Neuregulins 1, 2, and 3 Promote Early Neurite Outgrowth in ErbB4-Expressing Cortical GABAergic Interneurons
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Mei L, Xiong WC (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9(6):437–452
Mei L, Nave KA (2014) Neuregulin-ERBB signaling in the nervous system and neuropsychiatric diseases. Neuron 83(1):27–49
Buonanno A (2010) The neuregulin signaling pathway and schizophrenia: from genes to synapses and neural circuits. Brain Res Bull 83(3–4):122–131
Avramopoulos D (2018) Neuregulin 3 and its roles in schizophrenia risk and presentation. Am J Med Genet B Neuropsychiatr Genet 177(2):257–266
Greenwood TA, Lazzeroni LC, Murray SS, Cadenhead KS, Calkins ME, Dobie DJ, Green MF, Gur RE et al (2011) Analysis of 94 candidate genes and 12 endophenotypes for schizophrenia from the Consortium on the Genetics of Schizophrenia. Am J Psychiatry 168(9):930–946
Kao WT, Wang Y, Kleinman JE, Lipska BK, Hyde TM, Weinberger DR, Law AJ (2010) Common genetic variation in Neuregulin 3 (NRG3) influences risk for schizophrenia and impacts NRG3 expression in human brain. Proc Natl Acad Sci U S A 107(35):15619–15624
Mostaid MS, Lloyd D, Liberg B, Sundram S, Pereira A, Pantelis C, Karl T, Weickert CS et al (2016) Neuregulin-1 and schizophrenia in the genome-wide association study era. Neurosci Biobehav Rev 68:387–409
Fisher ML et al (2015) Role of the neuregulin signaling pathway in nicotine dependence and co-morbid disorders. Int Rev Neurobiol 124:113–131
Hayes LN, Shevelkin A, Zeledon M, Steel G, Chen PL, Obie C, Pulver A, Avramopoulos D et al (2016) Neuregulin 3 knockout mice exhibit behaviors consistent with psychotic disorders. Mol Neuropsychiatry 2(2):79–87
Silberberg G, Darvasi A, Pinkas-Kramarski R, Navon R (2006) The involvement of ErbB4 with schizophrenia: association and expression studies. Am J Med Genet B Neuropsychiatr Genet 141B(2):142–148
Law AJ, Kleinman JE, Weinberger DR, Weickert CS (2007) 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(2):129–141
Chung DW, Volk DW, Arion D, Zhang Y, Sampson AR, Lewis DA (2016) Dysregulated ErbB4 splicing in schizophrenia: selective effects on parvalbumin expression. Am J Psychiatry 173(1):60–68
Stefansson H, Petursson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J et al (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 71(4):877–892
Walsh T, McClellan JM, McCarthy SE, Addington AM, Pierce SB, Cooper GM, Nord AS, Kusenda M et al (2008) Rare structural variants disrupt multiple genes in neurodevelopmental pathways in schizophrenia. Science 320(5875):539–543
Neddens J, Buonanno A (2011) Expression of the neuregulin receptor ErbB4 in the brain of the rhesus monkey (Macaca mulatta). PLoS One 6(11):e27337
Vullhorst D, Neddens J, Karavanova I, Tricoire L, Petralia RS, McBain CJ, Buonanno A (2009) Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 29(39):12255–12264
Fazzari P, Paternain AV, Valiente M, Pla R, Luján R, Lloyd K, Lerma J, Marín O et al (2010) Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464(7293):1376–1380
Woo RS, Li XM, Tao Y, Carpenter-Hyland E, Huang YZ, Weber J, Neiswender H, Dong XP et al (2007) Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54(4):599–610
Batista-Brito R, Vinck M, Ferguson KA, Chang JT, Laubender D, Lur G, Mossner JM, Hernandez VG et al (2017) Developmental dysfunction of VIP interneurons impairs cortical circuits. Neuron 95(4):884–895 e9
Di Cristo G (2007) Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders. Clin Genet 72(1):1–8
Le Magueresse C, Monyer H (2013) GABAergic interneurons shape the functional maturation of the cortex. Neuron 77(3):388–405
Liu X, Bates R, Yin DM, Shen C, Wang F, Su N, Kirov SA, Luo Y et al (2011) Specific regulation of NRG1 isoform expression by neuronal activity. J Neurosci 31(23):8491–8501
Steinthorsdottir V, Stefansson H, Ghosh S, Birgisdottir B, Bjornsdottir S, Fasquel AC, Olafsson O, Stefansson K et al (2004) Multiple novel transcription initiation sites for NRG1. Gene 342(1):97–105
Zhang D, Frantz G, Godowski PJ (1998) New branches on the neuregulin family tree. Mol Psychiatry 3(2):112–115
Zhang D, Sliwkowski MX, Mark M, Frantz G, Akita R, Sun Y, Hillan K, Crowley C et al (1997) Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc Natl Acad Sci U S A 94(18):9562–9567
Wang JY, Miller SJ, Falls DL (2001) The N-terminal region of neuregulin isoforms determines the accumulation of cell surface and released neuregulin ectodomain. J Biol Chem 276(4):2841–2851
Vullhorst D, Ahmad T, Karavanova I, Keating C, Buonanno A (2017) Structural similarities between neuregulin 1-3 isoforms determine their subcellular distribution and signaling mode in central neurons. J Neurosci 37(21):5232–5249
Yarden Y, Sliwkowski MX (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2(2):127–137
Vullhorst D, Buonanno A (2019) NMDA receptors regulate neuregulin 2 binding to ER-PM junctions and ectodomain release. Mol Neurobiol 56:8345–8363
Vullhorst D, Mitchell RM, Keating C, Roychowdhury S, Karavanova I, Tao-Cheng JH, Buonanno A (2015) A negative feedback loop controls NMDA receptor function in cortical interneurons via neuregulin 2/ErbB4 signalling. Nat Commun 6:7222
Yan L, Shamir A, Skirzewski M, Leiva-Salcedo E, Kwon OB, Karavanova I, Paredes D, Malkesman O et al (2018) Neuregulin-2 ablation results in dopamine dysregulation and severe behavioral phenotypes relevant to psychiatric disorders. Mol Psychiatry 23(5):1233–1243
Lee KH, Lee H, Yang CH, Ko JS, Park CH, Woo RS, Kim JY, Sun W et al (2015) Bidirectional signaling of neuregulin-2 mediates formation of GABAergic synapses and maturation of glutamatergic synapses in newborn granule cells of postnatal hippocampus. J Neurosci 35(50):16479–16493
Longart M, Liu Y, Karavanova I, Buonanno A (2004) Neuregulin-2 is developmentally regulated and targeted to dendrites of central neurons. J Comp Neurol 472(2):156–172. https://doi.org/10.1002/cne.20016
Bartolini G, Sánchez-Alcañiz JA, Osório C, Valiente M, García-Frigola C, Marín O (2017) Neuregulin 3 mediates cortical plate invasion and laminar allocation of GABAergic interneurons. Cell Rep 18(5):1157–1170
Wang YN, Figueiredo D, Sun XD, Dong ZQ, Chen WB, Cui WP, Liu F, Wang HS et al (2018) Controlling of glutamate release by neuregulin3 via inhibiting the assembly of the SNARE complex. Proc Natl Acad Sci U S A 115(10):2508–2513
Muller T et al (2018) Neuregulin 3 promotes excitatory synapse formation on hippocampal interneurons. EMBO J 37(17):e98858
Rahman A, Weber J, Labin E, Lai C, Prieto AL (2019) Developmental expression of neuregulin-3 in the rat central nervous system. J Comp Neurol 527(4):797–817
Yau HJ et al (2003) 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(3):252–264
Bean JC, Lin TW, Sathyamurthy A, Liu F, Yin DM, Xiong WC, Mei L (2014) Genetic labeling reveals novel cellular targets of schizophrenia susceptibility gene: distribution of GABA and non-GABA ErbB4-positive cells in adult mouse brain. J Neurosci 34(40):13549–13566
Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JLR et al (2004) Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44(2):251–261
Li H, Chou SJ, Hamasaki T, Perez-Garcia CG, O’Leary DDM (2012) Neuregulin repellent signaling via ErbB4 restricts GABAergic interneurons to migratory paths from ganglionic eminence to cortical destinations. Neural Dev 7:10
Sun Y, Ikrar T, Davis MF, Gong N, Zheng X, Luo ZD, Lai C, Mei L et al (2016) Neuregulin-1/ErbB4 signaling regulates visual cortical plasticity. Neuron 92(1):160–173
Gu Y, Tran T, Murase S, Borrell A, Kirkwood A, Quinlan EM (2016) Neuregulin-dependent regulation of fast-spiking interneuron excitability controls the timing of the critical period. J Neurosci 36(40):10285–10295
Grieco SF et al (2019) Neuregulin and ErbB expression is regulated by development and sensory experience in mouse visual cortex. J Comp Neurol 528:419
Abe Y, Namba H, Kato T, Iwakura Y, Nawa H (2011) Neuregulin-1 signals from the periphery regulate AMPA receptor sensitivity and expression in GABAergic interneurons in developing neocortex. J Neurosci 31(15):5699–5709
Ting AK, Chen Y, Wen L, Yin DM, Shen C, Tao Y, Liu X, Xiong WC et al (2011) Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J Neurosci 31(1):15–25
Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y, Hines R, Ting AK, Craig AM et al (2008) ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem 283(47):32944–32956
Barros CS, Calabrese B, Chamero P, Roberts AJ, Korzus E, Lloyd K, Stowers L, Mayford M et al (2009) Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc Natl Acad Sci U S A 106(11):4507–4512
Chen Y, Fu AK, Ip NY (2008) Bidirectional signaling of ErbB and Eph receptors at synapses. Neuron Glia Biol 4(3):211–221
Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54(4):583–597
Yin DM, Sun XD, Bean JC, Lin TW, Sathyamurthy A, Xiong WC, Gao TM, Chen YJ et al (2013) Regulation of spine formation by ErbB4 in PV-positive interneurons. J Neurosci 33(49):19295–19303
Cahill ME, Remmers C, Jones KA, Xie Z, Sweet RA, Penzes P (2013) Neuregulin1 signaling promotes dendritic spine growth through kalirin. J Neurochem 126(5):625–635
Chen YJ, Zhang M, Yin DM, Wen L, Ting A, Wang P, Lu YS, Zhu XH et al (2010) ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc Natl Acad Sci U S A 107(50):21818–21823
Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ, Buonanno A (2012) The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci 32(9):2988–2997
Wen L, Lu YS, Zhu XH, Li XM, Woo RS, Chen YJ, Yin DM, Lai C et al (2010) Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 107(3):1211–1216
Cahill ME et al (2012) Control of interneuron dendritic growth through NRG1/erbB4-mediated kalirin-7 disinhibition. Mol Psychiatry 17(1):1 99-107
Liu Z, Gao W, Wang Y, Zhang W, Liu H, Li Z (2011) Neuregulin-1beta regulates outgrowth of neurites and migration of neurofilament 200 neurons from dorsal root ganglial explants in vitro. Peptides 32(6):1244–1248
Audisio C, Mantovani C, Raimondo S, Geuna S, Perroteau I, Terenghi G (2012) Neuregulin1 administration increases axonal elongation in dissociated primary sensory neuron cultures. Exp Cell Res 318(5):570–577
Bermingham-McDonogh O, McCabe KL, Reh TA (1996) Effects of GGF/neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development 122(5):1427–1438
Gerecke KM, Wyss JM, Carroll SL (2004) Neuregulin-1beta induces neurite extension and arborization in cultured hippocampal neurons. Mol Cell Neurosci 27(4):379–393
Chen Y, Hancock ML, Role LW, Talmage DA (2010) Intramembranous valine linked to schizophrenia is required for neuregulin 1 regulation of the morphological development of cortical neurons. J Neurosci 30(27):9199–9208
Zhang L, Fletcher-Turner A, Marchionni MA, Apparsundaram S, Lundgren KH, Yurek DM, Seroogy KB (2004) Neurotrophic and neuroprotective effects of the neuregulin glial growth factor-2 on dopaminergic neurons in rat primary midbrain cultures. J Neurochem 91(6):1358–1368
Modol-Caballero G et al (2017) Neuregulin 1 reduces motoneuron cell death and promotes neurite growth in an in vitro model of motoneuron degeneration. Front Cell Neurosci 11:431
Rieff HI, Raetzman LT, Sapp DW, Yeh HH, Siegel RE, Corfas G (1999) Neuregulin induces GABA(A) receptor subunit expression and neurite outgrowth in cerebellar granule cells. J Neurosci 19(24):10757–10766
Rieff HI, Corfas G (2006) ErbB receptor signalling regulates dendrite formation in mouse cerebellar granule cells in vivo. Eur J Neurosci 23(8):2225–2229
Gamett DC, Cerione RA (1994) Oncogenically activated or ligand-stimulated neu kinase stimulates neurite outgrowth in PC12 cells. FEBS Lett 351(3):335–339
Vaskovsky A, Lupowitz Z, Erlich S, Pinkas-Kramarski R (2000) ErbB-4 activation promotes neurite outgrowth in PC12 cells. J Neurochem 74(3):979–987
Villegas R, Villegas GM, Longart M, Hernández M, Maqueira B, Buonanno A, Garcı́a R, Castillo C (2000) Neuregulin found in cultured-sciatic nerve conditioned medium causes neuronal differentiation of PC12 cells. Brain Res 852(2):305–318
Tal-Or P, Erlich S, Porat-Shliom N, Goldshmit Y, Ben-Baruch G, Shaharabani E, Kloog Y, Pinkas-Kramarski R (2006) Ligand-independent regulation of ErbB4 receptor phosphorylation by activated Ras. J Cell Biochem 98(6):1482–1494
Nakano N, Kanekiyo K, Nakagawa T, Asahi M, Ide C (2016) NTAK/neuregulin-2 secreted by astrocytes promotes survival and neurite outgrowth of neurons via ErbB3. Neurosci Lett 622:88–94
Mizuno K, Carnahan J, Nawa H (1994) Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons. Dev Biol 165(1):243–256
Widmer HR, Hefti F (1994) Neurotrophin-4/5 promotes survival and differentiation of rat striatal neurons developing in culture. Eur J Neurosci 6(11):1669–1679
Rutherford LC, DeWan A, Lauer HM, Turrigiano GG (1997) Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J Neurosci 17(12):4527–4535
Vicario-Abejon C et al (1998) Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J Neurosci 18(18):7256–7271
Huang ZJ, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear MF, Maffei L, Tonegawa S (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98(6):739–755
Jin X, Hu H, Mathers PH, Agmon A (2003) Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J Neurosci 23(13):5662–5673
Berghuis P, Dobszay MB, Ibanez RM, Ernfors P, Harkany T (2004) Turning the heterogeneous into homogeneous: studies on selectively isolated GABAergic interneuron subsets. Int J Dev Neurosci 22(7):533–543
Pozas E, Ibanez CF (2005) GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45(5):701–713
Franchi SA et al (2017) A method to culture GABAergic interneurons derived from the medial ganglionic eminence. Front Cell Neurosci 11:423
Zagrebelsky M, Gödecke N, Remus A, Korte M (2018) Cell type-specific effects of BDNF in modulating dendritic architecture of hippocampal neurons. Brain Struct Funct 223(8):3689–3709
Ghashghaei HT, Weber J, Pevny L, Schmid R, Schwab MH, Lloyd KCK, Eisenstat DD, Lai C et al (2006) The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc Natl Acad Sci U S A 103(6):1930–1935
Prieto AL, O’Dell S, Varnum B, Lai C (2007) Localization and signaling of the receptor protein tyrosine kinase Tyro3 in cortical and hippocampal neurons. Neuroscience 150(2):319–334
Jiang M, Chen G (2006) High Ca2+-phosphate transfection efficiency in low-density neuronal cultures. Nat Protoc 1(2):695–700
Prieto AL, Weber JL, Lai C (2000) Expression of the receptor protein-tyrosine kinases Tyro-3, Axl, and Mer in the developing rat central nervous system. J Comp Neurol 425(2):295–314
Zhu X, Lai C, Thomas S, Burden SJ (1995) Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J 14(23):5842–5848
Solbach S, Celio MR (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat Embryol (Berl) 184(2):103–124
Kordeli E, Lambert S, Bennett V (1995) AnkyrinG. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 270(5):2352–2359
Bennett V, Lambert S (1999) Physiological roles of axonal ankyrins in survival of premyelinated axons and localization of voltage-gated sodium channels. J Neurocytol 28(4–5):303–318
Lim L, Mi D, Llorca A, Marín O (2018) Development and functional diversification of cortical interneurons. Neuron 100(2):294–313
Gottmann K, Mittmann T, Lessmann V (2009) BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp Brain Res 199(3–4):203–234
Rio C, Rieff HI, Qi P, Corfas G (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19(1):39–50
Elenius K, Corfas G, Paul S, Choi CJ, Rio C, Plowman GD, Klagsbrun M (1997) A novel juxtamembrane domain isoform of HER4/ErbB4. Isoform-specific tissue distribution and differential processing in response to phorbol ester. J Biol Chem 272(42):26761–26768
Xie F, Padival M, Siegel RE (2007) Association of PSD-95 with ErbB4 facilitates neuregulin signaling in cerebellar granule neurons in culture. J Neurochem 100(1):62–72
Perez-Garcia CG (2015) ErbB4 in laminated brain structures: a neurodevelopmental approach to schizophrenia. Front Cell Neurosci 9:472
Skirzewski M, Karavanova I, Shamir A, Erben L, Garcia-Olivares J, Shin JH, Vullhorst D, Alvarez VA et al (2018) ErbB4 signaling in dopaminergic axonal projections increases extracellular dopamine levels and regulates spatial/working memory behaviors. Mol Psychiatry 23(11):2227–2237
Steiner H, Blum M, Kitai ST, Fedi P (1999) Differential expression of ErbB3 and ErbB4 neuregulin receptors in dopamine neurons and forebrain areas of the adult rat. Exp Neurol 159(2):494–503
Zheng Y, Watakabe A, Takada M, Kakita A, Namba H, Takahashi H, Yamamori T, Nawa H (2009) Expression of ErbB4 in substantia nigra dopamine neurons of monkeys and humans. Prog Neuro-Psychopharmacol Biol Psychiatry 33(4):701–706
Gerecke KM, Wyss JM, Karavanova I, Buonanno A, Carroll SL (2001) ErbB transmembrane tyrosine kinase receptors are differentially expressed throughout the adult rat central nervous system. J Comp Neurol 433(1):86–100
Abe Y, Namba H, Zheng Y, Nawa H (2009) In situ hybridization reveals developmental regulation of ErbB1-4 mRNA expression in mouse midbrain: implication of ErbB receptors for dopaminergic neurons. Neuroscience 161(1):95–110
Cao SX, Zhang Y, Hu XY, Hong B, Sun P, He HY, Geng HY, Bao AM et al (2018) ErbB4 deletion in noradrenergic neurons in the locus coeruleus induces mania-like behavior via elevated catecholamines. Elife 7
Guo L, Stormmesand J, Fang Z, Zhu Q, Balesar R, van Heerikhuize J, Sluiter A, Swaab D et al (2019) Quantification of tyrosine hydroxylase and ErbB4 in the locus coeruleus of mood disorder patients using a multispectral method to prevent interference with immunocytochemical signals by neuromelanin. Neurosci Bull 35(2):205–215
Kataria H, Alizadeh A, Karimi-Abdolrezaee S (2019) Neuregulin-1/ErbB network: an emerging modulator of nervous system injury and repair. Prog Neurobiol 180:101643
Cespedes JC et al (2018) Neuregulin in health and disease. Int J Brain Disord Treat 4(1):024
Benes FM, Berretta S (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25(1):1–27
Heckers S, Stone D, Walsh J, Shick J, Koul P, Benes FM (2002) Differential hippocampal expression of glutamic acid decarboxylase 65 and 67 messenger RNA in bipolar disorder and schizophrenia. Arch Gen Psychiatry 59(6):521–529
Lewis DA, Hashimoto T, Morris HM (2008) Cell and receptor type-specific alterations in markers of GABA neurotransmission in the prefrontal cortex of subjects with schizophrenia. Neurotox Res 14(2–3):237–248
Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6(4):312–324
Gao R, Penzes P (2015) Common mechanisms of excitatory and inhibitory imbalance in schizophrenia and autism spectrum disorders. Curr Mol Med 15(2):146–167
Lauber E, Filice F, Schwaller B (2018) Parvalbumin neurons as a hub in autism spectrum disorders. J Neurosci Res 96(3):360–361
de Jonge JC, Vinkers CH, Hulshoff Pol HE, Marsman A (2017) GABAergic mechanisms in schizophrenia: linking postmortem and in vivo studies. Front Psychiatry 8:118
Dienel SJ, Lewis DA (2019) Alterations in cortical interneurons and cognitive function in schizophrenia. Neurobiol Dis 131:104208