Transient exposure of neonatal mice to neuregulin-1 results in hyperdopaminergic states in adulthood: implication in neurodevelopmental hypothesis for schizophrenia (original) (raw)
Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002; 71: 877–892. PubMedPubMed Central Google Scholar
Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, Cooper GM et al. Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 2008; 320: 539–543. ArticleCASPubMed Google Scholar
Chong VZ, Thompson M, Beltaifa S, Webster MJ, Law AJ, Weickert CS . Elevated neuregulin-1 and ErbB4 protein in the prefrontal cortex of schizophrenic patients. Schizophr Res 2008; 100: 270–280. ArticlePubMedPubMed Central Google Scholar
Hashimoto R, Straub RE, Weickert CS, Hyde TM, Kleinman JE, Weinberger DR . Expression analysis of neuregulin-1 in the dorsolateral prefrontal cortex in schizophrenia. Mol Psychiatry 2004; 9: 299–307. ArticleCASPubMed Google Scholar
Law AJ, Lipska BK, Weickert CS, Hyde TM, Straub RE, Hashimoto R et al. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5′ SNPs associated with the disease. Proc Natl Acad Sci USA 2006; 103: 6747–6752. ArticleCASPubMedPubMed Central Google Scholar
Petryshen TL, Middleton FA, Kirby A, Aldinger KA, Purcell S, Tahl AR et al. Support for involvement of neuregulin 1 in schizophrenia pathophysiology. Mol Psychiatry 2005; 10: 366–374. ArticleCASPubMed Google Scholar
Brown AS, Begg MD, Gravenstein S, Schaefer CA, Wyatt RJ, Bresnahan M et al. Serologic evidence of prenatal influenza in the etiology of schizophrenia. Arch Gen Psychiatry 2004; 61: 774–780. ArticlePubMed Google Scholar
Zornberg GL, Buka SL, Tsuang MT . Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry 2000; 157: 196–202. ArticleCASPubMed Google Scholar
Nadri C, Belmaker RH, Agam G . Oxygen restriction of neonate rats elevates neuregulin-1alpha isoform levels: possible relationship to schizophrenia. Neurochem Int 2007; 51: 447–450. ArticleCASPubMed Google Scholar
Parker MW, Chen Y, Hallenbeck JM, Ford BD . Neuregulin expression after focal stroke in the rat. Neurosci Lett 2002; 334: 169–172. ArticleCASPubMed Google Scholar
Tokita Y, Keino H, Matsui F, Aono S, Ishiguro H, Higashiyama S et al. Regulation of neuregulin expression in the injured rat brain and cultured astrocytes. J Neurosci 2001; 21: 1257–1264. ArticleCASPubMedPubMed Central Google Scholar
Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C et al. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 2004; 44: 251–261. ArticleCASPubMed Google Scholar
Taveggia C, Thaker P, Petrylak A, Caporaso GL, Toews A, Falls DL et al. Type III neuregulin-1 promotes oligodendrocyte myelination. Glia 2008; 56: 284–293. ArticlePubMed Google Scholar
Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y, Hines R et al. ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem 2008; 283: 32944–32956. ArticleCASPubMedPubMed Central Google Scholar
López-Bendito G, Cautinat A, Sánchez JA, Bielle F, Flames N, Garratt AN et al. Tangential neuronal migration controls axon guidance: a role for neuregulin-1 in thalamocortical axon navigation. Cell 2006; 125: 127–142. ArticlePubMedPubMed Central Google Scholar
Chen YJ, Johnson MA, Lieberman MD, Goodchild RE, Schobel S, Lewandowski N et al. Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J Neurosci 2008; 28: 6872–6883. ArticleCASPubMedPubMed Central Google Scholar
Ehrlichman RS, Luminais SN, White SL, Rudnick ND, Ma N, Dow HC et al. Neuregulin 1 transgenic mice display reduced mismatch negativity, contextual fear conditioning and social interactions. Brain Res 2009; 1294: 116–127. ArticleCASPubMedPubMed Central Google Scholar
O’Tuathaigh CM, Babovic D, O’Sullivan GJ, Clifford JJ, Tighe O, Croke DT et al. Phenotypic characterization of spatial cognition and social behavior in mice with ‘knockout’ of the schizophrenia risk gene neuregulin 1. Neuroscience 2007; 147: 18–27. ArticlePubMed Google Scholar
Rimer M, Barrett DW, Maldonado MA, Vock VM, Gonzalez-Lima F . Neuregulin-1 immunoglobulin-like domain mutant mice: clozapine sensitivity and impaired latent inhibition. Neuroreport 2005; 16: 271–275. ArticleCASPubMed Google Scholar
Abe Y, Namba H, Zheng Y, Nawa H . In situ hybridization reveals developmental regulation of ErbB1-4 mRNA expression in mouse midbrain: implication of ErbB receptors for dopaminergic neurons. Neuroscience 2009; 161: 95–110. ArticleCASPubMed Google Scholar
Zheng Y, Watakabe A, Takada M, Kakita A, Namba H, Takahashi H et al. Expression of ErbB4 in substantia nigra dopamine neurons of monkeys and humans. Prog Neuropsychopharmacol Biol Psychiatry 2009; 33: 701–706. ArticlePubMed Google Scholar
Fox IJ, Kornblum HI . Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions. J Neurosci Res 2005; 79: 584–597. ArticleCASPubMed Google Scholar
Neddens J, Vullhorst D, Paredes D, Buonanno A . Neuregulin links dopaminergic and glutamatergic neurotransmission to control hippocampal synaptic plasticity. Commun Integr Biol 2009; 2: 261–264. ArticleCASPubMedPubMed Central Google Scholar
Lewis DA, Levitt P . Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 2002; 25: 409–432. ArticleCASPubMed Google Scholar
Murray RM, Lewis SW . Is schizophrenia a neurodevelopmental disorder? Br Med J 1987; 295: 681–682. ArticleCAS Google Scholar
Weinberger DR . Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 1987; 44: 660–669. ArticleCASPubMed Google Scholar
Winterer G, Weinberger DR . Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 2004; 27: 683–690. ArticleCASPubMed Google Scholar
Ozaki M, Tohyama K, Kishida H, Buonanno A, Yano R, Hashikawa T . Roles of neuregulin in synaptogenesis between mossy fibers and cerebellar granule cells. J Neurosci Res 2000; 59: 612–623. ArticleCASPubMed Google Scholar
Umetsu M, Tsumoto K, Hara M, Ashish K, Goda S, Adschiri T et al. How additives influence the refolding of immunoglobulin-folded proteins in a stepwise dialysis system. Spectroscopic evidence for highly efficient refolding of a single-chain Fv fragment. J Biol Chem 2003; 278: 8979–8987. ArticleCASPubMed Google Scholar
Tohmi M, Tsuda N, Zheng Y, Mizuno M, Sotoyama H, Shibuya M et al. The cellular and behavioral consequences of interleukin-1 alpha penetration through the blood-brain barrier of neonatal rats: a critical period for efficacy. Neuroscience 2007; 150: 234–250. ArticleCASPubMed Google Scholar
Kapur S, VanderSpek SC, Brownlee BA, Nobrega JN . Antipsychotic dosing in preclinical models is often unrepresentative of the clinical condition: a suggested solution based on in vivo occupancy. J Pharmacol Exp Ther 2003; 305: 625–631. ArticleCASPubMed Google Scholar
Lim EP, Verma V, Nagarajah R, Dawe GS . Propranolol blocks chronic risperidone treatment-induced enhancement of spatial working memory performance of rats in a delayed matching-to-place water maze task. Psychopharmacology (Berl) 2007; 191: 297–310. ArticleCAS Google Scholar
Martinez-Gras I, Rubio G, del Manzano BA, Rodriguez-Jimenez R, Garcia-Sanchez F, Bagney A et al. The relationship between prepulse inhibition and general psychopathology in patients with schizophrenia treated with long-acting risperidone. Schizophr Res 2009; 115: 215–221. ArticlePubMed Google Scholar
Namba H, Zheng Y, Abe Y, Nawa H . Epidermal growth factor administered in the periphery influences excitatory synaptic inputs onto midbrain dopaminergic neurons in postnatal mice. Neuroscience 2009; 158: 1731–1741. ArticleCASPubMed Google Scholar
Tohmi M, Tsuda N, Mizuno M, Takei N, Frankland PW, Nawa H . Distinct influences of neonatal epidermal growth factor challenge on adult neurobehavioral traits in four mouse strains. Behav Genet 2005; 35: 615–629. ArticlePubMed Google Scholar
Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, Silva AJ . Consolidation of CS and US representations in associative fear conditioning. Hippocampus 2004; 14: 557–569. ArticlePubMed Google Scholar
Caldarone BJ, Duman CH, Picciotto MR . Fear conditioning and latent inhibition in mice lacking the high affinity subclass of nicotinic acetylcholine receptors in the brain. Neuropharmacology 2000; 39: 2779–2784. ArticleCASPubMed Google Scholar
Brown HE, Garcia MM, Harlan RE . A two focal plane method for digital quantification of nuclear immunoreactivity in large brain areas using NIH-image software. Brain Res Brain Protoc 1998; 2: 264–272. ArticleCAS Google Scholar
Mizuno M, Sotoyama H, Narita E, Kawamura H, Namba H, Zheng Y et al. A cyclooxygenase-2 inhibitor ameliorates behavioral impairments induced by striatal administration of epidermal growth factor. J Neurosci 2007; 27: 10116–10127. ArticleCASPubMedPubMed Central Google Scholar
Futamura T, Kakita A, Tohmi M, Sotoyama H, Takahashi H, Nawa H . Neonatal perturbation of neurotrophic signaling results in abnormal sensorimotor gating and social interaction in adults: implication for epidermal growth factor in cognitive development. Mol Psychiatry 2003; 8: 19–29. ArticleCASPubMed Google Scholar
Liu Y, Tao YM, Woo RS, Xiong WC, Mei L . Stimulated ErbB4 internalization is necessary for neuregulin signaling in neurons. Biochem Biophys Res Commun 2007; 354: 505–510. ArticleCASPubMedPubMed Central Google Scholar
Fujisawa H, Okuno S . Regulatory mechanism of tyrosine hydroxylase activity. Biochem Biophys Res Commun 2005; 338: 271–276. ArticleCASPubMed Google Scholar
Ozaki M, Sasner M, Yano R, Lu HS, Buonanno A . Neuregulin-beta induces expression of an NMDA-receptor subunit. Nature 1997; 390: 691–694. ArticleCASPubMed Google Scholar
Sardi SP, Murtie J, Koirala S, Patten BA, Corfas G . Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 2006; 127: 185–197. ArticleCASPubMed Google Scholar
Roy K, Murtie JC, El-Khodor BF, Edgar N, Sardi SP, Hooks BM et al. Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 2007; 104: 8131–8136. ArticleCASPubMedPubMed Central Google Scholar
Broersen LM, Feldon J, Weiner I . Dissociative effects of apomorphine infusions into the medial prefrontal cortex of rats on latent inhibition, prepulse inhibition and amphetamine-induced locomotion. Neuroscience 1999; 94: 39–46. ArticleCASPubMed Google Scholar
Grillon C, Ameli R, Charney DS, Krystal J, Braff D . Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol Psychiatry 1992; 32: 939–943. ArticleCASPubMed Google Scholar
Stankovic K, Rio C, Xia A, Sugawara M, Adams JC, Liberman MC et al. Survival of adult spiral ganglion neurons requires erbB receptor signaling in the inner ear. J Neurosci 2004; 24: 8651–8661. ArticleCASPubMedPubMed Central Google Scholar
Kumari V, Soni W, Sharma T . Prepulse inhibition of the startle response in risperidone-treated patients: comparison with typical antipsychotics. Schizophr Res 2002; 55: 139–146. ArticlePubMed Google Scholar
Gray NS, Pickering AD, Hemsley DR, Dawling S, Gray JA . Abolition of latent inhibition by a single 5 mg dose of d-amphetamine in man. Psychopharmacology (Berl) 1992; 107: 425–430. ArticleCAS Google Scholar
Peleg-Raibstein D, Knuesel I, Feldon J . Amphetamine sensitization in rats as an animal model of schizophrenia. Behav Brain Res 2008; 191: 190–201. ArticleCASPubMed Google Scholar
Baruch I, Hemsley DR, Gray JA . Differential performance of acute and chronic schizophrenics in a latent inhibition task. J Nerv Ment Dis 1998; 176: 598–606. Article Google Scholar
Nawa H, Takahashi M, Patterson PH . Cytokine and growth factor involvement in schizophrenia-support for the developmental model. Mol Psychiatry 2000; 5: 594–603. ArticleCASPubMed Google Scholar
Thuret S, Alavian KN, Gassmann M, Lloyd CK, Smits SM, Smidt MP et al. The neuregulin receptor, ErbB4, is not required for normal development and adult maintenance of the substantia nigra pars compacta. J Neurochem 2004; 91: 1302–1311. ArticleCASPubMed Google Scholar
Hu Z, Cooper M, Crockett DP, Zhou R . Differentiation of the midbrain dopaminergic pathways during mouse development. J Comp Neurol 2004; 476: 301–311. ArticlePubMed Google Scholar
Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HB . Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 1998; 269: 58–72. Article Google Scholar
Falls FL . Neuregulins: functions, forms, and signaling strategies. Exp Cell Res 2003; 284: 14–30. ArticleCASPubMed Google Scholar
Harrison PJ, Law AJ . Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 2006; 60: 132–140. ArticleCASPubMed Google Scholar
Li Q, Loeb JA . Neuregulin-heparan-sulfate proteoglycan interactions produce sustained erbB receptor activation required for the induction of acetylcholine receptors in muscle. J Biol Chem 2001; 276: 38068–38075. CASPubMed Google Scholar
Brummelte S, Teuchert-Noodt G . Postnatal development of dopamine innervation in the amygdala and the entorhinal cortex of the gerbil (Meriones unguiculatus). Brain Res 2006; 1125: 9–16. ArticleCASPubMed Google Scholar
Deakin IH, Law AJ, Oliver PL, Schwab MH, Nave KA, Harrison PJ et al. Behavioural characterization of neuregulin 1 type I overexpressing transgenic mice. Neuroreport 2009; 20: 1523–1528. ArticleCASPubMedPubMed Central Google Scholar
Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL . GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 1996; 17: 229–243. ArticleCASPubMed Google Scholar
Lieberman JA, Kane JM, Alvir J . Provocative tests with psychostimulant drugs in schizophrenia. Psychopharmacology (Berl) 1987; 91: 415–433. ArticleCAS Google Scholar
Clemens KJ, Van Nieuwenhuyzen PS, Li KM, Cornish JL, Hunt GE, McGregor IS . MDMA (‘ecstasy’), methamphetamine and their combination: long-term changes in social interaction and neurochemistry in the rat. Psychopharmacology (Berl) 2004; 173: 318–325. ArticleCAS Google Scholar
Lipska BK, Weinberger DR . To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000; 23: 223–239. ArticleCASPubMed Google Scholar
Hernandez L, Hoebel BG . Chronic clozapine selectively decreases prefrontal cortex dopamine as shown by simultaneous cortical, accumbens, and striatal microdialysis in freely moving rats. Pharmacol Biochem Behav 1995; 52: 581–589. ArticleCASPubMed Google Scholar
Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR . Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 2001; 156: 117–154. ArticleCASPubMed Google Scholar
Keith VA, Mansbach RS, Geyer MA . Failure of haloperidol to block the effects of phencyclidine and dizocilpine on prepulse inhibition of startle. Biol Psychiatry 1991; 30: 557–566. ArticleCASPubMed Google Scholar
Le Pen G, Moreau JL . Disruption of prepulse inhibition of startle reflex in a neurodevelopmental model of schizophrenia: reversal by clozapine, olanzapine and risperidone but not by haloperidol. Neuropsychopharmacology 2002; 27: 1–11. ArticleCASPubMed Google Scholar
Tamminga CA . The neurobiology of cognition in schizophrenia. J Clin Psychiatry 2006; 67 (Suppl 9): 9–13. CASPubMed Google Scholar
Jaaro-Peled H, Hayashi-Takagi A, Seshadri S, Kamiya A, Brandon NJ, Sawa A . Neurodevelopmental mechanisms of schizophrenia: understanding disturbed postnatal brain maturation through neuregulin-1-ErbB4 and DISC1. Trends Neurosci 2009; 32: 485–495. ArticleCASPubMedPubMed Central Google Scholar
Shi L, Fatemi SH, Sidwell RW, Patterson PH . Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003; 23: 297–302. ArticlePubMedPubMed Central Google Scholar
Decker MJ, Hue GE, Caudle WM, Miller GW, Keating GL, Rye DB . Episodic neonatal hypoxia evokes executive dysfunction and regionally specific alterations in markers of dopamine signalling. Neuroscience 2003; 117: 417–425. ArticleCASPubMed Google Scholar
Meyer U, Feldon J . Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia. Psychopharmacology (Berl) 2009; 206: 587–602. ArticleCAS Google Scholar
Romero E, Guaza C, Castellano B, Borrell J . Ontogeny of sensorimotor gating and immune impairment induced by prenatal immune challenge in rats: implications for the etiopathology of schizophrenia. Mol Psychiatry 2008; e-pub ahead of print 15 April 2008; doi:10.1038/mp.2008.44. ArticlePubMed Google Scholar
Nawa H, Takei N . Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci Res 2006; 56: 2–13. ArticleCASPubMed Google Scholar
Tohmi M, Tsuda N, Watanabe Y, Kakita A, Nawa H . Perinatal inflammatory cytokine challenge results in distinct neurobehavioral alterations in rats: implication in psychiatric disorders of developmental origin. Neurosci Res 2004; 50: 67–75. ArticleCASPubMed Google Scholar