Neuregulin 1 in neural development, synaptic plasticity and schizophrenia (original) (raw)

• Carlsson, A. & Lindqvist, M. Effect of chlorpromazine or haloperidol on formation of 3methoxytyramine and normetanephrine in mouse brain. Acta Pharmacol. Toxicol. 20, 140–144 (1963).
  CAS Google Scholar
• Laruelle, M. & Abi-Dargham, A. Dopamine as the wind of the psychotic fire: new evidence from brain imaging studies. J. Psychopharmacol. 13, 358–371 (1999).
  CAS PubMed Google Scholar
• Harrison, P. J. & Weinberger, D. R. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry 10, 40–68 (2005).
  CAS PubMed Google Scholar
• Tan, W. et al. Molecular cloning of a brain-specific, developmentally regulated neuregulin 1 (NRG1) isoform and identification of a functional promoter variant associated with schizophrenia. J. Biol. Chem. 282, 24343–24351 (2007).
  CAS PubMed Google Scholar
• Falls, D. L. Neuregulins: functions, forms, and signalling strategies. Exp. Cell Res. 284, 14–30 (2003).
  CAS PubMed Google Scholar
• Steinthorsdottir, V. et al. Multiple novel transcription initiation sites for NRG1. Gene 342, 97–105 (2004).
  CAS PubMed Google Scholar
• Meyer, D. et al. Isoform-specific expression and function of neuregulin. Development 124, 3575–3586 (1997). This study was the first to show that NRG1 isoforms have distinct functions in neural development. Type I NRG1 is required for the generation of neural-crest-derived neurons in the cranial ganglia, whereas Type III NRG1 has an important role in glial-cell development.
  CAS PubMed Google Scholar
• Harrison, P. J. & Law, A. J. Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol. Psychiatry 60, 132–140 (2006).
  CAS PubMed Google Scholar
• Peles, E. et al. Isolation of the Neu/HER-2 stimulatory ligand: a 44 kd glycoprotein that induces differentiation of mammary tumour cells. Cell 69, 205–216 (1992).
  CAS PubMed Google Scholar
• Holmes, W. E. et al. Identification of heregulin, a specific activator of p185erbB2. Science 256, 1205–1210 (1992).
  CAS PubMed Google Scholar
• Jessell, T. M., Siegel, R. E. & Fischbach, G. D. Induction of acetylcholine receptors on cultured skeletal muscle by a factor extracted from brain and spinal cord. Proc. Natl Acad. Sci. USA 76, 5397–5401 (1979).
  CAS PubMed PubMed Central Google Scholar
• Falls, D. L., Rosen, K. M., Corfas, G., Lane, W. S. & Fischbach, G. D. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the Neu ligand family. Cell 72, 801–815 (1993).
  CAS PubMed Google Scholar
• Raff, M. C., Abney, E., Brockes, J. P. & Hornby-Smith, A. Schwann cell growth factors. Cell 15, 813–822 (1978).
  CAS PubMed Google Scholar
• Lemke, G. E. & Brockes, J. P. Identification and purification of glial growth factor. J. Neurosci. 4, 75–83 (1984).
  CAS PubMed PubMed Central Google Scholar
• Marchionni, M. A. et al. Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362, 312–318 (1993).
  CAS PubMed Google Scholar
• Carraway, K. L. et al. Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinase. Nature 387, 512–516 (1997).
  CAS PubMed Google Scholar
• Fischbach, G. D. & Rosen, K. M. ARIA: a neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20, 429–458 (1997).
  CAS PubMed Google Scholar
• Kramer, R. et al. Neuregulins with an Ig-like domain are essential for mouse myocardial and neuronal development. Proc. Natl Acad. Sci. USA 93, 4833–4838 (1996).
  CAS PubMed PubMed Central Google Scholar
• Loeb, J. A., Susanto, E. T. & Fischbach, G. D. The neuregulin precursor proARIA is processed to ARIA after expression on the cell surface by a protein kinase C-enhanced mechanism. Mol. Cell. Neurosci. 11, 77–91 (1998).
  CAS PubMed Google Scholar
• Montero, J. C. et al. The extracellular linker of pro-neuregulin-α2c is required for efficient sorting and juxtacrine function. Mol. Biol. Cell 18, 380–393 (2007).
  CAS PubMed PubMed Central Google Scholar
• Hu, X. et al. Bace1 modulates myelination in the central and peripheral nervous system. Nature Neurosci. 9, 1520–1525 (2006).
  CAS PubMed Google Scholar
• Willem, M. et al. Control of peripheral nerve myelination by the β-secretase BACE1. Science 314, 664–666 (2006).
  CAS PubMed Google Scholar
• Yokozeki, T. et al. Meltrin β (ADAM19) mediates ectodomain shedding of Neuregulin β1 in the Golgi apparatus: fluorescence correlation spectroscopic observation of the dynamics of ectodomain shedding in living cells. Genes Cells 12, 329–343 (2007).
  CAS PubMed Google Scholar
• Bao, J., Wolpowitz, D., Role, L. W. & Talmage, D. A. Back signalling by the Nrg-1 intracellular domain. J. Cell Biol. 161, 1133–1141 (2003). This was the first report to indicate a role for NRG1 in backward signalling. Binding of the extracellular domains of ErbB receptors and NRG1 elicits proteolytic release and the translocation of NRG1-ICD to the nucleus.
  CAS PubMed PubMed Central Google Scholar
• Eilam, R., Pinkas-Kramarski, R., Ratzkin, B. J., Segal, M. & Yarden, Y. Activity-dependent regulation of Neu differentiation factor/neuregulin expression in rat brain. Proc. Natl Acad. Sci. USA 95, 1888–1893 (1998).
  CAS PubMed PubMed Central Google Scholar
• Han, B. & Fischbach, G. D. Processing of ARIA and release from isolated nerve terminals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 411–416 (1999).
  CAS PubMed PubMed Central Google Scholar
• Ozaki, M., Itoh, K., Miyakawa, Y., Kishida, H. & Hashikawa, T. Protein processing and releases of neuregulin-1 are regulated in an activity-dependent manner. J. Neurochem. 91, 176–188 (2004).
  CAS PubMed Google Scholar
• Bublil, E. M. & Yarden, Y. The EGF receptor family: spearheading a merger of signalling and therapeutics. Curr. Opin. Cell Biol. 19, 124–134 (2007).
  CAS PubMed Google Scholar
• Tzahar, E. et al. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16, 5276–5287 (1996).
  CAS PubMed PubMed Central Google Scholar
• Guy, P. M., Platko, J. V., Cantley, L. C., Cerione, R. A. & Carraway, K. L. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl Acad. Sci. USA 91, 8132–8136 (1994).
  CAS PubMed PubMed Central Google Scholar
• Gerlai, R., Pisacane, P. & Erickson, S. Heregulin, but not ErbB2 or ErbB3, heterozygous mutant mice exhibit hyperactivity in multiple behavioural tasks. Behav. Brain Res. 109, 219–227 (2000). This report was the first to link abnormal NRG1 signalling to behavioural deficits. Nrg1 hypomorphs, but not Erbb2 or Erbb3 hypomorphs, showed consistent hyperactivity in various behavioural tests.
  CAS PubMed Google Scholar
• Gu, Z., Jiang, Q., Fu, A. K., Ip, N. Y. & Yan, Z. Regulation of NMDA receptors by neuregulin signalling in PFC. J. Neurosci. 25, 4974–4984 (2005).
  CAS PubMed PubMed Central Google Scholar
• Liu, Y., Tao, Y. M., Woo, R. S., Xiong, W. C. & Mei, L. Stimulated ErbB4 internalization is necessary for neuregulin signalling in neurons. Biochem. Biophys. Res. Commun. 354, 505–510 (2007).
  CAS PubMed PubMed Central Google Scholar
• Yang, X. L., Huang, Y. Z., Xiong, W. C. & Mei, L. Neuregulin-induced expression of the acetylcholine receptor requires endocytosis of ErbB receptors. Mol. Cell. Neurosci. 28, 335–346 (2005).
  CAS PubMed Google Scholar
• Si, J., Wang, Q. & Mei, L. Essential roles of c-JUN and c-JUN N-terminal kinase (JNK) in neuregulin-increased expression of the acetylcholine receptor ɛ-subunit. J. Neurosci. 19, 8489–8508 (1999).
  Google Scholar
• Fu, A. K. et al. Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction. Nature Neurosci. 4, 374–381 (2001).
  CAS PubMed Google Scholar
• Yarden, Y. & Sliwkowski, M. X. Untangling the ErbB signalling network. Nature Rev. Mol. Cell Biol. 2, 127–137 (2001).
  CAS Google Scholar
• Bjarnadottir, M. et al. Neuregulin1 (NRG1) signalling through Fyn modulates NMDA receptor phosphorylation: differential synaptic function in NRG1+/− knock-outs compared with wild-type mice. J. Neurosci. 27, 4519–4529 (2007).
  CAS PubMed PubMed Central Google Scholar
• Ni, C. Y., Murphy, M. P., Golde, T. E. & Carpenter, G. γ-secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 2179–2181 (2001).
  CAS PubMed Google Scholar
• Lee, H. J. et al. Presenilin-dependent γ-secretase-like intramembrane cleavage of ErbB4. J. Biol. Chem. 277, 6318–6323 (2002).
  CAS PubMed Google Scholar
• Sardi, S. P., Murtie, J., Koirala, S., Patten, B. A. & Corfas, G. Presenilin-dependent ErbB4 nuclear signalling regulates the timing of astrogenesis in the developing brain. Cell 127, 185–197 (2006). This report showed evidence that ErbB4-ICD, which is released by presenilin-dependent cleavage, regulates gene transcription and cell fate by forming a complex with other regulators.
  CAS PubMed Google Scholar
• Fox, I. J. & Kornblum, H. I. Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions. J. Neurosci. Res. 79, 584–597 (2005).
  CAS PubMed Google Scholar
• Bao, J. et al. Activity-dependent transcription regulation of PSD-95 by neuregulin-1 and Eos. Nature Neurosci. 7, 1250–1258 (2004).
  CAS PubMed Google Scholar
• Harrison, P. J. Schizophrenia: a disorder of neurodevelopment? Curr. Opin. Neurobiol. 7, 285–289 (1997).
  CAS PubMed Google Scholar
• Corfas, G., Rosen, K. M., Aratake, H., Krauss, R. & Fischbach, G. D. Differential expression of ARIA isoforms in the rat brain. Neuron 14, 103–115 (1995).
  CAS PubMed Google Scholar
• Steiner, H., Blum, M., Kitai, S. T. & Fedi, P. Differential expression of ErbB3 and ErbB4 neuregulin receptors in dopamine neurons and forebrain areas of the adult rat. Exp. Neurol. 159, 494–503 (1999).
  CAS PubMed Google Scholar
• Liu, Y., Ford, B. D., Mann, M. A. & Fischbach, G. D. Neuregulin-1 increases the proliferation of neuronal progenitors from embryonic neural stem cells. Dev. Biol. 283, 437–445 (2005).
  CAS PubMed Google Scholar
• Gassmann, M. et al. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 378, 390–394 (1995). This report was the first to demonstrate that ErbB4 is an essential in vivo regulator of the development of the CNS.
  CAS PubMed Google Scholar
• Lee, K. F. et al. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 378, 394–398 (1995).
  CAS PubMed Google Scholar
• Erickson, S. L. et al. ErbB3 is required for normal cerebellar and cardiac development: a comparison with ErbB2-and heregulin-deficient mice. Development 124, 4999–5011 (1997).
  CAS PubMed Google Scholar
• Wolpowitz, D. et al. Cysteine-rich domain isoforms of the Neuregulin-1 gene are required for maintenance of peripheral synapses. Neuron 25, 79–91 (2000).
  CAS PubMed Google Scholar
• Meyer, D. & Birchmeier, C. Multiple essential functions of neuregulin in development. Nature 378, 386–390 (1995).
  CAS PubMed Google Scholar
• Golding, J. P., Trainor, P., Krumlauf, R. & Gassmann, M. Defects in pathfinding by cranial neural crest cells in mice lacking the neuregulin receptor ErbB4. Nature Cell Biol. 2, 103–109 (2000).
  CAS PubMed Google Scholar
• Rio, C., Rieff, H. I., Qi, P., Khurana, T. S. & Corfas, G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19, 39–50 (1997).
  CAS PubMed Google Scholar
• Anton, E. S., Marchionni, M. A., Lee, K. F. & Rakic, P. Role of GGF/neuregulin signalling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124, 3501–3510 (1997).
  CAS PubMed Google Scholar
• Gierdalski, M., Sardi, S. P., Corfas, G. & Juliano, S. L. Endogenous neuregulin restores radial glia in a (ferret) model of cortical dysplasia. J. Neurosci. 25, 8498–8504 (2005).
  CAS PubMed PubMed Central Google Scholar
• Schmid, R. S. et al. Neuregulin 1-erbB2 signalling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc. Natl Acad. Sci. USA 100, 4251–4256 (2003).
  CAS PubMed PubMed Central Google Scholar
• Yau, H. J., Wang, H. F., Lai, C. & Liu, F. C. Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences. Cereb. Cortex 13, 252–264 (2003).
  PubMed Google Scholar
• Flames, N. et al. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44, 251–261 (2004).
  CAS PubMed Google Scholar
• Luskin, M. B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11, 173–189 (1993).
  CAS PubMed Google Scholar
• Anton, E. S. et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nature Neurosci. 7, 1319–1328 (2004).
  CAS PubMed Google Scholar
• Gerecke, K. M., Wyss, J. M. & Carroll, S. L. Neuregulin-1β induces neurite extension and arborization in cultured hippocampal neurons. Mol. Cell. Neurosci. 27, 379–393 (2004).
  CAS PubMed Google Scholar
• Bermingham-McDonogh, O., McCabe, K. L. & Reh, T. A. Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development 122, 1427–1438 (1996).
  CAS PubMed Google Scholar
• Rieff, H. I. et al. Neuregulin induces GABAA receptor subunit expression and neurite outgrowth in cerebellar granule cells. J. Neurosci. 19, 10757–10766 (1999).
  CAS PubMed PubMed Central Google Scholar
• Lopez-Bendito, G. et al. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 125, 127–142 (2006).
  CAS PubMed PubMed Central Google Scholar
• Gamett, D. C. & Cerione, R. A. Oncogenically activated or ligand-stimulated neu kinase stimulates neurite outgrowth in PC12 cells. FEBS Lett. 351, 335–339 (1994).
  CAS PubMed Google Scholar
• Vaskovsky, A., Lupowitz, Z., Erlich, S. & Pinkas-Kramarski, R. ErbB-4 activation promotes neurite outgrowth in PC12 cells. J. Neurochem. 74, 979–987 (2000).
  CAS PubMed Google Scholar
• Pinkas-Kramarski, R. et al. Differential expression of NDF/neuregulin receptors ErbB-3 and ErbB-4 and involvement in inhibition of neuronal differentiation. Oncogene 15, 2803–2815 (1997).
  CAS PubMed Google Scholar
• Maroof, A. M. & Anderson, S. A. Off on a tangent: thalamocortical axons traverse a permissive corridor across the basal telencephalon. Neuron 50, 185–188 (2006).
  CAS PubMed Google Scholar
• Ho, W. H., Armanini, M. P., Nuijens, A., Phillips, H. S. & Osheroff, P. L. Sensory and motor neuron-derived factor. A novel heregulin variant highly expressed in sensory and motor neurons. J. Biol. Chem. 270, 14523–14532 (1995).
  CAS PubMed Google Scholar
• Garratt, A. N., Britsch, S. & Birchmeier, C. Neuregulin, a factor with many functions in the life of a schwann cell. Bioessays 22, 987–996 (2000).
  CAS PubMed Google Scholar
• Nave, K. A. & Salzer, J. L. Axonal regulation of myelination by neuregulin 1. Curr. Opin. Neurobiol. 16, 492–500 (2006).
  CAS PubMed Google Scholar
• Michailov, G. V. et al. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304, 700–703 (2004).
  CAS PubMed Google Scholar
• Taveggia, C. et al. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47, 681–694 (2005).
  CAS PubMed PubMed Central Google Scholar
• Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P. & Anderson, D. J. Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349–360 (1994).
  CAS PubMed Google Scholar
• Lai, C. & Feng, L. Implication of γ-secretase in neuregulin-induced maturation of oligodendrocytes. Biochem. Biophys. Res. Commun. 314, 535–542 (2004).
  CAS PubMed Google Scholar
• Dong, Z. et al. Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15, 585–596 (1995).
  CAS PubMed Google Scholar
• Grinspan, J. B., Marchionni, M. A., Reeves, M., Coulaloglou, M. & Scherer, S. S. Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J. Neurosci. 16, 6107–6118 (1996).
  CAS PubMed PubMed Central Google Scholar
• Winseck, A. K. et al. In vivo analysis of Schwann cell programmed cell death in the embryonic chick: regulation by axons and glial growth factor. J. Neurosci. 22, 4509–4521 (2002).
  CAS PubMed PubMed Central Google Scholar
• Mahanthappa, N. K., Anton, E. S. & Matthew, W. D. Glial growth factor 2, a soluble neuregulin, directly increases Schwann cell motility and indirectly promotes neurite outgrowth. J. Neurosci. 16, 4673–4683 (1996).
  CAS PubMed PubMed Central Google Scholar
• Scherer, S. S. et al. Connexin32 is a myelin-related protein in the PNS and CNS. J. Neurosci. 15, 8281–8294 (1995).
  CAS PubMed PubMed Central Google Scholar
• Trachtenberg, J. T. & Thompson, W. J. Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor. Nature 379, 174–177 (1996).
  CAS PubMed Google Scholar
• Adlkofer, K. & Lai, C. Role of neuregulins in glial cell development. Glia 29, 104–111 (2000).
  CAS PubMed Google Scholar
• Riethmacher, D. et al. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 389, 725–730 (1997).
  CAS PubMed Google Scholar
• Woldeyesus, M. T. et al. Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev. 13, 2538–2548 (1999).
  CAS PubMed PubMed Central Google Scholar
• Chen, S. et al. Neuregulin 1-erbB signalling is necessary for normal myelination and sensory function. J. Neurosci. 26, 3079–3086 (2006).
  CAS PubMed PubMed Central Google Scholar
• Chen, S. et al. Disruption of ErbB receptor signalling in adult non-myelinating Schwann cells causes progressive sensory loss. Nature Neurosci. 6, 1186–1193 (2003).
  CAS PubMed Google Scholar
• Fernandez, P. A. et al. Evidence that axon-derived neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 28, 81–90 (2000).
  CAS PubMed Google Scholar
• Canoll, P. D. et al. GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17, 229–243 (1996).
  CAS PubMed Google Scholar
• Flores, A. I. et al. Akt-mediated survival of oligodendrocytes induced by neuregulins. J. Neurosci. 20, 7622–7630 (2000).
  CAS PubMed PubMed Central Google Scholar
• Vartanian, T., Corfas, G., Li, Y., Fischbach, G. D. & Stefansson, K. A role for the acetylcholine receptor-inducing protein ARIA in oligodendrocyte development. Proc. Natl Acad. Sci. USA 91, 11626–11630 (1994).
  CAS PubMed PubMed Central Google Scholar
• Vartanian, T., Fischbach, G. & Miller, R. Failure of spinal cord oligodendrocyte development in mice lacking neuregulin. Proc. Natl Acad. Sci. USA 96, 731–735 (1999).
  CAS PubMed PubMed Central Google Scholar
• Kim, J. Y., Sun, Q., Oglesbee, M. & Yoon, S. O. The role of ErbB2 signalling in the onset of terminal differentiation of oligodendrocytes in vivo. J. Neurosci. 23, 5561–5571 (2003).
  CAS PubMed PubMed Central Google Scholar
• Roy, K. et al. Loss of erbB signalling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc. Natl Acad. Sci. USA 104, 8131–8136 (2007).
  CAS PubMed PubMed Central Google Scholar
• Park, S. K., Solomon, D. & Vartanian, T. Growth factor control of CNS myelination. Dev. Neurosci. 23, 327–337 (2001).
  CAS PubMed Google Scholar
• Schmucker, J. et al. erbB3 is dispensable for oligodendrocyte development in vitro and in vivo. Glia 44, 67–75 (2003).
  PubMed Google Scholar
• Si, J., Miller, D. S. & Mei, L. Identification of an element required for acetylcholine receptor-inducing activity (ARIA)-induced expression of the acetylcholine receptor epsilon subunit gene. J. Biol. Chem. 272, 10367–10371 (1997).
  CAS PubMed Google Scholar
• Si, J., Luo, Z. & Mei, L. Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase. J. Biol. Chem. 271, 19752–19759 (1996).
  CAS PubMed Google Scholar
• Altiok, N., Altiok, S. & Changeux, J. P. Heregulin-stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity. EMBO J. 16, 717–725 (1997).
  CAS PubMed PubMed Central Google Scholar
• Tansey, M. G., Chu, G. C. & Merlie, J. P. ARIA/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway. J. Cell Biol. 134, 465–476 (1996).
  CAS PubMed Google Scholar
• Sandrock, A. W. et al. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 276, 599–603 (1997).
  PubMed Google Scholar
• Escher, P. et al. Synapses form in skeletal muscles lacking neuregulin receptors. Science 308, 1920–1923 (2005).
  CAS PubMed Google Scholar
• Lin, W. et al. Aberrant development of motor axons and neuromuscular synapses in erbB2-deficient mice. Proc. Natl Acad. Sci. USA 97, 1299–1304 (2000).
  CAS PubMed PubMed Central Google Scholar
• Morris, J. K. et al. Rescue of the cardiac defect in ErbB2 mutant mice reveals essential roles of ErbB2 in peripheral nervous system development. Neuron 23, 273–283 (1999).
  CAS PubMed Google Scholar
• Hippenmeyer, S. et al. A role for neuregulin1 signalling in muscle spindle differentiation. Neuron 36, 1035–1049 (2002).
  CAS PubMed Google Scholar
• Liu, Y., Ford, B., Mann, M. A. & Fischbach, G. D. Neuregulins increase α7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. J. Neurosci. 21, 5660–5669 (2001).
  CAS PubMed PubMed Central Google Scholar
• Yang, X., Kuo, Y., Devay, P., Yu, C. & Role, L. A cysteine-rich isoform of neuregulin controls the level of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20, 255–270 (1998).
  CAS PubMed Google Scholar
• Okada, M. & Corfas, G. Neuregulin1 downregulates postsynaptic GABAA receptors at the hippocampal inhibitory synapse. Hippocampus 14, 337–344 (2004).
  CAS PubMed Google Scholar
• Ozaki, M., Sasner, M., Yano, R., Lu, H. S. & Buonanno, A. Neuregulin-β induces expression of an NMDA-receptor subunit. Nature 390, 691–694 (1997).
  CAS PubMed Google Scholar
• Stefansson, H. et al. Neuregulin 1 and susceptibility to schizophrenia. Am. J. Hum. Genet. 71, 877–892 (2002). This was the first report to identify SNPs and microsatellites in NRG1 as being associated with schizophrenia.
  PubMed PubMed Central Google Scholar
• Li, B., Woo, R. S., Mei, L. & Malinow, R. The neuregulin-1 receptor ErbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54, 583–597 (2007). In this study, the roles of NRG1 and ErbB4 in the formation and maturation of glutamatergic synapses were investigated by gain and loss of function in cultured postnatal hippocampal slices. Evidence was shown that NRG1–ErbB4 signalling is essential for synapse maturation and plasticity.
  CAS PubMed PubMed Central Google Scholar
• Woo, R. S. et al. Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54, 599–610 (2007). This paper provided evidence that NRG1 enhances activity-dependent GABA release through ErbB4 that is present in GABAergic terminals.
  CAS PubMed Google Scholar
• Lai, C. & Lemke, G. An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6, 691–704 (1991).
  CAS PubMed Google Scholar
• Harrison, P. J. The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl.) 174, 151–162 (2004).
  CAS Google Scholar
• Lewis, D. A. & Moghaddam, B. Cognitive dysfunction in schizophrenia: convergence of γ-aminobutyric acid and glutamate alterations. Arch. Neurol. 63, 1372–1376 (2006).
  PubMed Google Scholar
• Moghaddam, B. Targeting metabotropic glutamate receptors for treatment of the cognitive symptoms of schizophrenia. Psychopharmacology (Berl.) 174, 39–44 (2004).
  CAS Google Scholar
• Tsai, G. & Coyle, J. T. Glutamatergic mechanisms in schizophrenia. Annu. Rev. Pharmacol. Toxicol. 42, 165–179 (2002).
  CAS PubMed Google Scholar
• Huang, Y. Z. et al. Regulation of neuregulin signalling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26, 443–455 (2000). This paper and reference 119 were the first to show that ErbB4 interacts and colocalizes with PSD95 in cultured neurons. In addition, this paper provided the first evidence that NRG1 suppresses LTP in the hippocampus and that interaction with PSD95 facilitates NRG1 signalling.
  CAS PubMed Google Scholar
• Garcia, R. A. G., Vasudevan, K. & Buonanno, A. The neuregulin receptor ErbB4 interacts with PDZ-containing proteins at neuronal synapses. Proc. Natl Acad. Sci. USA 97, 3596–3601 (2000).
  CAS PubMed PubMed Central Google Scholar
• Ma, L. et al. Ligand-dependent recruitment of the ErbB4 signalling complex into neuronal lipid rafts. J. Neurosci. 23, 3164–3175 (2003).
  CAS PubMed PubMed Central Google Scholar
• Pitcher, G. M., Beggs, S., Woo, R. S., Mei, L. & Salter, M. W. ErbB4 is a suppressor of long-term potentiation in the adult hippocampus. Neuroreport 19, 139–143 (2008). This paper used pharmacological and genetic approaches to demonstrate the essential role of ErbB4 in the suppression of LTP by NRG1.
  CAS PubMed PubMed Central Google Scholar
• Kwon, O. B., Longart, M., Vullhorst, D., Hoffman, D. A. & Buonanno, A. Neuregulin-1 reverses long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 25, 9378–9383 (2005).
  CAS PubMed PubMed Central Google Scholar
• Role, L. W. & Talmage, D. A. Neurobiology: new order for thought disorders. Nature 448, 263–265 (2007).
  CAS PubMed Google Scholar
• Iyengar, S. S. & Mott, D. D. Neuregulin blocks synaptic strengthening after epileptiform activity in the rat hippocampus. Brain Res. 29 Feb 2008 [epub ahead of print].
• Wang, Y. T. & Salter, M. W. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369, 233–235 (1994).
  CAS PubMed Google Scholar
• Yu, X. M., Askalan, R., Keil, G. J. & Salter, M. W. NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275, 674–678 (1997).
  CAS PubMed Google Scholar
• Malinow, R. & Malenka, R. C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103–126 (2002).
  CAS PubMed Google Scholar
• Roysommuti, S., Carroll, S. L. & Wyss, J. M. Neuregulin-1β modulates in vivo entorhinal-hippocampal synaptic transmission in adult rats. Neuroscience 121, 779–785 (2003).
  CAS PubMed Google Scholar
• Fischbach, G. D. NRG1 and synaptic function in the CNS. Neuron 54, 495–497 (2007).
  CAS PubMed Google Scholar
• Belan, P. V. & Kostyuk, P. G. Glutamate-receptor-induced modulation of GABAergic synaptic transmission in the hippocampus. Pflugers Arch. 444, 26–37 (2002).
  CAS PubMed Google Scholar
• Xie, F., Raetzman, L. T. & Siegel, R. E. Neuregulin induces GABAA receptor β2 subunit expression in cultured rat cerebellar granule neurons by activating multiple signalling pathways. J. Neurochem. 90, 1521–1529 (2004).
  CAS PubMed Google Scholar
• Cameron, J. S., Dryer, L. & Dryer, S. E. β-neuregulin-1 is required for the in vivo development of functional Ca2+-activated K+ channels in parasympathetic neurons. Proc. Natl Acad. Sci. USA 98, 2832–2836 (2001).
  CAS PubMed PubMed Central Google Scholar
• Subramony, P. & Dryer, S. E. Neuregulins stimulate the functional expression of Ca2+-activated K+ channels in developing chicken parasympathetic neurons. Proc. Natl Acad. Sci. USA 94, 5934–5938 (1997).
  CAS PubMed PubMed Central Google Scholar
• Li, B. S. et al. Cyclin-dependent kinase-5 is involved in neuregulin-dependent activation of phosphatidylinositol 3-kinase and Akt activity mediating neuronal survival. J. Biol. Chem. 278, 35702–35709 (2003).
  CAS PubMed Google Scholar
• Ricart, K. et al. Interactions between β-neuregulin and neurotrophins in motor neuron apoptosis. J. Neurochem. 97, 222–233 (2006).
  CAS PubMed Google Scholar
• Zhang, L. et al. Neurotrophic and neuroprotective effects of the neuregulin glial growth factor-2 on dopaminergic neurons in rat primary midbrain cultures. J. Neurochem. 91, 1358–1368 (2004).
  CAS PubMed Google Scholar
• Stankovic, K. et al. Survival of adult spiral ganglion neurons requires erbB receptor signalling in the inner ear. J. Neurosci. 24, 8651–8661 (2004).
  CAS PubMed PubMed Central Google Scholar
• Goldshmit, Y., Erlich, S. & Pinkas-Kramarski, R. Neuregulin rescues PC12-ErbB4 cells from cell death induced by H2O2. Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 46379–46385 (2001).
  CAS PubMed Google Scholar
• Li, Y. et al. Neuroprotection by neuregulin-1 in a rat model of permanent focal cerebral ischemia. Brain Res. 1184, 277–283 (2007).
  CAS PubMed PubMed Central Google Scholar
• Shyu, W. C. et al. Neuregulin-1 reduces ischemia-induced brain damage in rats. Neurobiol. Aging 25, 935–944 (2004).
  CAS PubMed Google Scholar
• Croslan, D. R. et al. Neuroprotective effects of neuregulin-1 on B35 neuronal cells following ischemia. Brain Res. 4 Mar 2008 [epub ahead of print].
• Badner, J. A. & Gershon, E. S. Meta-analysis of whole-genome linkage scans of bipolar disorder and schizophrenia. Mol. Psychiatry 7, 405–411 (2002).
  CAS PubMed Google Scholar
• Lewis, C. M. et al. Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: schizophrenia. Am. J. Hum. Genet. 73, 34–48 (2003).
  CAS PubMed PubMed Central Google Scholar
• Yang, J. Z. et al. Association study of neuregulin 1 gene with schizophrenia. Mol. Psychiatry 8, 706–709 (2003). Using the polymerase-chain-reaction-based restriction-fragment length polymorphism method and denaturing high-performance liquid chromatography, this independent study identified two additional NRG1 SNPs that are associated with schizophrenia in 246 Chinese Han schizophrenic family trios.
  CAS PubMed Google Scholar
• Kim, J. W. et al. Linkage and association of schizophrenia with genetic variations in the locus of neuregulin 1 in Korean population. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 281–286 (2006).
  Google Scholar
• Hall, D., Gogos, J. A. & Karayiorgou, M. The contribution of three strong candidate schizophrenia susceptibility genes in demographically distinct populations. Genes Brain Behav. 3, 240–248 (2004).
  CAS PubMed Google Scholar
• Stefansson, H. et al. Association of neuregulin 1 with schizophrenia confirmed in a Scottish population. Am. J. Hum. Genet. 72, 83–87 (2003).
  CAS PubMed Google Scholar
• Williams, N. M. et al. Support for genetic variation in neuregulin 1 and susceptibility to schizophrenia. Mol. Psychiatry 8, 485–487 (2003).
  CAS PubMed Google Scholar
• Bakker, S. C. et al. Neuregulin 1: genetic support for schizophrenia subtypes. Mol. Psychiatry 9, 1061–1063 (2004).
  CAS PubMed Google Scholar
• Li, T. et al. Identification of a novel neuregulin 1 at-risk haplotype in Han schizophrenia Chinese patients, but no association with the Icelandic/Scottish risk haplotype. Mol. Psychiatry 9, 698–704 (2004).
  CAS PubMed Google Scholar
• Tang, J. X. et al. Polymorphisms within 5′ end of the Neuregulin 1 gene are genetically associated with schizophrenia in the Chinese population. Mol. Psychiatry 9, 11–12 (2004).
  CAS PubMed Google Scholar
• Petryshen, T. L. et al. Support for involvement of neuregulin 1 in schizophrenia pathophysiology. Mol. Psychiatry 10, 366–374, 328 (2005).
  CAS PubMed Google Scholar
• Corvin, A. P. et al. Confirmation and refinement of an 'at-risk' haplotype for schizophrenia suggests the EST cluster, Hs.97362, as a potential susceptibility gene at the Neuregulin-1 locus. Mol. Psychiatry 9, 208–213 (2004).
  CAS PubMed Google Scholar
• Zhao, X. et al. A case control and family based association study of the neuregulin1 gene and schizophrenia. J. Med. Genet. 41, 31–34 (2004).
  CAS PubMed PubMed Central Google Scholar
• Benzel, I. et al. Interactions among genes in the ErbB-Neuregulin signalling network are associated with increased susceptibility to schizophrenia. Behav. Brain Funct. 3, 31 (2007).
  PubMed PubMed Central Google Scholar
• Lachman, H. M. et al. Analysis of polymorphisms in AT-rich domains of neuregulin 1 gene in schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 102–109 (2006).
  Google Scholar
• Law, A. J. et al. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPs associated with the disease. Proc. Natl Acad. Sci. USA 103, 6747–6752 (2006). In this study, Type I NRG1 mRNA was found to be upregulated in the hippocampus of patients with schizophrenia, suggesting that the association of NRG1 with schizophrenia might be mediated by altered expression of the gene.
  CAS PubMed PubMed Central Google Scholar
• Silberberg, G., Darvasi, A., Pinkas-Kramarski, R. & Navon, R. The involvement of ErbB4 with schizophrenia: association and expression studies. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 142–148 (2006). This paper compared the expression of ErbB4 isoforms in the dorsolateral prefrontal cortex (DLPFC) of controls and patients with schizophrenia and showed that the CYT-1 and JMa isoforms are overexpressed at the mRNA level in the DLPFC of schizophrenia patients.
  Google Scholar
• Law, A. J., Kleinman, J. E., Weinberger, D. R. & Weickert, C. S. Disease-associated intronic variants in the ErbB4 gene are related to altered ErbB4 splice-variant expression in the brain in schizophrenia. Hum. Mol. Genet. 16, 129–141 (2007). This paper studied the expression of ErbB4 isoforms in the DLPFC and hippocampus of controls and patients with schizophrenia. The CYT-1 and JMa ErbB4 isoforms were increased in the DLPFC but not the hippocampus of the patients. This observation suggests that dysregulation of the splice-variant-specific expression of ErbB4 might be region-specific.
  CAS PubMed Google Scholar
• Hall, J. et al. A neuregulin 1 variant associated with abnormal cortical function and psychotic symptoms. Nature Neurosci. 9, 1477–1478 (2006).
  CAS PubMed Google Scholar
• Thiselton, D. L. et al. No evidence for linkage or association of neuregulin-1 (NRG1) with disease in the Irish study of high-density schizophrenia families (ISHDSF). Mol. Psychiatry 9, 777–783 (2004).
  CAS PubMed Google Scholar
• Iwata, N. et al. No association with the neuregulin 1 haplotype to Japanese schizophrenia. Mol. Psychiatry 9, 126–127 (2004).
  CAS PubMed Google Scholar
• Rosa, A. et al. Family-based association study of neuregulin-1 gene and psychosis in a Spanish sample. Am. J. Med. Genet. B Neuropsychiatr. Genet. 144, 954–957 (2007).
  Google Scholar
• Walss-Bass, C. et al. A novel missense mutation in the transmembrane domain of neuregulin 1 is associated with schizophrenia. Biol. Psychiatry 60, 548–553 (2006).
  CAS PubMed Google Scholar
• Hong, L. E., Wonodi, I., Stine, O. C., Mitchell, B. D. & Thaker, G. K. Evidence of missense mutations on the neuregulin 1 gene affecting function of prepulse inhibition. Biol. Psychiatry 63, 17–23 (2007).
  PubMed PubMed Central Google Scholar
• Lin, H. F. et al. Neuregulin 1 gene and variations in perceptual aberration of schizotypal personality in adolescents. Psychol. Med. 35, 1589–1598 (2005).
  PubMed Google Scholar
• Norton, N. et al. Evidence that interaction between neuregulin 1 and its receptor erbB4 increases susceptibility to schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 141, 96–101 (2006).
  Google Scholar
• Nicodemus, K. K. et al. Further evidence for association between ErbB4 and schizophrenia and influence on cognitive intermediate phenotypes in healthy controls. Mol. Psychiatry 11, 1062–1065 (2006).
  CAS PubMed Google Scholar
• Walsh, T. et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 320, 539–543 (2008). This study identified ERBB4 as one of the genes that is disrupted by the microdeletions and microduplications that are associated with schizophrenia.
  CAS PubMed Google Scholar
• Arguello, P. A. & Gogos, J. A. Modeling madness in mice: one piece at a time. Neuron 52, 179–196 (2006).
  CAS PubMed Google Scholar
• Golub, M. S., Germann, S. L. & Lloyd, K. C. Behavioral characteristics of a nervous system-specific erbB4 knock-out mouse. Behav. Brain Res. 153, 159–170 (2004).
  CAS PubMed Google Scholar
• O'Tuathaigh, C. M. et al. Phenotypic characterization of spatial cognition and social behaviour in mice with 'knockout' of the schizophrenia risk gene neuregulin 1. Neuroscience 147, 18–27 (2007).
  CAS PubMed Google Scholar
• Rimer, M., Barrett, D. W., Maldonado, M. A., Vock, V. M. & Gonzalez-Lima, F. Neuregulin-1 immunoglobulin-like domain mutant mice: clozapine sensitivity and impaired latent inhibition. Neuroreport 16, 271–275 (2005).
  CAS PubMed Google Scholar
• Thuret, S. et al. The neuregulin receptor, ErbB4, is not required for normal development and adult maintenance of the substantia nigra pars compacta. J. Neurochem. 91, 1302–1311 (2004).
  CAS PubMed Google Scholar
• Savonenko, A. V. et al. Alteration of BACE1-dependent NRG1/ErbB4 signalling and schizophrenia-like phenotypes in _BACE1_-null mice. Proc. Natl Acad. Sci. USA 105, 5585–5590 (2008).
  CAS PubMed PubMed Central Google Scholar
• Prevot, V. et al. Normal female sexual development requires neuregulin-erbB receptor signalling in hypothalamic astrocytes. J. Neurosci. 23, 230–239 (2003).
  CAS PubMed PubMed Central Google Scholar
• Lipska, B. K. Using animal models to test a neurodevelopmental hypothesis of schizophrenia. J. Psychiatry Neurosci. 29, 282–286 (2004).
  PubMed PubMed Central Google Scholar
• Lewis, D. A. & Levitt, P. Schizophrenia as a disorder of neurodevelopment. Annu. Rev. Neurosci. 25, 409–432 (2002).
  CAS PubMed Google Scholar
• Hashimoto, R. et al. Expression analysis of neuregulin-1 in the dorsolateral PFC in schizophrenia. Mol. Psychiatry 9, 299–307 (2004). This study was the first to show that Type I NRG1 expression is increased in the DLPFC of patients with schizophrenia and positively correlates with antipsychotic medication dosage.
  CAS PubMed Google Scholar
• Hakak, Y. et al. Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc. Natl Acad. Sci. USA 98, 4746–4751 (2001).
  CAS PubMed PubMed Central Google Scholar
• Sugai, T. et al. Prefrontal abnormality of schizophrenia revealed by DNA microarray: impact on glial and neurotrophic gene expression. Ann. NY Acad. Sci. 1025, 84–91 (2004).
  CAS PubMed Google Scholar
• Hahn, C. G. et al. Altered neuregulin 1-erbB4 signalling contributes to NMDA receptor hypofunction in schizophrenia. Nature Med. 12, 824–828 (2006). This paper showed that there is a marked increase in NRG1-induced activation of ErbB4, ERK and Akt and in the ErbB4–PSD95 interaction in the PFC in schizophrenia, accompanied by a reduction in tyrosine phosphorylation of NMDAR2A in response to NMDA stimulation. These findings suggest that enhanced NRG1 signalling might contribute to NMDA hypofunction in schizophrenia.
  CAS PubMed Google Scholar
• Chong, V. Z. et al. Elevated neuregulin-1 and ErbB4 protein in the PFC of schizophrenic patients. Schizophr. Res. 100, 270–280 (2008).
  PubMed PubMed Central Google Scholar
• Kalkman, H. O. The role of the phosphatidylinositide 3-kinase-protein kinase B pathway in schizophrenia. Pharmacol. Ther. 110, 117–134 (2006).
  CAS PubMed Google Scholar
• Lewis, D. A., Hashimoto, T. & Volk, D. W. Cortical inhibitory neurons and schizophrenia. Nature Rev. Neurosci. 6, 312–324 (2005).
  CAS Google Scholar
• Norton, N., Williams, H. J. & Owen, M. J. An update on the genetics of schizophrenia. Curr. Opin. Psychiatry 19, 158–164 (2006).
  PubMed Google Scholar
• Elenius, K. et al. A novel juxtamembrane domain isoform of HER4/ErbB4. Isoform-specific tissue distribution and differential processing in response to phorbol ester. J. Biol. Chem. 272, 26761–26768 (1997).
  CAS PubMed Google Scholar
• Sawyer, C., Hiles, I., Page, M., Crompton, M. & Dean, C. Two erbB-4 transcripts are expressed in normal breast and in most breast cancers. Oncogene 17, 919–924 (1998).
  CAS PubMed Google Scholar
• Junttila, T. T., Sundvall, M., Maatta, J. A. & Elenius, K. Erbb4 and its isoforms: selective regulation of growth factor responses by naturally occurring receptor variants. Trends Cardiovasc. Med. 10, 304–310 (2000).
  CAS PubMed Google Scholar
• Rio, C., Buxbaum, J. D., Peschon, J. J. & Corfas, G. Tumour necrosis factor-α-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275, 10379–10387 (2000).
  CAS PubMed Google Scholar
• Cheng, Q. C., Tikhomirov, O., Zhou, W. & Carpenter, G. Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment. J. Biol. Chem. 278, 38421–38427 (2003).
  CAS PubMed Google Scholar
• Arasada, R. R. & Carpenter, G. Secretase-dependent tyrosine phosphorylation of Mdm2 by the ErbB-4 intracellular domain fragment. J. Biol. Chem. 280, 30783–30787 (2005).
  CAS PubMed Google Scholar
• Feng, S. M. et al. The HER4 cytoplasmic domain, but not its C terminus, inhibits mammary cell proliferation. Mol. Endocrinol. 21, 1861–1876 (2007).
  CAS PubMed Google Scholar
• Linggi, B. & Carpenter, G. ErbB-4 s80 intracellular domain abrogates ETO2-dependent transcriptional repression. J. Biol. Chem. 281, 25373–25380 (2006).
  CAS PubMed Google Scholar
• Omerovic, J. et al. Ligand-regulated association of ErbB-4 to the transcriptional co-activator YAP65 controls transcription at the nuclear level. Exp. Cell Res. 294, 469–479 (2004).
  CAS PubMed Google Scholar
• Vidal, G. A., Naresh, A., Marrero, L. & Jones, F. E. Presenilin-dependent γ-secretase processing regulates multiple ERBB4/HER4 activities. J. Biol. Chem. 280, 19777–19783 (2005).
  CAS PubMed Google Scholar
• Komuro, A., Nagai, M., Navin, N. E. & Sudol, M. WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 278, 33334–33341 (2003).
  CAS PubMed Google Scholar
• Wang, J. Y., Wigston, D. J., Rees, H. D., Levey, A. I. & Falls, D. L. LIM kinase 1 accumulates in presynaptic terminals during synapse maturation. J. Comp. Neurol. 416, 319–334 (2000).
  CAS PubMed Google Scholar
• Wang, J. Y., Frenzel, K. E., Wen, D. & Falls, D. L. Transmembrane neuregulins interact with LIM kinase 1, a cytoplasmic protein kinase implicated in development of visuospatial cognition. J. Biol. Chem. 273, 20525–20534 (1998).
  CAS PubMed Google Scholar
• Liu, X. et al. Domain-specific gene disruption reveals critical regulation of neuregulin signalling by its cytoplasmic tail. Proc. Natl Acad. Sci. USA 95, 13024–13029 (1998).
  CAS PubMed PubMed Central Google Scholar
• Sherman, D. L. & Brophy, P. J. Mechanisms of axon ensheathment and myelin growth. Nature Rev. Neurosci. 6, 683–690 (2005).
  CAS Google Scholar
• Kim, E. & Sheng, M. PDZ domain proteins of synapses. Nature Rev. Neurosci. 5, 771–781 (2004).
  CAS Google Scholar
• Craig, A. M. & Kang, Y. Neurexin-neuroligin signalling in synapse development. Curr. Opin. Neurobiol. 17, 43–52 (2007).
  CAS PubMed PubMed Central Google Scholar
• Huang, Y. Z., Wang, Q., Xiong, W. C. & Mei, L. Erbin is a protein concentrated at postsynaptic membranes that interacts with PSD-95. J. Biol. Chem. 276, 19318–19326 (2001).
  CAS PubMed Google Scholar
• Borg, J. P. et al. ERBIN: a basolateral PDZ protein that interacts with the mammalian ERBB2/HER2 receptor. Nature Cell Biol. 2, 407–414 (2000).
  CAS PubMed Google Scholar
• Huang, Y. Z., Zang, M., Xiong, W. C., Luo, Z. & Mei, L. Erbin suppresses the MAP kinase pathway. J. Biol. Chem. 278, 1108–1114 (2003).
  CAS PubMed Google Scholar
• Dai, P., Xiong, W. C. & Mei, L. Erbin inhibits RAF activation by disrupting the sur-8-Ras-Raf complex. J. Biol. Chem. 281, 927–933 (2006).
  CAS PubMed Google Scholar
• Markram, H. et al. Interneurons of the neocortical inhibitory system. Nature Rev. Neurosci. 5, 793–807 (2004).
  CAS Google Scholar
• Gupta, A., Wang, Y. & Markram, H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273–278 (2000).
  CAS PubMed Google Scholar
• Kawaguchi, Y. & Kubota, Y. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85, 677–701 (1998).
  CAS PubMed Google Scholar
• Zaitsev, A. V. et al. Localization of calcium-binding proteins in physiologically and morphologically characterized interneurons of monkey dorsolateral PFC. Cereb. Cortex 15, 1178–1186 (2005).
  CAS PubMed Google Scholar