Neuregulin induces GABA(A) receptor subunit expression and neurite outgrowth in cerebellar granule cells

Journal of Neuroscience

Volumn 19, Issue 24, 1999, Pages 10757-10766

  Rieff, Heather I ^a,d   Raetzman, Lori T ^b   Sapp, Douglas W ^c   Yeh, Hermes H ^c   Siegel, Ruth E ^b   Corfas, Gabriel ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Cerebellar granule cells; Cerebellum; ErbB receptors; GABA(A) receptors; Neuregulin; Neurite outgrowth; Neuronal differentiation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEU DIFFERENTIATION FACTOR; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; GRANULE CELL; IMMUNOCYTOCHEMISTRY; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0033573450     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-24-10757.1999     Document Type: Article

References (54)

1. Anton ES, Marchionni MA, Lee KF, Rakie P (1997) Role of GGF/ neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124:3501-3510.
2. A receptor subunit mRNA expression in cultured cerebellar granule neurons. J Neurosci 13:1784-1792.
3. A receptor subunit mRNAs in rat cerebellar granule neurons: importance of environmental cues. J Neurochem 66:1347-1353.
4. A receptors display association of gamma 2-subunit with alpha 1- and beta 2/3-subunits. J Biol Chem 266:4478-4483.
5. Bermingham-McDonogh O, McCabe K, Reh T (1996) Effects of GGF/ neuregulins on neuronal survival and neurite outgrowth correlate with erbB2/neu expression in developing rat retina. Development 122:1427-1438.
6. Bovolin P, Santi MR, Puia G, Costa E, Grayson D (1992) Expression patterns of gamma-aminobutyric acid type A receptor subunit mRNAs in primary cultures of granule neurons and astrocytes from neonatal rat cerebella. Proc Natl Acad Sci USA 89:9344-9348.
7. Canoll PD, Musacchio JM, Hardy R, Reynolds R, Marchionni MA, Salzer JL (1996) GGF/neuregulin is a neuronal signal that promotes the proliferation and survival and inhibits the differentiation of oligodendrocyte progenitors. Neuron 17:229-243.
8. Connolly C, Wooltorton J, Smart T, Moss S (1996) Subcellular localization of gamma-aminobutyric acid type A receptors is determined by receptor beta subunits. Proc Natl Acad Sci USA 9:9899-9904.
9. A receptor alpha-1 subunit tagged with green fluorescent protein requires a beta subunit for functional surface expression. J Biol Chem 273:28906-28911.
10. + channels in cultured chick muscle is increased by ARIA, an acetylcholine receptor-inducing activity. J Neurosci 13:2118-2125.
11. Corfas G, Falls DL, Fischbach GD (1993) ARIA, a protein that stimulates acetylcholine receptor synthesis, also induces tyrosine phosphorylation of a 185-kDa muscle transmembrane protein. Proc Natl Acad Sci USA 90:1624-1628.
12. Corfas G, Krauss R, Erickson CA, Wietasch K, Plowman G, Fischbach GD (1994) ARIA induces differentiation of PC12 cells. Soc Neurosci Abstr 20:669.
13. Corfas G, Rosen KM. Aratake H, Krauss R, Fischbach GD (1995) Differential expression of ARIA isoforms in the rat brain. Neuron 14:103-115.
14. Dong Z, Brennan A, Liu N, Yarden Y, Lefkowitz G, Kirsky R, Jessen KR (1995) Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat Schwann cell precursors. Neuron 15:585-596.
15. Elenius K, Corfas G, Subruto P, Choi CJ, Rio C, Plowman GD, Klagsbrun M (1997) A novel juxtamembrane domain isoform of HER4/ crbB4. J Biol Chem 272:26761-26768.
16. Ewert M, de Blas AL, Mohler H, Seeburg PH (1992) A prominent epitope on GABAA receptors is recognized by two different monoclonal antibodies. Brain Res 569:57-62.
17. 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.
18. Gamett D, Greene T, Wagreich A, Kim H, Koland J, Cerione R (1995) Heregulin-stimulated signaling in rat pheochromocytoma cells. Evidence for ErbB3 interactions with Neu/ErbB2 and p85. J Biol Chem 270:19022-19027.
19. A receptor delta subunit is selectively modulated by depolarization in cultured rat cerebellar granule neurons. J Neurosci 17:2391-2399.
20. Ginty D, Kornhauser J, Thompson M, Bading H, Mayo K, Takahashi J, Greenberg M (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260:238-241.
21. Harris DA, Falls DL, Dill-Devor RM, Fischbach GD (1988) Acetylcholine receptor-inducing factor from chicken brain increases the level of mRNA encoding the receptor alpha subunit. Proc Natl Acad Sci USA 85:1983-1987.
22. Holmes WE, Sliwkowski MX, Akita RW, Henzel WJ, Lee J, Park JW, Yansura D, Abadi N, Raab H, Lewis GD, Shepard HM, Kuang W-J, Wood WI, Goeddel DV, Vandlen RL (1992) Identification of heregulin, a specific activator of p185erbB2. Science 256:1205-1210.
23. A receptors. Neuron 3:745-753.
24. A receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J Neurosci 12:1063-1076.
25. A receptor subunit mRNAs in the rat brain. II. Embryonic and postnatal development. J Neurosci 12:4151-4172.
26. Lemke G (1996) Neuregulins in development. Mol Cell Neurosci 7:247-262.
27. Lindholm D, Dechant G, Heisenberg CP, Thoenen H (1993) Brain-derived neurotrophic factor is a survival factor for cultured rat cerebellar granule neurons and protects them against glutamate-induced neurotoxicity. Eur J Neurosci 5:1455-1464.
28. Lindholm D, Hamner S, Zirrgiebel U (1997) Neurotrophins and cerebellar development. Perspect Dev Neurobiol 5:83-94.
29. A receptor subunits in cultured cerebellar granule neurons is dependent on the β2 subunit. Soc Neurosci Abstr 24:1832.
30. Marchionni MA, Goodearl ADJ, 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, Hsuam JJ, Totty NF, Otsu M, McBurney RN, Waterfield MD, Strootbent P, Gwynne D (1993) Glial growth factors are alternatively spliced erbB2 ligands expressed in the nervous system. Nature 362:312-318.
31. Martinou J-C, Falls DL, Fischbach GD, Merlie JP (1991) Acetylcholine receptor-inducing activity stimulates expression of the ∈-subunit gene of the muscle acetylcholine receptor. Proc Natl Acad Sci USA 88:7669-7673.
32. Ozaki M, Sasner M, Yano R, Lu HS, Buonanno A (1997) Neuregulin-β induces expression of an NMDA-rcceptor subunit. Nature 390:691-694.
33. 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 kd glycoprotein that induces differentiation of mammary tumor cells. Cell 69:205-216.
34. A receptor subunits in the rat CNS. J Comp Neurol 326:193-216.
35. 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.
36. 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.
37. Plowman GD, Culouscou J, Whitney GS, Green JM, Carlton GW, Foy L, Neubauer MG, Shoyab M (1993) Ligand-specific activation of HER4/ p180erbB4, a fourth member of the epidermal growth factor receptor family. Proc Natl Acad Sci USA 90:1746-1750.
38. Raetzman LT, Siegel RE (1999) Immature granule neurons from cerebella of different ages exhibit distinct developmental potentials. J Neurobiol 38:559-570.
39. Rio C, Rieff HI, Qi P, Khurana TJ, Corfas G (1997) Neuregulin and crbB receptors play a critical role in neuronal migration. Neuron 19:39-50.
40. Sandrock AJ, Dryer S, Rosen K, Gozani S, Kramer R, Theill L, Fischbach G (1997) Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 276:599-603.
41. Sandrock AWJ, Goodearl AD, Yin QW, Chang D, Fischbach GD (1995) ARIA is concentrated in nerve terminals at neuromuscular junctions and at other synapses. J Neurosci 15:6124-6136.
42. Segal RA, Takahashi H, McKay R (1992) Changes in neurotrophin responsiveness during the development of cerebellar granule neurons. Neuron 9:1041-1052.
43. Segal RA, Pomeroy SL, Stiles CD (1995) Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J Neurosci 15:4970-4981.
44. A receptor subunits exist in distinct neuronal subpopulations. Neuron 5:703-771.
45. Sundstrom P, Deborah S, Sypherd P (1990) Sequence analysis and expression of two genes for elongation factor 1-alpha from the dimorphic yeast Candida albician. J Bacteriol 172:2036-2042.
46. Taberno A, Stewart HJS, Jessen KR, Mirsky R (1998) The neuron-glia signal β-neuregulin induces sustained CREB phosphorylation on Ser133 in cultured rat Schwann cells. Mol Cell Neurosci 10:309-322.
47. Vartanian T, Corfas G, Li Y, Fischbach GD, Stefansson K (1994) A role for the acetylcholine receptor-inducing protein ARIA in oligodendrocyte development. Proc Natl Acad Sci USA 91:11626-11630.
48. Watanabe M, Inoue Y, Sakimura K, Mishina M (1992) Developmental changes in distribution of NMDA receptor channel subunit mRNAs. NeuroReport 3:1138-1140.
49. Watanabe M, Mishina M, Inoue Y (1994) Distinct spatiotemporal expressions of five NMDA receptor channel subunit mRNAs in the cerebellum. J Comp Neurol 343:513-519.
50. A receptor subunits with special reference to the cerebellum. Ann NY Acad Sci 757:506-515.
51. Yang X, Kuo Y, Devay P, Yu C, Role L (1998) A cysteine-rich isoform of neuregulin controls the levels of expression of neuronal nicotinic receptor channels during synaptogenesis. Neuron 20:255-270.
52. A receptor β subunit heterogeneity: functional expression of cloned cDNAs. EMBO J 8:1665-1670.
53. Yoshioka A, Ikegaki N, Williams M, Pleasure D (1996) Expression of N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptor genes in neuroblastoma, medulloblastoma, and other cells lines. J Neurosci Res 46:164-178.
54. Zhu XJ, Lai C, Thomas S, Burden SJ (1995) Neuregulin receptors, erbB3 and erhB4, are localized at neuromuscular synapses. EMBO J 14:5842-5848.