Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: Preferential expression by interneurons tangentially migrating from the ganglionic eminences

Cerebral Cortex

Volumn 13, Issue 3, 2003, Pages 252-264

  Yau, Hau Jie ^a   Wang, Hsiao Fang ^a   Lai, Cary ^b   Liu, Fu Chin ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NEU DIFFERENTIATION FACTOR; PARVALBUMIN; PROTEIN; PROTEIN DLX; PROTEIN ERB4; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN TISSUE; CELL COUNT; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; GABAERGIC SYSTEM; GANGLION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INTERNEURON; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROBE; SIGNAL TRANSDUCTION; TELENCEPHALON; WESTERN BLOTTING;

ANIMALS; CELL MOVEMENT; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; INTERNEURONS; NEUREGULINS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 0037369224     PISSN: 10473211     EISSN: None     Source Type: Journal    
DOI: 10.1093/cercor/13.3.252     Document Type: Article

References (84)

1. Adlkofer K, Lai C (2000) Role of neuregulins in glial cell development. Glia 29:104-111.
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
3. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353-363.
4. Anderson SA, Kaznowski CE, Horn C, Rubenstein JL, McConnell SK (2002) Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb Cortex 12:702-709.
5. Anton ES, Marchionni MA, Lee KF, Rakic P (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124:3501-3510.
6. Benes FM, Berretta S (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacology 25:1-27.
7. Bulfone A, Wang F, Hevner R, Anderson S, Cutforth T, Chen S, Menesés J, Pedersen R, Axel R, Rubenstein JL (1998) An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21:1273-1282.
8. Buonanno A, Fischbach GD (2001) Neuregulin and ErbB receptor signaling pathways in the nervous system. Curr Opin Neurobiol 11:287-296.
9. Burden S, Yarden Y (1997) Neuregulins and their receptors: a versatile signaling module in organogenesis and oncogenesis. Neuron 18:847-855.
10. Busfield SJ, Michnick DA, Chickering TW, Revett TL, Ma J, Woolf EA, Comrack CA, Dussault BJ, Wool J, Goodearl AD, Gearing DP (1997) Characterization of a neuregulin-related gene, Don-1, that is highly expressed in restricted regions of the cerebellum and hippocampus. Mol Cell Biol 17:4007-4014.
11. Calaora V, Rogister B, Bismuth K, Murray K, Brandt H, Leprince P, Marchionni M, Dubois-Dalcq M (2001) Neuregulin signaling regulates neural precursor growth and the generation of oligodendrocytes in vitro. J Neurosci 21:4740-4751.
12. Carraway KL, Weber JL, Unger MJ, Ledesma J, Yu N, Gassmann M, Lai C (1997) Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature 387:512-516.
13. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894-3906.
14. Chang H, Riese DJ, Gilbert W, Stern DF, McMahan UJ (1997) Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature 387:509-512.
15. + channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J Neurosci 19:9332-9345.
16. Corbin JG, Nery S, Fishell G (2001) Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci 4:1177-1182.
17. De Carlos JA, Lopez-Mascaraque L, Valverde F (1996) Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 16:6146-6156.
18. DeDiego I, Smith-Fernandez A, Fairen A (1994) Cortical cells that migrate beyond area boundaries: characterization of an early neuronal population in the lower intermediate zone of prenatal rats. Eur J Neurosci 6:983-997.
19. Elenius K, Paul S, Allison G, Sun J, Klagsbrun M (1997) Activation of HER4 by heparin-binding EGF-like growth factor stimulates chemotaxis but not proliferation. EMBO J 16:1268-1278.
20. Falls DL, Rosen KM, Corfas G, Lane WS, Fischbach GD (1993) ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell 72:801-815.
21. Garratt AN, Britsch S, Birchmeier C (2000) Neuregulin, a factor with many functions in the life of a Schwann cell. Bioessays 22:987-296.
22. Gassmann M, Lemke G (1997) Neuregulins and neuregulin receptors in neural development. Curr Opin Neurobiol 7:87-92.
23. Gassmann M, Golding J, Tsoni V, Lumsden A, Dixon M (2001) Role of ErbB4 receptor tyrosine kinase in vertebrate hindbrain development. Soc Neurosci Abstr 27:692.8.
24. Golding JP, Trainor P, Krumlauf R, Gassmann M (2001) Defects in pathfinding by cranial neural crest cells in mice lacking the neuregulin receptor ErbB4. Nat Cell Biol 2:103-109.
25. Goldman SA, Luskin MB (1998) Strategies utilized by migrating neurons of the postnatal vertebrate forebrain. Trends Neurosci 21:107-114.
26. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
27. Harari D, Tzahar E, Romano J, Shelly M, Pierce JH, Andrews GC, Yarden Y (1999) Neuregulin-4: a novel growth factor that acts through the ErbB-4 receptor tyrosine kinase. Oncogene 18:2681-2689.
28. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366.
29. Holmes WE, Sliwkowski MX, Akita RW, Henzel WJ, Lee J, Park JW, Yansura D, Abadi N, Raab H, Lewis GD, Shepard M, Wood WI, Goeddel DV, Vandlen RL (1992) Identification of heregulin, a specific activator of p185erbB2. Science 256:1205-1210.
30. Jimenez D, Lopez-Mascaraque LM, Valverde F, De Carlos JA (2002) Tangential migration in neocortical development. Dev Biol 244:155-169.
31. Kaplan DR, Miller FD (2000) Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol 10:381-391.
32. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
33. Knoll B, Drescher U (2002) Ephrin-As as receptors in topographic projections. Trends Neurosci 25:145-149.
34. Komurasaki T, Toyoda H, Uchida D, Morimoto S (1997) Epiregulin binds to epidermal growth factor receptor and ErbB4 and induces tyrosine phosphorylation of epidermal growth factor receptor, ErbB-2, ErbB-3 and ErbB-4. Oncogene 15:2841-2848.
35. Kornblum HI, Zurcher SD, Werb Z, Derynck R, Seroogy KB (1999) Multiple trophic actions of heparin-binding epidermal growth factor (HB-EGF) in the central nervous system. Eur J Neurosci 11:3236-3246.
36. Kornblum HI, Yanni DS, Easterday MC, Seroogy KB (2000) Expression of the EGF receptor family members ErbB2, ErbB3, and ErbB4 in germinal zones of the developing brain and in neurosphere cultures containing CNS stem cells. Dev Neurosci 22:16-24.
37. Lai C, Lemke G (1991) An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6:691-704.
38. Lauder JM, Han VK, Henderson P, Verdoorn T, Towle AC (1986) Prenatal ontogeny of the GABAergic system in the rat brain: an immunocytochemical study. Neuroscience 19:465-493.
39. Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 19:7881-7888.
40. Lenz S, Perney TM, Qin Y, Robbins E, Chesselet MF (1994) GABA-ergic interneurons of the striatum express the Shaw-like potassium channel Kv3.1. Synapse 18:55-66.
41. Letinic K, Zoncu R, Rakic P (2002) Origin of GABAergic neurons in the human neocortex. Nature 417:645-649.
42. Lewis DA, Levitt P (2002) Schizophrenia as a disorder of neurodevelopment. Annu Rev Neurosci 25:409-432.
43. 28K-positive D28K-POSitiVe systems in the telencephalon: ganglionic eminence, developing striatum and cerebral cortex. J Neurosci 12:674-690.
44. Liu XB, Jones EG (1996) Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. Proc Natl Acad Sci USA 93:7332-7336.
45. Liu Y, Ford B, Mann MA, Fischbach GD (2001) Neuregulins increase alpha7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. J Neurosci 21:5660-5669.
46. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
47. Marchionni MA, Goodearl AD, Chen MS, Bermingham-McDonogh O, Kirk C, Hendricks M, Danehy F, Misumi D, Sudhalter J, Kobayashi K, Wroblewski D, Lynch C, Baldassare M, Hiles I, Davis JB, Hsuan JJ, Totty NF, Otsu M, McBurney RN, Waterfield MD, Stroobant P, Gwynne D (1993) Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362:312-318.
48. Marin O, Rubenstein JL (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
49. Marin O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL (2001) Sorting of striatal and cortical interneurons regulated by semaphorinneuropilin interactions. Science 293:872-875.
50. Meyer D, Yamaai T, Garratt A, Riethmacher-Sonnenberg E, Kane D, Theill LE, Birchmeier C (1997) Isoform-specific expression and function of neuregulin. Development 124:3575-3586.
51. Mione MC, Cavanagh JF, Harris B, Parnavelas JG (1997) Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J Neurosci 17:2018-2029.
52. Nadarajah B, Parnavelas JG (2002) Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci 3:423-432.
53. Nadarajah B, Alifragis P, Wong RO, Parnavelas JG (2002) Ventricle-directed migration in the developing cerebral cortex. Nat Neurosci 5:218-224.
54. Ozaki M, Sasner M, Yano R, Lu HS, Buonanno A (1997) Neuregulin-beta induces expression of an NMDA-receptor subunit. Nature 390:691-694.
55. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363-1366.
56. Parnavelas JG (2000) The origin and migration of cortical neurones: new vistas. Trends Neurosci 23:126-131.
57. Peles E, Bacus SS, Koski RA, Lu HS, Wen D, Ogden SG, Levy RB, Yarden Y (1992) Isolation of the neu/HER-2 stimulatory ligand: a 44 kDa glycoprotein that induces differentiation of mammary tumor cells. Cell 69:205-216.
58. Pinkas-Kramarski R, Eilam R, Spiegler O, Lavi S, Liu N, Chang D, Wen D, Schwartz M, Yarden Y (1994) Brain neurons and glial cells express Neu differentiation factor/heregulin: a survival factor for astrocytes. Proc Natl Acad Sci USA 91:9387-9391.
59. Pinkas-Kramarski R, Eilam R, Alroy I, Levkowitz G, Lonai P, Yarden Y (1997) Differential expression of NDF/neuregulin receptors ErbB-3 and ErbB-4 and involvement in inhibition of neuronal differentiation. Oncogene 15:2803-2815.
60. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL (2001) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740.
61. Plowman GD, Green JM, Culouscou JM, Carlton GW, Rothwell VM, Buckley S (1993) Heregulin induces tyrosine phosphorylation of HER4/p180erbB4. Nature 366:473-475.
62. Rakic P (1988) Specification of cerebral cortical areas. Science 241:170-176.
63. A receptor subunit expression and neurite outgrowth in cerebellar granule cells. J Neurosci 19:10757-10766.
64. Riese DJ, Bermingham Y, van Raaij TM, Buckley S, Plowman GD, Stern DF (1996) Betacellulin activates the epidermal growth factor receptor and erbB-4, and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-beta. Oncogene 12:345-353.
65. Rio C, Rieff HI, Qi P, Khurana TS, Corfas G (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19:39-50. [Published erratum appears in Neuron (1997) 19:1349.]
66. Shindler KS, Roth KA (1996) Double immunofluorescent staining using two unconjugated primary antisera raised in the same species. J Histochem Cytochem 44:1331-1335.
67. Shinozaki K, Miyagi T, Yoshida M, Miyata T, Ogawa M, Aizawa S, Suda Y (2002) Absence of Cajal-Retzius cells and subplate neurons associated with defects of tangential cell migration from ganglionic eminence in Emx1/2 double mutant cerebral cortex. Development 129:3479-3492.
68. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, Hjaltason O, Birgisdottir B, Jonsson H, Gudnadottir VG, Gudmundsdottir E, Bjornsson A, Ingvarsson B, Ingason A, Sigfusson S, Hardardottir H, Harvey RP, Lai D, Zhou M, Brunner D, Mutel V, Gonzalo A, Lemke G, Sainz J, Johannesson G, Andresson T, Gudbjartsson D, Manolescu A, Frigge ML, Gurney ME, Kong A, Gulcher JR, Petursson H, Stefansson K (2002) Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet (in press).
69. 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 159:494-503.
70. Stuhmer T, Puelles L, Ekker M, Rubenstein JL (2002) Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75-85.
71. Sweeney C, Lai C, Riese DJ, Diamonti AJ, Cantley LC, Carraway KL (2000) Ligand discrimination in signaling through an ErbB4 receptor homodimer. J Biol Chem 275:19803-19807.
72. Tamamaki N, Fujimori KE, Takauji R (1997) Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17:8313-8323.
73. Tan SS, Kalloniatis M, Sturm K, Tam PP, Reese BE, Faulkner-Jones B (1998) Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex. Neuron 21:295-304.
74. Van Eden CG, Mrzljak L, Voorn P, Uylings HB (1989) Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 289:213-227.
75. Wang H-F, Liu F-C (2001) Developmental restriction of the LIM homeodomain transcription factor Isl-1 expression to cholinergic neurons in the striatum. Neuroscience 103:999-1016.
76. Weber J, Ledesma E, Battenberg M, Morales M, Bloom FE, Lemke G, Lai C (1996) The erbB4 receptor is expressed in cells which express the neurotransmitter GABA. Soc Neurosci Abstr 22:1579.
77. Weber JL, Fung E, McCann C, Anton ES, Lai C (2000) Neuregulin and ErbB expression in the rostral migratory stream. Soc Neurosci Abstr 26:57.
78. Wen D, Peles E, Cupples R, Suggs SV, Bacus SS, Luo Y, Trail G, Hu S, Silbiger SM, Levy RB (1992) Neu differentiation factor: a trans-membrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell 69:559-572.
79. Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A (1999) Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 2:461-466.
80. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A (2001) In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128:3759-3771.
81. Wilson SW, Rubenstein JL (2000) Induction and dorsoventral patterning of the telencephalon. Neuron 28:641-651.
82. Yau H-J, Wang H-F, Lai C, Liu F-C (2001) Developmental expression of the neuregulin receptor ErbB4 in the rat forebrain. Soc Neurosci Abstr 27:473.1.
83. Yee KT, O'Leary DDM (2001) Migrating basilar pontine and inferior olive neurons express ErbB4. Soc Neurosci Abstr 27:692.7.
84. Zhang D, Sliwkowski MX, Mark M, Frantz G, Akita R, Sun Y, Hillan K, Crowley C, Brush J, Godowski PJ (1997) Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc Natl Acad Sci USA 94:9562-9567.