficits in chronic schizophrenia.
Schizophr Res. 2004 Aug 1;69(2-3):219-35
PMID: 15469195
-
Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5.
Development. 2003 Nov;130(21):5257-68
PMID: 12954715
-
Progenitor cell maintenance requires numb and numblike during mouse neurogenesis.
Nature. 2002 Oct 31;419(6910):929-34
PMID: 12410312
-
Neuregulin 1-erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex.
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4251-6
PMID: 12649319
-
Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor.
Nature. 1995 Nov 23;378(6555):390-4
PMID: 7477376
-
hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo.
Genesis. 2001 Oct;31(2):85-94
PMID: 11668683
-
Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex.
Neuron. 2001 Aug 16;31(3):367-79
PMID: 11516395
-
Impact of prepulse characteristics on the detection of sensorimotor gating deficits in schizophrenia.
Schizophr Res. 2001 Apr 15;49(1-2):171-8
PMID: 11343875
-
Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex.
Development. 1997 Sep;124(18):3501-10
PMID: 9342043
-
Susceptibility genes for schizophrenia: characterisation of mutant mouse models at the level of phenotypic behaviour.
Neurosci Biobehav Rev. 2007;31(1):60-78
PMID: 16782199
-
Neuregulin and erbB receptors play a critical role in neuronal migration.
Neuron. 1997 Jul;19(1):39-50
PMID: 9247262
-
Essential role for the PKC target MARCKS in maintaining dendritic spine morphology.
Neuron. 2005 Oct 6;48(1):77-90
PMID: 16202710
-
Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain.
Cell. 2006 Oct 6;127(1):185-97
PMID: 17018285
-
Genesis of dendritic spines: insights from ultrastructural and imaging studies.
Nat Rev Neurosci. 2004 Jan;5(1):24-34
PMID: 14708001
-
The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity.
Neuron. 2007 May 24;54(4):583-97
PMID: 17521571
-
Mitotic spindle regulation by Nde1 controls cerebral cortical size.
Neuron. 2004 Oct 14;44(2):279-93
PMID: 15473967
-
ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice.
Development. 1997 Dec;124(24):4999-5011
PMID: 9362461
-
Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins.
Neuron. 2006 Oct 19;52(2):307-20
PMID: 17046693
-
Neuregulin 1 and susceptibility to schizophrenia.
Am J Hum Genet. 2002 Oct;71(4):877-92
PMID: 12145742