Neuregulin-2 is synthesized by motor neurons and terminal Schwann cells and activates acetylcholine receptor transcription in muscle cells expressing ErbB4

Molecular and Cellular Neuroscience

Volumn 26, Issue 2, 2004, Pages 271-281

  Rimer, Mendell ^a,b   Prieto, Anne L ^c,d   Weber, Janet L ^c   Colasante, Cesare ^b,e   Ponomareva, Olga ^b   Fromm, Larry ^a,f   Schwab, Markus H ^c,g   Lai, Cary ^c   Burden, Steven J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d INDIANA UNIVERSITY   (United States)

^e Universidad De Los Andes Facultad de Medicina   (Venezuela)

^f BALL STATE UNIVERSITY   (United States)

^g MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEUREGULIN 1 RELATED PROTEIN; NEUREGULIN 2; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; MOTONEURON; MUSCLE CELL; MYOTUBE; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT; SCHWANN CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SYNAPSE; TRANSCRIPTION INITIATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; MOTOR NEURONS; MUSCLE FIBERS; MUSCLE, SKELETAL; NERVE GROWTH FACTORS; NEUROMUSCULAR JUNCTION; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-3; RECEPTORS, CHOLINERGIC; SCHWANN CELLS; SYNAPTIC MEMBRANES; TRANS-ACTIVATION (GENETICS);

EID: 2942661582     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2004.02.002     Document Type: Article

References (40)

1. Altiok N., Bessereau J.L., Changeux J.P. ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate. EMBO J. 14:1995;4258-4266
2. Bansal R., Pfeiffer S.E. Regulated galactolipid synthesis and cell surface expression in Schwann cell line D6P2T. J. Neurochem. 49:1987;1902-1911
3. Braissant O., Wahli W. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNAs on tissue sections. Biochemica. 1:1998;10-16
4. Busfield S.J., Michnick D.A., Chickering T.W., Revett T.L., Ma J., Woolf E.A., Comrack C.A., Dussault B.J., Woolf J., Goodearl A.D., Gearing D.P. Characterization of a neuregulin-related gene, Don-1, that is highly expressed in restricted regions of the cerebellum and hippocampus. Mol. Cell. Biol. 17:1997;4007-4014
5. Carraway K.L. III, Sweeney C. Localization and modulation of ErbB receptor tyrosine kinases. Curr. Opin. Cell Biol. 13:2001;125-130
6. Carraway K.L. III, Weber J.L., Unger M.J., Ledesma J., Yu N., Gassmann M., Lai C. Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature. 387:1997;512-516
7. Chang H., Riese D.J. II, Gilbert W., Stern D.F., McMahan U.J. Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature. 387:1997;509-512
8. Cohen I., Rimer M., Lomo T., McMahan U.J. Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. [published erratum appears in Mol. Cell. Neurosci. 1997;10(3-4):208] Mol. Cell. Neurosci. 9:1997;237-253
9. Corfas G., Rosen K.M., Aratake H., Krauss R., Fischbach G.D. Differential expression of ARIA isoforms in the rat brain. Neuron. 14:1995;103-115
10. DeChiara T.M., Bowen D.C., Valenzuela D.M., Simmons M.V., Poueymirou W.T., Thomas S., Kinetz E., Compton D.L., Rojas E., Park J.S., Smith C., DiStefano P.S., Glass D.J., Burden S.J., Yancopoulos G.D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 85:1996;501-512
11. 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. 72:1993;801-815
12. Fischbach G.D., Rosen K.M. ARIA: a neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20:1997;429-458
13. Gautam M., Noakes P.G., Moscoso L., Rupp F., Scheller R.H., Merlie J.P., Sanes J.R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 85:1996;525-535
14. Glass D.J., Bowen D.C., Stitt T.N., Radziejewski C., Bruno J., Ryan T.E., Gies D.R., Shah S., Mattsson K., Burden S.J., DiStefano P.S., Valenzuela D.M., DeChiara T.M., Yancopoulos G.D. Agrin acts via a MuSK receptor complex. Cell. 85:1996;513-523
15. Harari D., Tzahar E., Romano J., Shelly M., Pierce J.H., Andrews G.C., Yarden Y. Neuregulin-4: a novel growth factor that acts through the ErbB-4 receptor tyrosine kinase. Oncogene. 18:1999;2681-2689
16. Higashiyama S., Horikawa M., Yamada K., Ichino N., Nakano N., Nakagawa T., Miyagawa J., Matsushita N., Nagatsu T., Taniguchi N., Ishiguro H. A novel brain-derived member of the epidermal growth factor family that interacts with ErbB3 and ErbB4. J. Biochem. (Tokyo). 122:1997;675-680
17. Jo S.A., Zhu X., Marchionni M.A., Burden S.J. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature. 373:1995;158-161
18. Jones G., Meier T., Lichtsteiner M., Witzemann V., Sakmann B., Brenner H.R. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. U. S. A. 94:1997;2654-2659
19. Jones J.T., Akita R.W., Sliwkowski M.X. Binding specificities and affinities of egf domains for ErbB receptors. FEBS Lett. 447:1999;227-231
20. Karnovsky M.J. The localization of cholinesterase activity in rat cardiac muscle by electron microscopy. J. Cell Biol. 23:1964;217-232
21. McMahan U.J. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55:1990;407-418
22. Meyer D., Yamaai T., Garratt A., Riethmacher-Sonnenberg E., Kane D., Theill L.E., Birchmeier C. Isoform-specific expression and function of neuregulin. Development. 124:1997;3575-3586
23. Moscoso L.M., Chu G.C., Gautam M., Noakes P.G., Merlie J.P., Sanes J.R. Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle. Dev. Biol. 172:1995;158-169
24. Pinkas-Kramarski R., Shelly M., Guarino B.C., Wang L.M., Lyass L., Alroy I., Alimandi M., Kuo A., Moyer J.D., Lavi S., Eisenstein M., Ratzkin B.J., Seger R., Bacus S.S., Pierce J.H., Andrews G.C., Yarden Y., Alamandi M. ErbB tyrosine kinases and the two neuregulin families constitute a ligand-receptor network. [published errata appear in Mol. Cell. Biol. 1998 Dec; 18(12):7602 and 1999 Dec; 19(12):8695] Mol. Cell. Biol. 18:1998;6090-6101
25. Rimer M., Cohen I., Lomo T., Burden S.J., McMahan U.J. Neuregulins and erbB receptors at neuromuscular junctions and at agrin-induced postsynaptic-like apparatus in skeletal muscle. Mol. Cell. Neurosci. 12:1998;1-15
26. Salpeter M.M., Marchaterre M., Harris R. Distribution of extrajunctional acetylcholine receptors on a vertebrate muscle: evaluated by using a scanning electron microscope autoradiographic procedure. J. Cell Biol. 106:1988;2087-2093
27. Sandrock A.W. Jr., Dryer S.E., Rosen K.M., Gozani S.N., Kramer R., Theill L.E., Fischbach G.D. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science. 276:1997;599-603
28. Schaeffer L., de Kerchove d'Exaerde A., Changeux J.P. Targeting transcription to the neuromuscular synapse. Neuron. 31:2001;15-22
29. Schaeren-Wiemers N., Gerfin-Moser A. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry. 100:1993;431-440
30. Simmons D.M., Arriza J.L., Swanson L.W. A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labeled single-stranded RNA Probes. J. Histotechnol. 12:1989;169-181
31. Simon A.M., Burden S.J. An E box mediates activation and repression of the acetylcholine receptor delta-subunit gene during myogenesis. Mol. Cell. Biol. 13:1993;5133-5140
32. Simon A.M., Hoppe P., Burden S.J. Spatial restriction of AChR gene expression to subsynaptic nuclei. Development. 114:1992;545-553
33. Sweeney C., Lai C., Riese D.J. II, Diamonti A.J., Cantley L.C., Carraway K.L. III Ligand discrimination in signaling through an ErbB4 receptor homodimer. J. Biol. Chem. 275:2000;19803-19807
34. Trinidad J.C., Fischbach G.D., Cohen J.B. The agrin/MuSK signaling pathway is spatially segregated from the neuregulin/ErbB receptor signaling pathway at the neuromuscular junction. J. Neurosci. 20:2000;8762-8770
35. Woldeyesus M.T., Britsch S., Riethmacher D., Xu L., Sonnenberg- Riethmacher E., Abou-Rebyeh F., Harvey R., Caroni P., Birchmeier C. Peripheral nervous system defects in erbB2 mutants following genetic rescue of heart development. Genes Dev. 13:1999;2538-2548
36. Yamada K., Ichino N., Nishii K., Sawada H., Higashiyama S., Ishiguro H., Nagatsu T. Characterization of the human NTAK gene structure and distribution of the isoforms for rat NTAK mRNA. Gene. 255:2000;15-24
37. Yang X., Arber S., William C., Li L., Tanabe Y., Jessell T.M., Birchmeier C., Burden S.J. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron. 30:2001;399-410
38. Zhang D., Sliwkowski M.X., Mark M., Frantz G., Akita R., Sun Y., Hillan K., Crowley C., Brush J., Godowski P.J. Neuregulin-3 (NRG3): a novel neural tissue-enriched protein that binds and activates ErbB4. Proc. Natl. Acad. Sci. U. S. A. 94:1997;9562-9567
39. Zhao Y.Y., Feron O., Dessy C., Han X., Marchionni M.A., Kelly R.A. Neuregulin signaling in the heart. Dynamic targeting of erbB4 to caveolar microdomains in cardiac myocytes. Circ. Res. 84:1999;1380-1387
40. Zhu X., Lai C., Thomas S., Burden S.J. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J. 14:1995;5842-5848